Connecting Global Priorities:

Biodiversity and Human Health

A State of Knowledge Review
Connecting Global Priorities:
Biodiversity and Human Health
A State of Knowledge Review
WHO Library Cataloguing-in-Publication Data

Connecting global priorities: biodiversity and human health: a state of knowledge review.

1.Biodiversity. 2.Global Health. 3.Public Health. 4.Socioeconomic Factors. 5.Communicable Disease Control. 6.Climate
Change. 7.Humans. I.World Health Organization. II.Convention on Biological Diversity.

ISBN 978 92 4 150853 7 (NLM classification: WD 600)

© World Health Organization and Secretariat of the Convention on Biological Diversity, 2015.

All rights reserved. Publications of the World Health Organization are available on the WHO web site (www.who.int) or can
be purchased from WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland (tel.: +41 22
791 3264; fax: +41 22 791 4857; e-mail: bookorders@who.int). Requests for permission to reproduce or translate WHO
publications – whether for sale or for noncommercial distribution – should be addressed to WHO Press through the WHO
web site (http://www.who.int/about/licensing/copyright_form/en/index.html ).

The designations employed and the presentation of the material in this publication do not imply the expression of any
opinion whatsoever on the part of the World Health Organization (WHO) nor on the part of the Secretariat of the
Convention on Biological Diversity (CBD) concerning the legal status of any country, territory, city or area or of its
authorities, or concerning the delimitation of its frontiers or boundaries. Dotted and dashed lines on maps represent
approximate border lines for which there may not yet be full agreement. Moreover, the views expressed do not represent
the decision or the stated policy of WHO or CBD. The citing of trade names and commercial processes do not constitute
endorsement by WHO or CBD.

The mention of specific companies or of certain manufacturers’ products, whether or not these have been patented, does
not imply that they are endorsed or recommended by WHO or CBD in preference to others of a similar nature that are not
mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters.

All reasonable precautions have been taken by WHO and CBD to verify the information contained in this publication.
However, the published material is being distributed without warranty of any kind, either expressed or implied. The
responsibility for the interpretation and use of the material lies with the reader. In no event shall the World Health
Organization nor the Secretariat of the Convention on Biological Diversity be liable for damages arising from its use.

Cover photo credits: (left to right) 1st row i) iStockphoto/pailoolom ii) Conor Kretsch iii) Glen Bowes 2nd row i) Danny Hunter
ii)Bioversity International iii) A.Camacho 3rd row i) Glen Bowes ii) Jon Betz / NGS iii) Barry Kretsch 4th row i) iStockphoto/
rssfhs ii) iStockphoto iii) Ecohealth Alliance

Editing and design by Inís Communication (www.iniscommunication.com)

CONOR KRETSCH

Acknowledgements
This volume was jointly prepared by the Secretariat of the Convention on Biological Diversity and the World
Health Organization, in collaboration with several partners including: Bioversity International, COHAB
Initiative,  DIVERSITAS, Ecohealth Alliance, Food and Agriculture Organization of the United Nations
(FAO),  Harvard School of Public Health (HSPH), Platform for Agrobiodiversity Research (PAR), United
Nations  University-Institute for Advanced Studies (UNU-IAS), United Nations  University -International
Institute for Global Health (UNU-IIGH), Wildlife Conservation Society, Health and Ecosystems Analysis of
Linkages (WCS-HEAL) and several other partners and experts.

The World Health Organization and the Secretariat of the Convention on Biological Diversity, wish to express
particular gratitude to the numerous authors and contributors to this volume without whom this unique volume
would not have been possible.

WHO and SCBD also wish to extend their gratitude to the following reviewers: Maria Purificacion Neira (WHO),
Sir Andy Haines (Chair of the The Lancet-Rockefeller Foundation Commission on Planetary Health), Carlo Blasi
(Sapienza University of Rome), Luiz Augusto Cassanha Galvão (PAHO), Ruth Charrondiere (FAO), Florence
Egal, Pablo Eyzaguirre (Bioversity International), Jessica Fanzo (Columbia University), Viviana Figueroa (CBD
Secretariat), Trevor Hancock (University of Victoria), Danna Leaman (IUCN, MPSG-SSC), Markus Lehmann
(CBD), Catherine Machalaba (EcoHealth Alliance), Keith Martin (CUGH), Jonathan Patz (Global Health Institute,
University of Wisconsin), Simone Schiele (CBD Secretariat), Cristina Tirado (UCLA), and the numerous Parties,
Governments and other peer reviewers who participated in two open peer review processes and in the final
consultation held at IUCN World Parks Congress in Sydney, Australia.

WHO and SCBD additionally wish to thank the following individuals and organizations: Flavia Bustreo (WHO)
Annie Cung (CBD), David Ainsworth (CBD), Didier Babin (CIRAD), Mateusz Banski (CBD), Charles Besancon
(CBD), Francesco Branca (WHO), Kathryn Campbell (Parks Victoria, Australia), Kimberly Chriscaden (WHO),
Stéphane de la Rocque (WHO/OIE), Carlos Francisco Dora (WHO), Beatriz Gomez Castro (CBD), Samantha
Collins (Bioversity International), Annie Cung (CBD), Jennifer Garard, Bruce Allan Gordon (WHO), Johan
Hedlund (CBD), Kahoru Kanari, Sakhile Koketso (CBD), Lina Mahy (WHO/SCN), Yukiko Maruyama (WHO),
Tanya McGregor (CBD), Christian Morris (CBD), Sabina Moya Huerta (WHO), Liz Mumford (WHO), Trang
Nguyen (Bioversity International), Steve Osofsky (WCS), Nada Osseiran (WHO), Michaela Pfeiffer (WHO),
Neil Pratt (CBD), Cathy Roth (WHO), Catalina Santamaria (CBD), Yahaya Sekagya, Negar Tayyar (UNU-IAS),
Billy Tsekos (CBD), Ann Tutwiler (Bioversity International), Kieran Noonan Mooney (CBD), Anthony Ramos
(EcoHealth Alliance), Shekar Saxena (WHO), Mohammad Taghi Yasamy (WHO), Stephan Weise (Bioversity
International), Sarah Whitmee (Lancet – Rockefeller Foundation Commission on Planetary Health), Ekaterina
Yakushina, Elena Villalobos (WHO), Qi Zhang (WHO), Camilla Zanzanaini (Bioversity International), United
Nations Food and Agriculture Organization (FAO), Alexander von Humboldt Institute, Australian National
University, Biodiversity Institute of Ontario, CONABIO, Global Crop Diversity Trust, Inís Communication,
Loyola Sustainability Research Centre (LSRC), International Union for the Conservation of Nature (IUCN), Parks
Victoria, Australia, Organization for Animal Health (OIE), TRAFFIC, and World Agroforestry Centre (ICRAF).

The production of the State of Knowledge Review was enabled through financial and in kind contributions from
the European Commission and the Government of France.

PAR
platform for
agrobiodiversity
research
 Chapter authors
Lead coordinating authors: Cristina Romanelli, David Cooper, Diarmid Campbell-Lendrum, Marina
Maiero, William B. Karesh, Danny Hunter and Christopher D. Golden

PART I

chapter  and chapter : Introduction to the state of knowledge review / Biodiversity and
human health linkages: concepts, determinants, drivers of change and approaches to integration
Lead authors: Cristina Romanelli, David Cooper, Marina Maiero, Diarmid Campbell-Lendrum, Elena
Villalobos, Johannes Sommerfeld and Mariam Otmani del Barrio
Contributing authors: William B. Karesh, Catherine Machalaba, Anne-Hélène Prieur-Richard, Daniel
Buss, Christopher D. Golden, and Lynne Gaffikin

PART II

chapter : Freshwater, wetlands, biodiversity and human health

Lead authors: Cristina Romanelli and Daniel Buss
Contributing authors: David Coates, Toby Hodgkin, Peter Stoett, and Ana Boischio

chapter : Biodiversity, air quality and human health

Lead authors: David Nowak, Sarah Jovan
Contributing authors: Cristina Branquinho, Sofia Augusto, Manuel C Ribeiro and Conor E. Kretsch

chapter : Agricultural biodiversity and food security

Lead authors: Toby Hodgkin and Danny Hunter
Contributing authors: Sylvia Wood, Nicole Demers

chapter : Biodiversity and nutrition

Lead authors: Danny Hunter, Barbara Burlingame, Roseline Remans
Contributing authors: Teresa Borelli, Bruce Cogill, Lidio Coradin, Christopher D. Golden, Ramni
Jamnadass, Katja Kehlenbeck, Gina Kennedy, Harriet Kuhnlein, Stepha McMullin, Samuel Myers,
Daniela Moura de Oliveira Beltrame, Alberto Jorge da Rocha Silva, Manika Saha, Lars Scheerer, Charlie
Shackleton, Camila Neves Soares Oliveira, Celine Termote, Corrado Teofili, Shakuntala Thilsted, and
Roberto Valenti.

chapter : Infectious diseases

Lead authors: William B. Karesh and Pierre Formenty
Contributing authors: Christopher Allen, Colleen Burge, Marcia Chame dos Santos, Peter Daszak,

iv Connecting Global Priorities: Biodiversity and Human Health

Piero Genovesi, Jacqueline Fletcher, Pierre Formenty, Drew Harvell, William B. Karesh, Richard Kock,
Elizabeth H. Loh, Juan Lubroth, Catherine Machalaba, Anne-Hélène Prieur-Richard, Kristine M. Smith,
Peter J. Stoett, and Hillary S. Young.

chapter : Environmental microbial diversity and noncommunicable diseases

Lead Authors: Graham A.W. Rook and Rob Knight

chapter : Biodiversity and biomedical discovery

Lead author: Aaron Bernstein

chapter : Biodiversity, health care & pharmaceuticals

Lead authors: Alistair B.A. Boxall and Conor E. Kretsch

chapter : Traditional medicine

Lead authors: Unnikrishnan Payyappallimana and Suneetha M. Subramanian
Contributing authors: Anastasiya Timoshyna, Bertrand Graz, Danna Leaman, Rainer W. Bussman,
Hariramamurthi G., Darshan Shankar, Charlotte I.E.A. van’t Klooster, Gerard Bodeker, Yahaya Sekagya,
Wim Hemstra, Felipe Gomez, Bas Verschuuren, Eileen de Ravin, James Ligare, Andrew M. Reid and
Leif M. Petersen

chapter : Contribution of biodiversity and green spaces to mental and physical fitness, and
cultural dimensions of health
Lead Authors: Pierre Horwitz and Conor Kretsch
Contributing Authors: Aaron Jenkins, Abdul Rahim bin Abdul Hamid, Ambra Burls, Kathryn Campbell,
May Carter, Wendy Henwood, Rebecca Lovell, Lai Choo Malone-Lee, Tim McCreanor, Helen Moewaka-
Barnes, Raul A. Montenegro, Margot Parkes, Jonathan Patz, Jenny J Roe, Cristina Romanelli, Katesuda
Sitthisuntikul, Carolyn Stephens, Mardie Townsend, Pam Wright

PART III

chapter : Climate change, biodiversity and human health

Lead authors: Cristina Romanelli, Anthony Capon, Marina Maiero, Diarmid Campbell-Lendrum
Contributing authors: Colin Butler, Carlos Corvalan, Rita Issa, Ro McFarlane, and M. Cristina Tirado-
von der Pahlen

chapter : Increasing resilience and disaster risk reduction: the value of biodiversity and
ecosystem approaches to resistance, resilience and relief
Lead Authors: R. David Stone, Emma Goring and Conor E. Kretsch

chapter : Population, consumption and the demand for resources; pathways to sustainability
Lead Authors: Cristina Romanelli, David Cooper

chapter : Integrating health and biodiversity: strategies, tools and further research
Lead Authors: David Cooper, Cristina Romanelli, Marina Maiero, Diarmid Campbell-Lendrum, Carlos
Corvalan and Lynne Gaffikin, Contributing authors: Kevin Bardosh, Daniel Buss, Emma Goring, William
B. Karesh, Conor Kretsch, Christopher D. Golden, Catherine Machalaba, Mariam Otmani del Barrio
and Anne-Hélène Prieur-Richard

Connecting Global Priorities: Biodiversity and Human Health v

 Table of Contents
Forewords _______________________________________ ix

Preface __________________________________________ xi

Executive Summary ________________________________ 1

Part I. Concepts, Themes & Directions

1. Introduction to the State of Knowledge 2. EQUITY AND SOCIAL DIMENSIONS OF
Review __________________________ 24 HEALTH AND BIODIVERSITY ____________30
3. BIODIVERSITY, ECOSYSTEM FUNCTIONS
2. Biodiversity and human health linkages: AND SERVICES ________________________33
concepts, determinants, drivers of 4. DRIVERS OF CHANGE __________________37
change and approaches to integration 28
5. INTEGRATING BIODIVERSITY AND HUMAN
1. BIODIVERSITY, HEALTH AND HEALTH: APPROACHES AND FRAMEWORKS 41
INTERACTIONS _______________________28
6. CONCLUSION: A THEMATIC APPROACH TO
COMMON LINKAGES __________________43

Part II. Thematic Areas in Biodiversity & Health

3. Freshwater, wetlands, biodiversity 4. Biodiversity, air quality and human
and human health _________________ 46 health ___________________________ 63
1. Introduction __________________________46 1. Introduction __________________________63
2. Water resources: an essential ecosystem 2. Air pollution and its effects on human health _63
service _______________________________47
3. Impacts of vegetation on air quality ________64
3. Dual threats to freshwater ecosystems
and human health ______________________49 4. The role of plant biodiversity in regulating
air quality_____________________________67
4. Impacts of agriculture on water
ecosystems and human health _____________54 5. Impacts of air quality on plant communities __71

5. Waterborne and water-related diseases ______56 6. Bioindicators __________________________72

6. Ways forward and additional considerations __61 7. Knowledge gaps and ways forward _________74

vi Connecting Global Priorities: Biodiversity and Human Health

5. Agricultural biodiversity, food 8. Environmental microbial diversity
security and human health _________ 75 and noncommunicable diseases ____ 150
1. Introduction __________________________75 1. Introduction _________________________150
2. Agricultural biodiversity _________________76 2. The ‘hygiene hypothesis’: the updated concept 150
3. Agricultural production, land use, ecosystem 3. Commensal microbiotas and environmental
services and human health _______________78 biodiversity __________________________153
4. Food production, food security and human 4. Loss of biodiversity: consequences for
health________________________________89 human health ________________________153
5. Conclusions ___________________________95 5. Commensal microbiota and
noncommunicable diseases ______________157
6. Biodiversity and Nutrition __________ 97 6. Ways forward: preliminary recommendations
1. Introduction __________________________97 for global and sectoral policy _____________159

2. Biodiversity and food composition _________99 9. Biodiversity and biomedical discovery164

3. Systems diversity and human nutrition_____102 1. Introduction _________________________164
4. Wild foods and human nutrition __________107 2. Why biodiversity matters to medical discovery 164
5. Biodiversity and traditional food systems ___112 3. Biodiversity, the microbiome and
6. Biodiversity and the nutrition transition ____114 antimicrobial resistance _________________167

7. Nutrition, biodiversity and agriculture in the 4. Future challenges: implications of

context of urbanization _________________117 biodiversity loss for medical discovery _____168

8. Food cultures: local strategies with global 5. Ways forward: conservation as a public
policy implications _____________________119 health imperative ______________________169

9. Mainstreaming biodiversity for food and 10. Biodiversity, health care

nutrition into public policies _____________122
& pharmaceuticals _______________ 170
10. Global policy initiatives ________________124
1. Introduction _________________________170
11. Ways forward: toward a post-2015
development agenda __________________127 2. Inputs and occurrence of active
pharmaceutical ingredients (APIs) _________172
7. Infectious diseases _______________ 130 3. Impacts of pharmaceuticals on biodiversity
and ecosystem services _________________174
1. Introduction and background ____________130
4. Future challenges: effects of social and
2. Infectious disease ecology and drivers ______132 environmental changes _________________177
3. Challenges and approaches ______________144 5. Ways forward: reducing the impact of APIs
in the environment ____________________179

Connecting Global Priorities: Biodiversity and Human Health vii

 11. Traditional medicine_____________ 180 12. Contribution of biodiversity and green
1. Introduction _________________________180 spaces to mental and physical fitness,
and cultural dimensions of health___ 200
2. Trends in demand for biological resources ___181
1. Introduction _________________________200
3. Traditional medicine and traditional
knowledge at a crossroads _______________188 2. Biodiversity and mental health ___________201

4. Strengthening traditional health practices 3. Biodiversity, green space, exercise and health _205
and addressing loss of resources __________189 4. The contribution of biodiversity to cultural
5. Challenges to the protection of traditional ecosystem services that support health and
medical knowledge ____________________193 well-being ___________________________212

6. Ways forward _________________________196 5. Conclusions and ways forward____________219

Part III: Cross-Cutting Issues, Tools & Ways Forward

13. Climate change, biodiversity and 4. Global trends to 2050 and pathways to
human health __________________ 222 sustainability _________________________254

1. Introduction _________________________222 5. Conclusion ___________________________257

2. Climate change challenges at the intersection 16. Integrating health and biodiversity:
of biodiversity and human health _________227
strategies, tools and further
3. Ways forward _________________________235 research _______________________ 258
4. Conclusion ___________________________236 1. Introduction _________________________258
2. Strategic objectives for the integration of
14. Increasing resilience and disaster risk biodiversity and human health ___________258
reduction: the value of biodiversity
and ecosystem approaches to 3. Priority interventions for the integration of
biodiversity and human health ___________261
resistance, resilience and relief ____ 238
4. Towards the development of common
1. Introduction _________________________238 metrics and approaches _________________263
2. Biodiversity and disaster risk reduction: 5: Keeping tabs: The need for monitoring and
prevention and mitigation _______________240 accountability for evidence-based indicators
3. Specific considerations for internally at the intersection of biodiversity and health 265
displaced persons and refugees ___________246 6. Assessing the economic value of biodiversity
and health: benefits and limitations _______266
15. Population, consumption and the
7. Shaping behaviour and engaging
demand for resources; pathways communities for transformational change __269
to sustainability ________________ 251
8. Research needs _______________________271
1. Introduction _________________________251
9. Integrating biodiversity and health into the
2. Current Trends and Alternatives __________252 sustainable development agenda __________272
3. Consumption – the demand for food and
energy ______________________________253

References ______________________________________ 276

viii Connecting Global Priorities: Biodiversity and Human Health

CONOR KRETSCH

Forewords
Foreword by the Executive Secretary of the Convention on Biological
Diversity
Biodiversity, ecosystems and the essential services to human life and to the surrounding environment
that they deliver are central pillars for all life on that sustains it. Increasing our knowledge of
the planet, including human life. They are sources these complex relationships at all scales, and the
of food and essential nutrients, medicines and influences by which they are mediated, enables
medicinal compounds, fuel, energy, livelihoods us to develop effective solutions capable of
and cultural and spiritual enrichment. They also strengthening ecosystem resilience and mitigating
contribute to the provision of clean water and air, the forces that impede their ability to deliver life-
and perform critical functions that range from supporting services. This state of knowledge
the regulation of pests and disease to that of review is a constructive step in this direction.
climate change and natural disasters. Each of these I am especially grateful to the World Health
functions has direct and indirect consequences for Organization and all partners and experts who
our health and well-being, and each an important generously contributed to bring this to fruition.
component of the epidemiological puzzle that
confront our efforts to stem the tide of infectious We must ensure that interventions made in the
and noncommunicable diseases. name of biodiversity, health or other sectors do
not compound but rather help to face the public
The inexorable links between biodiversity, health and conservation challenges posed by rising
ecosystems, the provision of these benefits and socio-demographic pressures, travel, trade and
human health are deeply entrenched in the the transformation of once natural landscapes
Strategic Plan for Biodiversity, and reflected in its into intensive agricultural zones and urban and
2050 Vision: “Biodiversity is valued, conserved, peri-urban habitats. We are all stakeholders
restored and wisely used, maintaining ecosystem in the pursuit of a healthier, more sustainable
services, sustaining a healthy planet and delivering planet capable of meeting the growing needs of
benefits essential for all people”. They are central to present and future generations. All sectors, policy-
our common agenda for sustainable development. makers, scientists, educators, communities and
citizens alike can – and must – contribute to the
As science continues to unravel our understanding development of common solutions to the common
of the vital links between biodiversity, its persistent threats that we face. Only in this way can we truly
loss, global health and development, we become pave the road toward a more equitable, and truly
better equipped to develop robust, coherent and sustainable, agenda in 2015 and beyond.
coordinated solutions that jointly reduce threats

Braulio Ferreira de Souza Dias

Executive Secretary, Convention on Biological Diversity Assistant Secretary General of the United Nations

Connecting Global Priorities: Biodiversity and Human Health ix

 Foreword by the Director, Public Health, Environmental and Social
Determinants of Health, World Health Organization
At WHO, we are aware of the growing body of epidemic infectious diseases such as the Ebola
evidence that biodiversity loss is happening virus; and the connection between biodiversity,
at unprecedented rates. There is increasing nutritional diversity and health. It also covers
recognition that this is a fundamental risk to the the potential benefits of closer partnerships
healthy and stable ecosystems that sustain all between conservation and health, from improved
aspects of our societies. surveillance of infectious diseases in wildlife and
human populations, to promoting access to green
Human health is not immune from this threat. All spaces to promote physical activity and mental
aspects of human wellbeing depend on ecosystem health. Of course, it also highlights the many areas
goods and services, which in turn depend on in which further research is needed.
biodiversity. Biodiversity loss can destabilize
ecosystems, promote outbreaks of infectious We hope this joint report will be able to help
disease, and undermine development progress, policy makers to recognize the intrinsic value of
nutrition security and protection from natural biodiversity and its role as a critical foundation
disasters. for sustainable development and human health
and well-being.
Protecting public health from these risks lies
outside of the traditional roles of the health In particular, we hope the report provides a useful
sector. It relies on working with partners engaged reference for the Sustainable Development Goals
in conservation, and the sustainable use and and post-2015 development agenda, which
management of natural resources. represents an unique opportunity to promote
integrated approaches to biodiversity and health
In this regard, WHO appreciates the leadership by highlighting that biodiversity contributes
that the Secretariat of the Convention on to human well-being, and highlighting that
Biological Diversity has shown in promoting the biodiversity needs protection for development to
linkages between biodiversity and health. be sustainable.

The report synthesizes the available information WHO looks forward to working jointly with our
on the most important inter-linkages; for example CBD colleagues, and the wider conservation
between biodiversity, ecosystem stability, and community, to support this important agenda.

Dr. Maria Neira

Director, Public Health, Environmental and Social Determinants of Health, World Health Organization

x Connecting Global Priorities: Biodiversity and Human Health

 Preface
GLEN BOWES

Preface by the Chair of the Rockefeller-Lancet Commission on

Planetary Health
The last 50 years have seen unprecedented improvements in human health, as measured by most
conventional metrics. This human flourishing has, however, been at the cost of extensive degradation
to the Earth’s ecological and biogeochemical systems. The impacts of transformations to these
systems; including accelerating climatic disruption, land degradation, growing water scarcity, fisheries
degradation, pollution, and biodiversity loss; have already begun to negatively impact human health.
Left unchecked these changes threaten to reverse the global health gains of the last several decades
and will likely become the dominant threat to health over the next century. But there is also much
cause for hope. The interconnected nature of people and the planet mean that solutions that benefit
both the biosphere and human health lie within reach. Improving the evidence base of links between
environment and health, identifying and communicating examples of co-benefits and building inter-
disciplinary relationships across research themes are key challenges which must be addressed, to help
build a post-2015 agenda where a healthy biosphere is recognised as a precondition for human health
and prosperity.

In response to these challenges, The Rockefeller Foundation and The Lancet, have formed a Commission
to review the scientific basis for linking human health to the underlying integrity of Earth’s natural
systems (The Commission on Planetary Health) and set out recommendations for action to the health
community and policymakers working in sectors that influence health, development and the biosphere.
The Commission has been underway since July 2014, and will conclude its work through the publication
of a peer-reviewed Commission Report in The Lancet in July 2015.

The Commission welcomes this timely and important State of Knowledge Review from the Convention
on Biological Diversity and the World Health Organization. The greatest challenge to protecting
Planetary Health over the coming century is to develop the capability of human civilisations, to interpret,
understand, and respond to the risks that we ourselves have created and this Review is a major advance
in our understanding of these risks and the benefits of actions to reduce them.

Professor Sir Andy Haines

Chair of the Lancet-Rockefeller Foundation Commission on Planetary Health and Professor of Public Health
and Professor of Primary Care at the London School of Hygiene and Tropical Medicine

Connecting Global Priorities: Biodiversity and Human Health xi

 Biodiversity and
Nutrition
Agricultural
Health “is a state of biodiversity
complete physical, mental
and social well-being and
not merely the absence of
disease or inƥrmityŚ.

Mental health

Biological diversity Food & Water

(biodiversity) is “the variability security
among living organisms from
all sources including, inter
alia, terrestrial, marine and
other aquatic ecosystems and
the ecological complexes of
which they are part; this
includes diversity within Sustainable Hea
species, between species and development outco
of ecosystems.Ś

Biomedical/
pharmaceutical
Biodiversity discovery
underpins ecosystem
functioning and the provision
of goods and services that are
essential to human health and Traditional
well being. medicine

The links between

biodiversity and
health are manifested at
various spatial and temporal Biodiv
scales. Biodiversity and
human health, and the
respective policies and
activities, are interlinked in
various ways.
 human health
Disaster risk
Direct drivers of
biodiversity loss include
Air quality land-use change, habitat loss,
over-exploitation, pollution,
invasive species and climate
change. Many of these drivers
Water quality aƤect human health directly
and through their impacts on
biodiversity.

Climate
change
Women and men
have diƤerent roles in the
conservation and use of
biodiversity and varying
health impacts.
alth
omes
Microbial
biodiversity
Ecosystems Human population
health is determined, to a
large extent, by social, eco-
nomic and environmental
factors.

Infectious
diseases

The social and

natural sciences are
important contributors to
biodiversity and health
research and policy. Integra-
tive approaches such as the
versity Ecosystem Approach, Eco-
health and One Health unite
diƤerent ƥelds and require
the development of mutual
understanding and coopera-
tion across disciplines.
 Executive Summary
GLEN BOWES

INTRODUCTION
1. Health “is a state of complete physical, 3. Biodiversity underpins ecosystem
mental and social well-being and functioning and the provision of goods
not merely the absence of disease or and services that are essential to human
infirmity”. This is the definition of the health and well-being. Ecosystems,
World Health Organization. Health status including our food production systems,
has important social, economic, behavioural depend on a whole host of organisms:
and environmental determinants and wide- primary producers, herbivores, carnivores,
ranging impacts. Typically health has been decomposers, pollinators, pathogens,
viewed largely in a human-only context. natural enemies of pests. Services provided
However, there is increasing recognition of by ecosystems include food, clean air and
the broader health concept that encompasses both the quantity and quality of fresh water,
other species, our ecosystems and the integral medicines, spiritual and cultural values,
ecological underpinnings of many drivers or climate regulation, pest and disease regulation,
protectors of health risks. and disaster risk reduction. Biodiversity is a
key environmental determinant of human
2. Biological diversity (biodiversity) is “the health; the conservation and the sustainable
variability among living organisms from use of biodiversity can benefit human health
all sources including, inter alia, terrestrial, by maintaining ecosystem services and by
marine and other aquatic ecosystems and maintaining options for the future.
the ecological complexes of which they are
part; this includes diversity within species, 4. The links between biodiversity and
between species and of ecosystems.” This health are manifested at various spatial
definition of the Convention on Biological and temporal scales. At a planetary scale,
Diversity (Article 2) reflects different levels ecosystems and biodiversity play a critical role
of biodiversity (including genetic diversity, in determining the state of the Earth System,
species and ecosystems) and the complexities regulating its material and energy flows and its
of biotic and abiotic interactions. The responses to abrupt and gradual change. At a
attributes and interactions of biotic and more intimate level, the human microbiota –
abiotic components determine ecosystem the symbiotic microbial communities present
processes and their properties. The effective on our gut, skin, respiratory and urino-genital
management of ecosystems as part of tracts, contribute to our nutrition, can help
comprehensive public health measures regulate our immune system, and prevent
requires that these various complex linkages infections.
and interactions be identified and understood.

Connecting Global Priorities: Biodiversity and Human Health 1

 5. Biodiversity and human health, and and economic processes. Social change and
the respective policies and activities, development trends (such as urbanization),
are interlinked in various ways. First, poverty and gender also influence these
biodiversity gives rise to health benefits. drivers of change. Macro-economic policies
For example, the variety of species and and structures and public policies that provide
genotypes provide nutrients and medicines. perverse incentives or fail to incorporate the
Biodiversity also underpins ecosystem value of biodiversity often compound the dual
functioning which provides services such as threat to biodiversity and public health.
water and air purification, pest and disease
control and pollination. However, it can also 7. Human population health is determined,
be a source of pathogens leading to negative to a large extent, by social, economic and
health outcomes. A second type of interaction environmental factors. Social determinants
arises from drivers of change that affect both of health include poverty, gender, sex, age,
biodiversity and health in parallel. For example, and rural versus urban areas. Vulnerable
air and water pollution can lead to biodiversity people, and groups (such as women and
loss and have direct impacts on health. A third the poor) who tend to be more reliant on
type of interaction arises from the impacts of biodiversity and ecosystem services suffer
health sector interventions on biodiversity disproportionately from biodiversity loss
and of biodiversity-related interventions and have less access to social protection
on human health. For example, the use of mechanisms (for example, access to
pharmaceuticals may lead to the release of healthcare). A social justice perspective is
active ingredients in the environment and needed to address the various dimensions of
damage species and ecosystems, which in turn equity in the biodiversity and health dynamic.
may have negative knock-on effects on human Vulnerability and adaptation assessments are
health. Protected areas or hunting bans could needed and should be tailored to the contexts
deny access of local communities to bushmeat of these populations.
and other wild sourcs of food and medicines
with negative impacts on health. Positive 8. Women and men have different roles in the
interactions of this type are also possible; for conservation and use of biodiversity and
example the establishment of protected areas varying health impacts. Access to, use, and
may protect water supplies with positive management of biodiversity has differential
health benefits. gender health impacts shaped by respective
cultural values and norms which in turn
6. Direct drivers of biodiversity loss include determine roles, responsibilities, obligations,
land-use change, habitat loss, over- benefits and rights. Institutional capacity and
exploitation, pollution, invasive species legal frameworks often inadequately reflect
and climate change. Many of these differential gender roles. There is also a lack
drivers affect human health directly and of gender disaggregated data on biodiversity
through their impacts on biodiversity. The access, use and control and on the differential
continued decline of biodiversity, including health impacts of biodiversity change.
loss or degradation of ecosystems, is reducing
the ability of biodiversity and ecosystems to 9. The social and natural sciences are
provide essential life-sustaining services and, important contributors to biodiversity
in many cases, leads to negative outcomes for and health research and policy. Integrative
health and well-being. Ecosystem degradation approaches, such as the ecosystem
may lead to both biodiversity loss and approach, ecohealth and One Health,
increased risk from infectious diseases. In unite different fields and require the
turn, the indirect drivers of biodiversity loss development of mutual understanding
are demographic change and large-scale social and cooperation across disciplines.

2 Connecting Global Priorities: Biodiversity and Human Health

 Multi-disciplinary research and approaches and quality of water supply but are themselves
can provide valuable insights on the drivers degraded by pollution.
of disease emergence and spread, contribute to
identifying previous patterns of disease risk, 10. Ecosystems provide clean water that
and help predict future risks through the lens underpin many aspects of human health.
of social-ecological systems. Such challenges All terrestrial and freshwater ecosystems
necessitate engagement of many stakeholders, play a role in underpinning the water cycle
including governments, civil society, and non- including regulating nutrient cycling and soil
governmental and international organizations. erosion. Many ecosystems can also play a role
Integrative approaches such as these make it in managing pollution; the water purification
possible to maximize resource efficiency as services they provide underpin water quality.
well as conservation, health and development Mountain ecosystems are of particular
outcomes. While their value is increasingly significance in this regard. Many protected
recognized for infectious disease prevention areas are established primarily to protect water
and control, their wider applications and supplies for people.
benefits can also extend to other areas. For
example, to the assessment of environmental 11. Freshwater ecosystems, such as rivers, lakes
health exposures and outcomes, better and wetlands, face disproportionately high
understanding of the health services provided levels of threats due largely to demands on
by biodiversity, and of how anthropogenic water and impacts of human activities such
changes to an ecosystem or biodiversity may as dam construction and mining. In some
influence disease risks. regions, up to 95% of wetlands have been lost
and two-thirds of the world’s largest rivers
are now moderately to severely fragmented
WATER, AIR QUALITY AND HEALTH by dams and reservoirs. Freshwater species
have declined at a rate greater than any other
biome, with the sharpest decline in tropical
freshwater biomes. More than one-third
of the accessible renewable freshwater on
earth is consumptively used for agriculture,
industrial and domestic use, which often leads
to chemical pollution of natural water sources.
Other human activity, such as mining, can also
lead to bioaccumulation and biomagnification.

12. Impaired water quality results in

ERIC SALES / ASIAN DEVELOPMENT BANK / FLICKR

significant social and economic costs.

Ecosystem degradation–for example through
eutrophication caused by excessive nutrients–
is a major cause of declines in water quality.
Left untreated, poor quality water results in
massive burdens on human health, with the
most pronounced impacts on women, children
Access to clean water is fundamental to human health and the poor. Maintaining or restoring healthy
and a priority for sustainable development. Yet, ecosystems (for example, through protected
almost 1 billion people lack access to safe drinking areas) is a cost-effective and sustainable way
water and 2 million annual deaths are attributable to to improve water quality while also benefitting
unsafe water, sanitation and hygiene. Biodiversity and biodiversity.
ecosystems play a major role in regulating the quantity

Connecting Global Priorities: Biodiversity and Human Health 3

 13. Water-related infrastructure has positive buildings, ecosystems in cities alter energy
and negative impacts on biodiversity, use and consequent greenhouse gas emissions;
livelihoods, and human health. Altered (3) Emissions – many ecosystems emit volatile
waterways (e.g. dams, irrigation canals, organic carbons (VOCs) including terpenes
urban drainage systems) can provide valuable and arenes. While sometimes considered
benefits to human communities, but may be as pollutants, many natural VOCs play a
costly to build and maintain, and in some critical role in atmospheric chemistry and air
cases increase risks (e.g. flood risk from coastal quality regulation. Ecosystems also release
wetlands degradation). They can also diminish pollen, sometimes associated with acute
native biodiversity and sometimes increase respiratory problems. Burning of vegetation
the incidence of water-borne or water-related is also associated with significant pollution
illnesses such as schistosomiasis. Approaches emissions.
integrating benefits of both physical/built
and natural infrastructure can provide more 15. Components of biodiversity can be used
sustainable and cost-effective solutions. as bioindicators of known human health
stressors, as well as in air and water quality
mapping, monitoring, and regulation.
Lichens are among the most widely utilized
and well-developed indicators of air quality
to date and are making headway as reliable
indicators for air quality regulation. The shift
in species is predictable and often correlates
UNDP BANGLADESH / FLICKR

highly with deposition measures, making

lichens an accurate, cost-effective tool for
mapping and monitoring. Other groups of
organisms with high local biological diversity
Air pollution is one of the most significant (e.g., insects and other arthropods) have high
environmental health risks worldwide, responsible for potential as bioindicators because they have
seven million deaths in 2012. Bronchial asthma and the capacity to provide more fine-grained
chronic obstructive pulmonary disease are on the rise. information about the state of ecosystems;
Cardiovascular disease, immune disorders, various they are also relatively easy to survey. Water
cancers, and disorders of the eye, ear, nose and throat quality can be monitored through chemical
are also affected by air pollution. Air pollution also analysis but long-term trends in freshwater
affects biodiversity; it can reduce plant biodiversity ecosystems are perhaps better monitored
and affect other ecosystem services, such as clean using the diversity of aquatic organisms (e.g.,
water and carbon storage. benthic invertebrates) as proxy for water
quality and ecosystem health.
14. Ecosystems may affect air quality and have
primarily beneficial outcomes for human
health. Ecosystems affect air quality in
three main ways: (1) Deposition – ecosystems
directly remove air pollution, through
absorption or intake of gases through leaves,
and through direct deposition of particulate
matters on plant surfaces; (2) Changes in
meteorological patterns – as ecosystems affect
local temperature, precipitation, air flows,
etc., they also affect air quality and pollutant
emissions. By altering climate and shading

4 Connecting Global Priorities: Biodiversity and Human Health

 BIODIVERSITY, FOOD control, nutrient cycling, erosion control and
PRODUCTION AND NUTRITION water supply.

17. The loss of diversity from agro-ecosystems

is increasing the vulnerability and reducing
the sustainability of many production
systems and has had negative effects
on human health. While there have been
significant increases in food production
through the introduction of higher yielding
uniform varieties and breeds, loss of genetic
diversity in production systems through
monocropping of uniform crop varieties or
animal breeds has led to instances of large
production losses and, in some cases, has had
significantly negative health consequences.
Loss of diversity has also resulted in the
reduced provision of regulating and supporting
ecosystem services, requiring additional
chemical inputs and creating negative feedback
loops.
BIOVERSITY

18. The use of chemical inputs, particularly

pesticides, has had severe negative
Agricultural productivity has increased substantially consequences for wildlife, human health
over the last 50 years yet some 800 million people and for agricultural biodiversity. While
are food insecure. It is estimated that by 2050 food the control of disease vectors such as malaria
production will have to feed over 9 billion people, many has generated health benefits, the use of
of whom will be wealthier and demand more food with pesticides, especially in agriculture, has led
proportionately more meat and dairy products that to serious environmental pollution, affected
have greater ecological footprints. human health (25 million people per year
suffer acute pesticide poisoning in developing
Biodiversity underpins the productivity and resilience countries) and caused the death of many
of agricultural and other ecosystems. However, land non-target animals, plants and fish. The use
use change and agriculture are dominant causes of of agricultural biodiversity to help cope with
biodiversity loss. pests and diseases and to increase soil quality
is a win-win option which produces benefits to
16. Biodiversity in and around agricultural human health and to biodiversity.
production systems makes essential
contributions to food security and health. 19. Pollination is essential to food security
Biodiversity is the source of the components generally and to the production of many
of production (crops, livestock, farmed fish), of the most nutritious foods in particular.
and the genetic diversity within these that Pollinators play a significant role in the
ensures continuing improvements in food production of approximately one third of
production, allows adaptation to current global food supply. Pollination also affects
needs and ensures adaptability to future ones. the quantity, nutritional content, quality, and
Agricultural biodiversity is also essential for variety of foods available. Global declines of
agricultural production systems, underpinning pollinator species diversity and in numbers
ecosystem services such as pollination, pest of pollinators have critical implications for

Connecting Global Priorities: Biodiversity and Human Health 5

 food security, agricultural productivity and, Malnutrition is the single largest contributor to the global
potentially, human nutrition. burden of disease affecting citizens of every country in
the world from the least developed to the most. Two
20. Increasing sustainable production and billion people are estimated to be deficient in one or more
meeting the challenges associated with micronutrients. At the same time, the consumption of
climate change will require the increased poor-quality processed foods, together with low physical
use of agricultural biodiversity. Climate activity, has contributed to the dramatic emergence of
change is already having an impact the obesity and associated chronic diseases.
nutritional quality and safety of food and
increasing the vulnerability of food insecure
individuals and households. The increased
use of agricultural biodiversity will play an
essential part in the adaptation and mitigation
actions needed to cope with climate change
and ensuring continued sustainable supplies
of healthy food, providing adaptive capacity,
diverse options to cope with future change

B. VINCETI / BIOVERSITY
and enhanced resilience in food production
systems.

A diversity of species, varieties and breeds, as

well as wild sources (fish, plants, bushmeat,
insects and fungi) underpins dietary diversity
and good nutrition. Variety-specific differences
within staple crops can often be the difference
between nutrient adequacy and nutrient
deficiency in populations and individuals.
Significant nutrient content differences in meat
S. PADULOSI / BIOVERSITY

and milk among breeds of the same animal species

have also been documented. Wildlife, from aquatic
and terrestrial ecosystems, is a critical source of
calories, protein and micronutrients like iron and
21. Agricultural practices, which make zinc for more than a billion people. Fish provide
improved use of agricultural biodiversity, more than 3 billion people with important sources
have been identified and are being used of protein, vitamins and minerals.
around the world. Their potential value needs
to be more widely recognized and their adoption 22. Access to wildlife in terrestrial, marine,
more strongly supported through research and and freshwater systems is critical to
support for appropriate policy and economic human nutrition, and global declines will
regimes, including appropriate support to present major public health challenges for
small-scale producers. Inter-disciplinary resource-dependent human populations,
analysis and cross-sectoral collaboration particularly in low- and middle- income
(among the agriculture, environment, health countries. Even a single portion of local
and nutrition communities) is essential to traditional animal-source foods may result
ensure the integration of biodiversity into in significantly increased clinical levels of
policies, programmes and national and energy, protein, vitamin A, vitamin B6/B12,
regional plans of action on food and nutrition vitamin D, vitamin E, riboflavin, iron, zinc,
security. magnesium and fatty acids–thus reducing
the risk of micronutrient deficiency. The use

6 Connecting Global Priorities: Biodiversity and Human Health

 of wild foods increases during the traditional nutrient deficiencies (e.g. vitamin A and
‘hungry season’ when crops are not yet ready iron), they cannot provide the full range of
for harvest, and during times of unexpected nutrients needed. Food based approaches can
household shocks such as crop failure or be supported by a greater focus on nutrition
illness. However, wildlife populations are and biological diversity in agricultural, food
in worldwide decline as a result of habitat system and value chain programs and policies
destruction, over-exploitation, pollution and (compared to a dominant focus on a few staple
invasive species. Conservation strategies can crops), including by promoting traditional
therefore provide significant public health food systems and food cultures.
dividends.
25. Some dietary patterns that offer substantial
23. The harvesting and trade of wild edible health benefits could also reduce climate
plants and animals provides additional change and pressures on biodiversity. The
benefits but also risks. The collection and global dietary transition towards diets higher
trade of wild foods indirectly contributes to in refined sugars, refined fats, oils and meats,
health and well-being by providing income for are increasing the environmental footprint
household needs, particularly in less developed of the food system and also increasing the
countries. Aggregating across numerous local incidence of type II diabetes, coronary heart
level studies, estimates of the annual value of disease and other chronic non-communicable
the bushmeat trade alone in west and central diseases. Some traditional diets, such as the
Africa range between US$42 and 205 million Mediterranean diet, and alternative vegetarian
(at 2000 values). This scale of economy poses or near-vegetarian diets, if widely adopted,
important subsistence benefits. Hunting, would reduce global agricultural greenhouse
butchering, consumption, global trade, and/ gas emissions, reduce land clearing and
or contact in markets with other species can resultant species extinctions, and help prevent
also presents risks of transmission and spread diet-related chronic non-communicable
of infectious disease diseases.

MICROBIAL DIVERSITY AND

NONCOMMUNICABLE DISEASES
S. LANDERSZ / BIOVERSITY

24. Food based approaches are needed to

help combat malnutrition and promote
NIAID / FLICKR

health. A healthy, balanced diet requires

a variety of foods to supply the full range
of nutrients needed (vitamins, minerals, Non-communicable diseases are becoming prevalent
individual amino acids and fatty acids, and in all parts of the world. Some NCDs including
other beneficial bioactive food components) autoimmune diseases, type 1 diabetes, multiple
sclerosis, allergic disorders, eczema, asthma,
While fortification and bio-fortification may inflammatory bowel diseases and Crohn’s disease may
be cost-effective solutions to address specific

Connecting Global Priorities: Biodiversity and Human Health 7

 be linked to depleted microbial diversity in the human 28. Several categories of organism with
microbiome. which we co-evolved play a role in setting
up the mechanisms that “police” and
26. Humans, like all complex plants and animals regulate the immune system. In addition
have microbiota without which they could to the microbiota, some other organisms
not survive. The human microbiome contains (the “Old Infections”) that caused persistent
ten times more microorganisms than cells that infections or carrier states in hunter-gatherer
comprise the human body. These occur inter communities were always present during
alia on the skin, and in the gut, airways and human evolution, and so had to be tolerated by
urogenital tracts. The biodiversity of bacteria, the immune system. Therefore they co-evolved
viruses, fungi, archaea and protozoa of which roles in inducing the mechanisms that regulate
microbes are comprised, and the interactions the immune system, terminate immune
of microbes within the complex human activity when it is no longer needed, and block
microbiome, influence both the physiology inappropriate attack on self (autoimmunity),
of and susceptibility to disease and play an allergens (allergic disorders) or gut contents
important role in the processes that link (inflammatory bowel disease). Some of these
environmental changes and human health. immunoregulation-inducing organisms,
The realization that humans are not merely for example a heavy load of helminths, can
“individuals”, but rather complex ecosystems have detrimental effects on health, and so
may be one of the major advances in our are eliminated by modern medicine in high-
understanding of human health in recent income settings. This increases the importance
years, with significant implications for both of the immunoregulatory role of microbiota
ecology and human health. and the microbial environment in high-income
settings, where these categories of organism
27. Environmental microbial ecosystems are need to compensate for loss of these “Old
in constant dialogue and interchange Infections”.
with the human symbiotic ecosystems. 
Microbes from the environment supplement 29. Reduced contact of people with the
and diversify the composition of the symbiotic natural environment and biodiversity and
microbial communities that we pick up biodiversity loss in the wider environment
from mothers and family, which in turn leads to reduced diversity in the human
play significant roles from a physiological microbiota, which itself can lead to immune
perspective.  Our physiological requirements dysfunction and disease. The immune
for microbial biodiversity are evolutionarily system needs an input of microbial diversity
determined. In addition to supplementation from the natural environment in order to
of the symbiotic microbiota by organisms from establish the mechanisms that regulate it.
the natural environment, the adaptability When this regulation fails there may be
of the human microbiota (for example, to immune responses to forbidden targets such
enable digestion of novel foods) depends as our own tissues (autoimmune diseases;
upon acquiring organisms with the relevant type 1 diabetes, multiple sclerosis), harmless
capabilities, or genes encoding necessary allergens and foods (allergic disorders,
enzymes from the environment by horizontal eczema, asthma, hay fever) or gut contents
gene transfer. Therefore, we need appropriate (inflammatory bowel diseases, ulcerative
contact with potential sources of genetic colitis, Crohn’s disease). Urbanization and
innovation and diversity, and our adaptability loss of access to green spaces are increasingly
is threatened by loss of biodiversity in the gene discussed in relation to these NCDs. Half of
reservoir of environmental microbes. the world’s population already lives in urban
areas and this number is projected to increase
markedly in the next half century, with the

8 Connecting Global Priorities: Biodiversity and Human Health

 most rapid increase in low- and middle- for deliberate modification and diversification
income countries. Combined, these findings of the microbiota, which is emerging as an
suggest an important opportunity for cross- exciting new approach to prevention and cure
over between health promotion and education of many human diseases.
on biodiversity.
32. Innovative design of cities and dwellings
30. Failing immunoregulatory mechanisms might be able to increase exposure to
partly attributable to reduced contact the microbial biodiversity that our
with the natural environment and physiological systems have evolved to
biodiversity lead to poor control of expect. In high-income settings several very
background inflammation. In high-income large studies reveal significant health benefits
urban settings, there is often continuous of living near to green spaces. The benefits
background inflammation even in the are greatest for people of low socioeconomic
absence of a specific chronic inflammatory status. Recent data suggest that the effect is
disorder. But persistently raised circulating not due primarily to exercise, and exposure
levels of inflammatory mediators predispose to environmental microbial biodiversity is a
to insulin resistance, metabolic syndrome, plausible explanation. This provides a strong
type 2 diabetes, obesity, cardiovascular medical rationale for increased provision of
disease and psychiatric disorders. Moreover, green spaces in modern cities. It might be
in high-income settings several cancers sufficient to supplement a few large green
rise in parallel with the increases in chronic spaces with multiple small green spaces that
inflammatory disorders, because chronic deliver appropriate microbial diversity.
inflammation drives mutation, and provides
growth factors and mediators that stimulate 33. Considering “microbial diversity” as
tumour vascularisation and metastasis. We an ecosystem service provider may
need to maintain the microbial biodiversity contribute to bridging the chasm between
of the environment in order to drive essential ecology and medicine/immunology, by
regulation of the immune system. considering microbial diversity in public
health and conservation strategies aimed
31. Understanding the factors that influence at maximizing services obtained from
functional and compositional changes in ecosystems. The relationships our individual
the human microbiome can contribute to bodies have with our microbiomes are a
the development of therapies that address microcosm for the vital relationships our
the gut microbiota and corresponding species shares with countless other organisms
diseases. Disturbances in the composition with which we share the planet.
and diversity of the gut microbiota are
associated with a wide range of immunological,
gastrointestinal, metabolic and psychiatric
disorders. The required microbial diversity is
obtained from the individual’s mother, from
other people and from animals (farms, dogs)
and the natural environment. The major
influences on this diversity are antibiotics,
diet, and diversity loss in the environment
due to urbanisation and modern agricultural
methods. We need to document the microbial
biodiversity and the causes of diversity loss,
preserve diversity, and identify the beneficial
organisms and genes. These may be exploited

Connecting Global Priorities: Biodiversity and Human Health 9

 INFECTIOUS DISEASES or distribution. Changes in land use and food
production practices are among leading drivers
of disease emergence in humans. At the same
time, pathogen dynamics are changing. While
pathogen evolution is a natural phenomenon,
factors such as global travel, climate change,
and use of antimicrobial agents are rapidly
affecting pathogen movement, host ranges,
and persistence and virulence. Beyond direct
infection risks for human and animals, such
changes also have implications for food

CSIRO
security and medicine.
Infectious diseases cause over one billion human
infections per year, with millions of deaths each year 36. Areas of high biodiversity may have high
globally. Extensive health and financial burden is seen numbers of pathogens, yet biodiversity
from both established and emerging infectious diseases. may serve as a protective factor for
Infectious diseases also affect plants and animals, which preventing transmission, and maintaining
may pose threats to agriculture and water supplies with ecosystems may help reduce exposure to
additional impacts on human health. infectious agents. While the absolute number
of pathogens may be high in areas of high
34. Pathogens play a complex role in biodiversity, disease transmission to humans
biodiversity and health, with benefits in is highly determined by contact, and in some
some contexts and threats to biodiversity cases, biodiversity may serve to protect against
and human health in others. The pathogen exposure through host species
relationships between infectious pathogens competition and other regulating functions.
and host species are complex; disease and Limiting human activity in biodiverse habitats
microbial composition can serve vital may reduce human exposure to high-risk
regulating roles in one species or communities settings for zoonotic pathogens while serving
while having detrimental effects on others. to protect biodiversity.
Microbial dynamics, and their implications
for biodiversity and health, are multifactorial; 37. Infectious diseases threaten wild species
similarly, the role of biodiversity in pathogen as well as the people that depend on them.
maintenance and not fully understood. The health burden of infectious diseases
is not limited to humans and domestic
35. Human-caused changes in ecosystems, species; infectious diseases pose threat to
such as modified landscapes, intensive biodiversity conservation as well. Pathogen
agriculture, and antimicrobial use, are spill-over can occur from one wild species
increasing infectious disease transmission to another, potentially causing an outbreak
risks and impact. Approximately two- if the species or population is susceptible to
thirds of known human infectious diseases the pathogen; similarly, diseases of domestic
are shared with animals, and the majority animals and humans can also be infectious
of recently emerging diseases are associated to wild species, as seen with the local
with wildlife. Vector-borne diseases also extinctions of African Wild Dog populations
account for a large share of endemic diseases. following the introduction of rabies virus
Increasing anthropogenic activity is resulting from domestic dogs. Ebola virus has also
in enhanced opportunities for contact at the been recognized as causing severe declines in
human/animal/environment interface that great ape populations, including the critically-
is facilitating disease spread, and through endangered wild lowland gorilla troops. Past
changing vector abundance, composition, and/ Ebola outbreaks in great apes have preceded

10 Connecting Global Priorities: Biodiversity and Human Health

 human outbreaks, suggesting a sentinel Many of the diseases that afflicted or killed most
or predictive value of wildlife monitoring people a century ago are today largely curable or
to aid in early detection or prevention of preventable today thanks to medicines, many of which
human infections. In addition to the direct are derived from biodiversity. Yet, in many instances,
potential morbidity and mortality threats the very organisms that have given humanity vital
from infectious diseases to the survival of insights into human diseases, or are the sources of
wild populations, infection-related population human medications, are endangered with extinction
declines may compromise health-benefitting because of human actions.
ecosystem services that wildlife provide. For
example, major declines recently seen from 39. Biodiversity has been an irreplaceable
fungal infections associated with White Nose resource for the discovery of medicines
Syndrome in North American bats and chytrid and biomedical breakthroughs that have
in amphibians may affect the pest control alleviated human suffering. Drugs derived
functions that these animals provide. from natural products may perhaps be the
most direct and concrete bond that many
38. The rapidly growing number of invasive may find between biodiversity and medicine.
species cause significant impacts on human Among the breakthroughs that dramatically
health, and this effect is expected to further improved human health in the twentieth
increase in the future, due to synergistic century, antibiotics rank near the top. The
effects of biological invasions and climate penicillins as well as nine of the thirteen
change. Preventing and mitigating biological other major classes of antibiotics in use,
invasions is not only is important to protecting derive from microorganisms. Between 1981
biodiversity, but can also protect human health. and 2010, 75% (78 of 104) of antibacterials
Through trade and travel, the number of invasive newly approved by the USFDA can be traced
species is increasing globally as a consequence back to natural product origins. Percentages
of the globalization of the economies, and the of antivirals and antiparasitics derived from
increase is expected to intensify in the future natural products approved during that same
due to synergistic effects with climate change. period are similar or higher. Reliance upon
Invasive species not only impact biodiversity, biodiversity for new drugs continues to this
but also affect human health causing diseases or day in nearly every domain of medicine.
infections, exposing humans to bites and stings,
causing allergic reactions, and facilitating the 40. For many of the most challenging health
spread of pathogens. problems facing humanity today, we look to
biodiversity for new treatments or insights
into their cures. Most of the medicinal
MEDICINES: THE CONTRIBUTION potential of nature potential has yet to be
OF BIODIVERSITY TO tapped. Plants have been the single greatest
THE DEVELOPMENT OF source of natural product drugs to date, and
PHARMACEUTICALS although an estimated 400,000 plant species
populate the earth, only a fraction of these
have been studied for pharmacologic potential.
One of the largest plant specimen banks, the
natural products repository at the National
Cancer Institute, contains ~60,000 specimens,
for instance. Other realms of the living world,
especially the microbial and marine, are only
beginning to be studied and hold vast potential
GENEVIÈVE ANDERSON

for new drugs given both their diversity and

the medicines already discovered from them.
Many species, potential sources of medicines
are threatened by extinction.

Connecting Global Priorities: Biodiversity and Human Health 11

 41. Greater even than what individual species contexts. Some traditional medical systems
offer to medicine through molecules are codified, and some even institutionalized.
they contain or traits they possess, an They range from highly developed ways of
understanding of biodiversity and ecology perception and understanding, classification
yield irreplaceable insights into how life systems (local-taxonomies) to metaphysical
works that bear upon current epidemic precepts. Links to geography, community,
diseases. Consider the multiple pandemics worldviews, biodiversity and ecosystems based
that have resulted from antibiotic resistance. on specific epistemologies make traditional
Human medicine tends to use a paradigm for health practices diverse and unique. By
treating infections unknown in nature which extension, level of expertise is heterogeneous
is treating one pathogen with one antibiotic. and therefore internal validation methods
Most multicellular life (and a good share of differ substantially despite an underlying
single cellular life) produces compounds with philosophical principle of interconnectedness
antibiotic properties but never uses them in of social and natural worlds.
isolation. Infections are attacked, or more
often prevented, through the secretion of 43. Medicinal and aromatic plants, the great
several compounds at once. majority of which are sourced from the
wild, are used in traditional medicine and
also in the pharmaceutical, cosmetic and
TRADITIONAL MEDICINE food industries. The global use and trade
in medicinal plants and other biological
resources, including wildlife, is high and
growing. Plants used in traditional medicine
are not only important in local health care, but
are important to innovations in healthcare
and associated international trade; they
enter various commodity chains based on
information gathered from their use in
traditional medical pharmacopeia. Globally,
an estimated 60,000 species are used for
C. KRESTCH

their medicinal, nutritional and aromatic

properties, and every year more than 500,000
Millions of people rely on traditional medicine tons of material from such species are traded.
that is dependent on biological resources, well It is estimated that the global trade in plants
functioning ecosystems and on the associated context for medicinal purposes reaches a value of over
specific knowledge of local health practitioners. In 2,5 billion USD and is increasingly driven by
local communities, health practitioners trained in industry demand.
traditional and non–formal systems of medicine often
44. Threats to medicinal plants, animals and
play a crucial role in linking health-related knowledge
other medicinal resources are increasing.
to affordable healthcare delivery.
Wild plant populations are declining- one in
42. Traditional medical knowledge spans five species is estimated to be threatened with
various dimensions relating to medicines, extinction in the wild. Animals (amphibians,
food and nutrition, rituals, daily routines reptiles, birds, mammals) used for food and
and customs. There is no single approach to medicine are more threatened than those
traditional medical knowledge. Traditional not used. Overharvesting, habitat alteration,
knowledge is not restricted to any and climate change are among major drivers
particular period in time, and constantly of declines in commercially important wild
undergoes re-evaluation based on local plant resources used for food and medicinal

12 Connecting Global Priorities: Biodiversity and Human Health

 purposes. These pose a threat both to the wild and promote existing tools, databases and
species and to the livelihoods of collectors, registers and intellectual property rights that
who often belong to the poorest social groups. are sensitive to community values.
There is a clear need to continue efforts at
developing assessment methods and indicators 47. Improving public health outcomes and
for conservation and sustainable use. achieving objectives of ‘Health for All’
and ‘Good Health at Low Cost’ should
45. Sustainable use of medicinal resources can include traditional medical care and the
provide multiple benefits to biodiversity, development of appropriate integrative
livelihoods and human health, in methodologies and safety standards
particular, relating to their affordability, within and across medical systems. More
accessibility and cultural acceptability. than one-third of the population in many
Sustainable medicinal resource management developing countries do not have access to
for both captive-breeding and wild-collection modern healthcare, and are dependent on
is crucial for the future of traditional medicine, traditional medical systems. There is a high
that involves all stakeholders including patronage of and dependence on traditional
conservationists, private healthcare sector, health practitioners to provide care to people
medical practitioners and its consumers. with inadequate access to modern health
Appropriate market-based instruments to infrastructure or with a preference for
enable sustainable and responsible utilization traditional systems. Pluralistic approaches
of resources in traditional medicine are that integrate natural resources and medical
required. Value chains of traditional medicines knowledge and are sensitive to local priorities
can be simple and local or global and extremely and contexts can enable better health
complex. Some resources have one or a few outcomes. This implies the need to develop
specific uses while others are used in many cross-sectoral, cost-effective measures to
different products and markets. In many cases test safety, efficacy and quality of traditional
the people who harvest these resources have medicines, the integration of traditional
little knowledge of the subsequent uses and healers in the healthcare system through
values. Ensuring equitable economic returns appropriate accreditation practices and
to local communities by promoting value processes, cross-learning between different
added activities at the local level could help to knowledge systems and disciplines through
harness the knowledge of local communities participatory, formal and informal learning
on medicinal resources and promote their processes to supplement current practices in
sustainable use. a culturally sensitive way.

46. Sui generis models may need to be

developed and applied to secure rights of BIODIVERSITY AND MENTAL,
indigenous peoples and local communities PHYSICAL AND CULTURAL WELL-
over traditional medical knowledge and BEING
related resources. Traditional medical
It is well established that biodiversity is a central
knowledge is often an inspiration for
component of many cultures and cultural traditions,
industrial R&D processes in bio-resource
and evidence that exposure to nature and more
based sectors, necessitating mechanisms to
biodiverse environments can also provide mental
secure appropriate attribution and sharing of
and physical health benefits. Over half of the world’s
rights and benefits with knowledge holders,
population lives in cities and that proportion is
as set out in the Nagoya Protocol on Access
increasing. There is a rising trend for people, especially
to genetic resources and equitable sharing
from poor communities, to be separated from nature
of benefits arising from their commercial
and be deprived of the physical, physiological and
utilization. It would be beneficial to strengthen
psychological benefits that nature provides.

Connecting Global Priorities: Biodiversity and Human Health 13

 has indicated that experience of nature can
reduce recuperation times and improve
recovery outcomes in hospital patients.

50. Access to natural green space can increase

levels of physical activity with benefits
for health. The benefits of physical activity
may include reduced risk of several non-
communicable diseases, as well as improved
immune function. It may also provide mental
GLEN BOWES

health benefits, and facilitate social connections

and independence. Among populations for
48. The interaction with nature – including which access to open countryside is limited,
domestic animals, and wild animals in wild particularly those in poorer inner-urban areas
settings – may contribute to treatments of large cities, access to green spaces in the
for depression, anxiety, and behavioural urban environment can encourage regular
problems, including for children. physical activity and improve life expectancy.
Exposure to nature is important to childhood It has also been suggested that health benefits
development, and children who grow up with may be more significantly attributable to
knowledge about the natural world and the enhanced exposure to environmental microbes
importance of conservation may be more in green spaces. There is evidence that
likely to conserve nature themselves as adults. biodiversity encourages use of urban green
Conversely, it has been stipulated that children spaces. Efforts to develop biodiverse settings,
in developed countries increasingly suffer from including wildlife-rich gardens, can also boost
a “nature-deficit disorder”, due to a reduction physical activity in sedentary and vulnerable
in the time spent playing outdoors as a result patients and residents. While, the potential
of increased use of technology and parental that green space can offer for promoting and
/ societal fears for child safety. On the other enhancing physical fitness is still not fully
hand, some research has suggested that some recognised, there is a growing interest in many
children, particularly those from urban areas, countries to promote and enhance “green and
are fearful of spending time in certain natural blue infrastructure” (terrestrial and aquatic
habitats (woodland and wetland) owing to environments) within tourism, public health
perceived threats from isolation, wild animals and environmental policies.
or the actions of other people.

49. Exposure to green space may have positive

impacts on mental health. Depression
accounts for 4.3% of the global burden of
disease and is among the largest single causes
of disability worldwide, particularly for women.
Some studies of populations in developed
countries have suggested that adults exposed
B. SHAPIT / BIOVERSITY

to green space report fewer symptoms and a

lower overall incidence of certain diseases than
others, and that the relationship is strongest
for mental illnesses such as depression, anxiety 51. Biodiversity is often central to cultures,
and stress. Similarly beneficial mental health cultural traditions and cultural well-
impacts have been associated with greater being. Species, habitats, ecosystems, and
exposure to microbial diversity. Other research landscapes influence forms of music, language,

14 Connecting Global Priorities: Biodiversity and Human Health

 art, literature and dance. They form essential IMPACTS OF PHARMACEUTICAL
elements of food production systems, PRODUCTS ON BIODIVERSITY AND
culinary traditions, traditional medicine,
rituals, worldviews, attachments to place and
CONSEQUENCES FOR HEALTH
community, and social systems. Use of the Antibiotics and other pharmaceuticals are essential
WHO Quality Of Life Assessment (devised to for human health and also play an important role
determine an individual’s quality of life in the in veterinary medicine. However, the release
context of their culture and value systems) has of active pharmaceutical ingredients into the
shown that the environmental domain is an environment can be harmful to biodiversity, with
important part of the quality of life concept. negative consequences for human health.
Socio-ecological production landscapes (e.g.
Satoyama in Japan) or conservation systems 54. The release of pharmaceuticals and
(e.g. sacred groves, ceremonial sites) or Active Pharmaceutical Ingredients
therapeutic landscapes (e.g. sacred healing (APIs) into the environment can have an
sites), and related traditional knowledge impact on biodiversity, ecosystems and
practices can have therapeutic value and ecosystem service delivery, and, may, in
contribute to health and well-being. turn negatively impact human health.
A range of pharmaceuticals, including
52. Significant changes to local biodiversity or hormones, antibiotics, anti-depressants
ecosystem sustainability can have specific and antifungal agents have been detected in
and unique impacts on local community rivers and streams across the world. Most
health where the physical health of a pharmaceuticals are designed to interact with
community is directly influenced by or a target (such as a specific receptor, enzyme,
dependent upon ecosystem services, or biological process) in humans and animals
particularly regarding access to diverse to deliver the desired therapeutic effect. If
food and medicinal species. Indigenous and these targets are present in organisms in
local communities often act as stewards of local the natural environment, exposure to some
living natural resources based on generations of pharmaceuticals might be able to elicit effects
accumulated traditional knowledge, including in those organisms. Pharmaceuticals can also
knowledge of agricultural biodiversity, cause side effects in humans and it is possible
and biodiversity that supports traditional that these and other side effects can also occur
medicinal knowledge. Where local traditions in organisms in the environment. During the
and cultural identity are closely associated life cycle of a pharmaceutical product, APIs
with biodiversity and ecosystem services, may be released to the natural environment,
declines in the availability and abundance of including during the manufacturing process
such resources can have a detrimental impact via human or domestic animal excretion
on community well-being, with implications into sewage systems, surface water or soils,
for mental and physical health, social welfare when contaminated sewage sludge, sewage
and community cohesion. effluent or animal manure is applied to
land. APIs may also be released into the soil
53. While many community-specific links environment when contaminated sewage
between health, culture and biodiversity sludge, sewage effluent or animal manure is
have been documented and measured, applied to land. Veterinary pharmaceuticals
much of the evidence for a more universal may also be excreted directly to soils by pasture
relationship is relatively sparse beyond animals. Measures are needed to reduce this
anecdotal accounts. However, there is environmental contamination.
growing recognition of the role of biodiversity
and ecosystem services in shaping broad 55. Antibiotic and antimicrobial use can
perspectives of quality of life. alter the composition and function of the

Connecting Global Priorities: Biodiversity and Human Health 15

 human microbiome and limiting their use perspective, the use of antimicrobials and
would provide biodiversity and health antibiotics may disrupt microbial composition,
co-benefits. Antibiotic use can dramatically including the relationships between hosts and
alter the composition and function of the their symbiotic microbes, and lead to diseases.
human microbiome. Although much of the At the same time, antibiotic resistance in
microbiome and its relationship to its host any environment can pose serious threats
remains unexplored, already apparent is that to public health. Aside from its potential to
changes to the variety and abundance of cultivate resistance, antibiotic use also carries
various microorganisms, as can occur with the potential to disrupt symbiotic bacterial
antibiotic use, may affect everything from composition.
the host’s weight and the risk of contracting
autoimmune disease, to susceptibility to 57. Endocrine disrupting chemicals found in
infections. The microbiome may also be able pharmaceuticals products and also in many
to affect mood and behaviour. The use of household, food and consumer products
antibacterial products and antibiotics may have adverse effects on the health of
also be linked to the increase in chronic terrestrial, freshwater and marine wildlife
inflammatory disorders, including allergies and human health. The use of contraceptive
such as asthma and eczema, because they hormones and veterinary growth hormones
reduce exposure to microbial agents that set up have been linked to endocrine disruption
the regulation of the immune system. Limiting and reproductive dysfunction in wildlife.
the use of antimicrobial agents could provide They also affect both male and female human
potential co-benefits for human health and reproduction, and have been linked to prostate
biodiversity, reducing chronic inflammatory cancer, neurological, endocrinological,
diseases through a healthy and more diverse thyroid, obesity, and cardiovascular problems.
human microbiota while also reducing the risk Biodiversity has also been a good monitor for
of emerging disease from antibiotic-resistant some of these human health problems. In
strains and the potential impacts of antibiotics some cases, health specialists were alerted
on ecosystems more broadly. to the scale of a potential problem through
changes originally recorded in wild fish
56. The inappropriate use of antibiotics in populations.
plants, animals, and humans has cultivated
numerous highly resistant bacterial 58. The inappropriate use of some non-
strains. In some instances, resistant bacterial steroidal anti-inflammatory drugs and
strains cannot be effectively treated with any other veterinary drugs threatens wildlife
currently available antibiotic. Promoting the populations. For example, in the 1980s,
responsible and prudent use of antibiotics and populations of three previously abundant
antimicrobials in human health, agricultural vulture species in South Asia were reduced to
practices and food production systems near extinction due to the use in livestock of
can achieve public health and biodiversity diclofenac, residues of which remained in the
co-benefits. Poorly managed industrial carcasses of treated animals. This led to negative
agricultural practices contribute to ecosystem impacts on human health through spread of
degradation, air and water pollution and soil diseases by feral dogs as access to carcasses
depletion and rely heavily on the inappropriate increased, especially among communities
use of antibiotics for both therapeutic as well who rely on vultures to consume their dead.
as prophylactic (growth promotion) use, which Following bans on the use of diclofenac and its
may lead to environmental dispersion of replacement by meloxicam, vulture population
antimicrobial agents, antibiotic resistance, and declines have slowed and some show signs of
reduced efficacy in subsequent use for medical recovery in the region. Without proper risk
or food production applications. From a health assessment and regulation the marketing and

16 Connecting Global Priorities: Biodiversity and Human Health

 use of pharmaceuticals used for livestock may there would be increased productivity at high
continue to pose threats to human and wildlife latitudes there will be decreased productivity
health. at low/mid latitudes, affecting poor developing
countries.
GLOBAL CHANGE ADAPTATION TO 61. Disasters may be precipitated by impacts
CLIMATE CHANGE AND DISASTER on critical ecosystems or the collapse of
RISK REDUCTION essential ecosystem services. Disasters
may include disease epidemics, flooding,
storm, extreme weather, and wildfires. Some
of these may be precipitated by ecosystem
disruption. There is an increase in frequency
AIRMAN 1ST CLASS CHERYL SANZI (USAF)

and intensity of some climate-related extreme

events. Ecosystem degradation can increase
the vulnerability of human populations to
such disasters. New environmental impacts
often occur during and after an emergency
with an increased demand for certain natural
59. Climate change is already negatively resources which can place additional stress
impacting on human health and these on specific ecosystems (such as groundwater
impacts are expected to intensify. Direct resources) and their functioning.
effects of climate change on health may
include stroke and dehydration associated 62. Competition over access to ecosystem
with heat waves (in particular in urban areas), goods and services can contribute to,
negative health consequences associated with and become a cause of, conflict, with
reduced air quality and the spread of allergens consequences that can negatively impact
Effects are also mediated through the impacts ecosystem goods and services in both the
on ecosystems and biodiversity. Such effects short- and long-term. Greater recognition
may include decreased food production and needs to be given to the potential positive role
changes in the spread of climate-sensitive that conservation and ecosystem management
waterborne and water-related, food-borne can play in conflict prevention and resolution
and vector-borne diseases. There may be and peace building, while the converse also
synergistic effects of climate change, land use holds.
change, pollution invasive species and other
drivers of change which can amplify impacts 63. The creation of disaster-resilient societies
on both health and biodiversity. is increasingly tied to and dependent upon
resilience in ecosystems, and sustainability
60. Climate change will not only affect and security in the flow and delivery of
agricultural production systems but also essential ecosystem goods and services
the nutritional content of foods and the – not only those directly associated with
distribution and availability of fisheries. resilience to immediate disaster impacts, but
Changes in temperature and precipitation also those that normally support communities
patterns will have complex effects, but the and wider society. Long-term health status is
net effect on food production will be negative. an important indicator of the resilience of
While rising levels of atmospheric carbon, a community – as a marker for capacity to
tend to increase productivity, they will lead overcome or adapt to health challenges and
to reduced concentrations of minerals such other social, environmental and economic
as zinc and iron in crops such as wheat and pressures. Communities whose ability to
rice. With regard to marine fisheries, while overcome current challenges are affected by

Connecting Global Priorities: Biodiversity and Human Health 17

 ecosystem degradation at the time of a disaster efficiency, including a decarbonization of
event – natural or man-made – are likely to be energy supplies this century. These changes
significantly more vulnerable to disasters than will need to be complemented by increased
communities with greater ecological security. equality in access to and use of energy and
other natural resources.
64. Biodiversity helps to improve resilience of
ecosystems, contributing to adaptation to 66. Alternative scenarios to 2050, as well as
climate change and moderating the impacts practical experience, demonstrate that it is
of disasters. Ecosystem-based adaptation and possible to secure food security and reduce
mitigation strategies are needed to build the poverty while also protecting biodiversity
resilience of managed landscapes and jointly and addressing climate change and attain
reduce the vulnerabilities of ecosystems and other human development goals, but that
communities reliant upon them for their this requires transformational change.
health, livelihoods and well-being. For example, Scenario analyses show that there are multiple
Ecosystem-based approaches to flood-plain plausible pathways to simultaneously achieve
and coastal development can reduce human globally agreed goals. Common elements of
exposure to risks from flooding. Coral reefs these pathways include: reducing greenhouse
are very effective in protecting against coastal gas emissions from energy and industry;
hazards (reducing wave energy by 97%) and increasing agricultural productivity and
protect over 100 million people in this way containing agricultural expansion to prevent
from coastal storm surges. The conservation further biodiversity loss and to avoid excessive
and use of genetic resources in agriculture, greenhouse gas emissions from conversion
aquaculture and forestry is important to of natural habitats; restoring degraded
allow crops, trees, fish and livestock to adapt land, protecting critical habitats; managing
to climate change. biodiversity in agricultural landscapes; reducing
nutrient and pesticide pollution and water use;
reducing post harvest losses in agriculture
SUSTAINABLE CONSUMPTION AND
and food waste by retailers and consumers
PRODUCTION as well as moderating the increase in meat
65. Increased pressure on the biosphere, driven consumption. Implementing these measures
by increasing human populations and per requires a package of actions including legal
capita consumption threatens biodiversity and policy frameworks, economic incentives,
and human health. Biosphere integrity and public and stakeholder engagement.
is threatened by a number of interacting Coherence of policies and coordination across
drivers including climate change, land-use sectors are essential.
change, pollution and biodiversity loss. Global
population is projected to increase to nine 67. Behavioural change is needed to improve
to ten billion by 2050, and may continue to human health and protect biodiversity.
increase this century. Greater investment in Human behaviour, which is informed by
education of girls and women and improved differences in knowledge, values, social norms,
access to contraceptives information and power relationships, and practices is at the
services can improve human health and core of the interlinkages between health and
well-being directly and also help to slow biodiversity, including challenges related to
these trends, potentially reducing pressures food, water, disease, medicine, physical and
on ecosystems. Under business as usual mental well-being, adaptation and mitigation
scenarios, increased per-capita consumption of climate change. There is a need to draw
will lead to even greater increased pressures on upon the social sciences to motivate choices
the biosphere. Slowing these trends requires consistent with health and biodiversity
improvements in energy and resource use objectives and to develop new approaches

18 Connecting Global Priorities: Biodiversity and Human Health

 through, inter alia, better understanding c. Addressing drivers of environmental change
of behavioural change, production and (deforestation and other ecosystem loss and
consumption patterns, policy development, degradation and chemical pollution) that
and the use of non-market tools. The need harm both biodiversity and human health,
for more effective communication, education including direct health impacts and those
and public awareness to be spread more widely mediated by biodiversity loss;
through school systems and other channels
and to devise communication and awareness d. Promoting lifestyles that might contribute
strategies on biodiversity and health. jointly to positive health and biodiversity
outcomes (for example, protecting
traditional foods and food cultures,
STRATEGIES FOR HEALTH AND promoting dietary diversity)
BIODIVERSITY
e. Addressing the unintended negative impacts
68. Health and biodiversity strategies could be
of health interventions on biodiversity
developed with the aim of ensuring that
(for example, antibiotic resistance,
the biodiversity and health linkages are
contamination from pharmaceuticals), and
widely recognized, valued, and reflected
incorporating ecosystem concerns into
in national public health and biodiversity
public health policies.
strategies, and in the programs, plans, and
strategies of other relevant sectors, with
f. Addressing the unintended negative impacts
the involvement of local communities. The
of biodiversity interventions on health (for
implementation of such strategies could be
example, effect of protected areas or hunting
a joint responsibility of ministries of health,
bans on access to food, medicinal plants).
environment, and other relevant ministries
responsible for the implementation of g. Adopting the One Health approach or
environmental health programs and national other integrative approaches that consider
biodiversity strategies and action plans. Such connections between human, animal,
strategies would need to be tailored to the and plant diseases and promotes cross-
needs and priorities of particular countries. disciplinary synergies for health and
Such strategies might include the following biodiversity.
objectives:
h. Educating, engaging and mobilizing the
a. Promoting the health benefits provided by public and the health sector, including
biodiversity for food security and nutrition, professional health associations as
water supply, and other ecosystem services, potential, powerful advocates for the
pharmaceuticals and traditional medicines, sustainable management of ecosystems.
mental health and physical and cultural Mobilize organizations and individuals
well-being. In turn, this provides a rationale who can articulate the linkage and the
for the conservation and sustainable use of enormous value proposition investments
biodiversity as well as the fair and equitable in sustainable ecosystem management
sharing of benefits; provide to the social and economic health
of communities;
b. Managing ecosystems to reduce the risks
of infectious diseases, including zoonotic i. Monitoring, evaluating and forecasting
and vector-borne diseases, for example by progress toward the achievement of
avoiding ecosystem degradation, preventing national, regional and global targets at
invasive alien species, and limiting or regular intervals against evidence-based
controlling human-wildlife contact; indicators, including threshold values for
critical ecosystem services, such as the

Connecting Global Priorities: Biodiversity and Human Health 19

 availability and access to food, water and computerized modeling programs should
medicines. also consider health-biodiversity linkages to
manage future risks and safeguard ecosystem
functioning while ensuring that social costs,
TOOLS, METRICS AND FURTHER
including health impacts, associated with
RESEARCH new measures and strategies do not outweigh
69. Integration of biodiversity and human potential benefits;
health concerns will require the use
of common metrics and frameworks. 71. The development of precautionary policies
Conventional measures of health are often that place a value on ecosystem services to
too limited in focus to adequately encompass health, and make positive use of linkages
the health benefits from biodiversity. between biodiversity and health are
Notwithstanding the broad WHO definition needed. For example, for integrated disease
of health, traditional measures of health, surveillance in wildlife, livestock and human
such as disability adjusted life years (DALYs) populations as a cost-effective measure to
and burden of disease, tend to have a more promote early detection and avoid the much
narrow focus on morbidity, mortality and greater damage and costs of disease outbreaks;
disability, and fail to capture the full breadth
72. Measuring health effects of ecosystem
of complex linkages between biodiversity and
change considering established “exposure”
health. Alternative metrics defining health are
threshold values helps highlight
needed to reflect the broad aspects of human
biodiversity-health-development linkages.
health and well-being. Further, to increase
Mechanisms linking ecosystem change to
collaboration across disciplines and sectors
health effects are varied. For many sub-fields,
more attention could be paid to “translating”
exposure thresholds or standards have been
the meaning of key metrics to increase
scientifically established that serve as trigger
shared relevance. Similarly, frameworks
points for taking action to avoid or minimize
provide a conceptual structure to build on
disease or disability. For example, air quality
for research, demonstration projects, policy
standards exist for particle pollution, WHO
and other purposes. Embracing a broad
has established minimum quantities of per
framework that aims to maximize the health
capita water required to meet basic needs,
of ecosystems and humans both could help the
and thresholds for food security define the
different disciplines and sectors work more
quantity of food required to meet individual
collaboratively. The conceptual framework of
daily nutritional needs. Measuring the
the IPBES, building upon that articulated in
health effects of ecosystem change relative
the Millennium Ecosystem Assessment, is a
to established threshold values highlights
framework that links biodiversity to human
how such change constitutes exposure – an
well-being, considering also institutions and
important principle linking cause and disease
drivers of change.
or other health effects –and encourages action
70. The development of comparable tools–and if thresholds are exceeded
maximizing the use of existing tools–
73. Economic valuation approaches linking
to promote a common evidence base
ecosystem functioning and health that
across sectors is needed. Tools ranging
support decisions about resource allocation
from systematic assessment processes (for
may appeal to a variety of stakeholders.
example, environmental impact assessments,
Many approaches enhance understanding
strategic environmental assessments, risk
of ecosystem functioning and human health
assessments, and health impact assessments)
linkages. Common on the health side are
to the systematic reviews of research findings,
environmental hazard or risk factor analyses.
to standardized data collection forms to

20 Connecting Global Priorities: Biodiversity and Human Health

 Others include identifying and reducing into Goals on food security and nutrition,
health disparities/inequities; focusing water and health. The SDG framework should
on environmental and socio-economic also provide for the enabling conditions for
determinants of disease, and conducting human health and for the conservation and
health impact assessments. Conservation sustainable use of biodiversity, and for the
approaches include land-/seascape change underlying drivers of both biodiversity loss and
modelling, vulnerability and adaptation ill-health to be addressed. This implies Goals
assessments, linked health and environmental for improved governance, and institutions, at
assessments and ecosystem service analyses. appropriate scales (from local to global), for
the management of risks and the negotiation
74. Further research is needed to elucidate of trade-offs among stakeholder groups, where
some of the potential knowledge gaps on they exist, as well as for behavioural change.
linkages between biodiversity and human
health. Examples of key questions include: 76. Ongoing evaluation of synergistic and
a. What are the relationships between antagonistic effects of complementary
biodiversity, biodiversity change and sustainable development goals and
infectious diseases? Specifically, what are targets is needed. This includes sustainable
the effects of species diversity, disturbance development goals and targets addressing
and human-wildlife contacts? What are the health, food and freshwater security, climate
implications for spatial planning? change and biodiversity loss and evaluate the
long-term impacts of trade-offs is needed;
b. What are the linkages between biodiversity such as the trade-off and short-term gains
(including biodiversity in the food from intensive and unsustainable agricultural
production system), dietary diversity and production, against longer-term nutritional
health? Is there a relationship between security. For example, the impacts of
dietary biodiversity and the composition and unsustainable agricultural practices that may
diversity of the human microbiome? What exacerbate climatic pressures may also lead
are good indicators of dietary biodiversity? to greater food insecurity, particularly among
What are the cumulative health impacts of poor and vulnerable populations, by negatively
ecosystem alteration? influencing its availability, accessibility,
utilization and sustainability.
THE SUSTAINABLE DEVELOPMENT
77. Health is our most basic human right
GOALS AND POST-2015 and therefore one of the most important
SUSTAINABLE DEVELOPMENT indicators of sustainable development.
AGENDA At the same time, the conservation
and sustainable use of biodiversity is
75. Health and biodiversity, and the linkages
imperative for the continued functioning
among them and with other elements
of ecosystems at all scales, and for the
of sustainable development must be
delivery of ecosystem services that are
well integrated into the post-2015
essential for human health. There are many
developmentw agenda. The post-2015
opportunities for synergistic approaches that
development agenda provides a unique
promote both biodiversity conservation and
opportunity to advance the parallel goals
the health of humans. However, in some
of improving human health and protecting
cases there must be trade-offs among these
biodiversity. The Sustainable Development
objectives. Indeed, because of the complexity
Goals will address various aspects of human
of interactions among the components
well-being and be accompanied by targets
of biodiversity at various tropical levels
and indicators. Specific biodiversity related
(including parasites and symbionts), and
targets and indicators should be integrated

Connecting Global Priorities: Biodiversity and Human Health 21

 across ecosystems at various scales (from of health–biodiversity relationships will allow
the planetary-scale biomes to human- for the adjustment of interventions in both
microbial interactions), positive, negative sectors, with a view to promoting human well-
and neutral links are quite likely to occur being over the long-term.
simultaneously. An enhanced understanding

ISTOCKPHOTO

22 Connecting Global Priorities: Biodiversity and Human Health

PART I
Concepts, Themes &
Directions
 1. Introduction to the State of
CONOR KRETSCH

Knowledge Review
The right to health is well established as a The dual challenges of biodiversity loss and rising
fundamental right of every human being.¹ global health burdens are not only multifaceted
Biodiversity is at the heart of the intricate web and complex; they also transcend sectoral,
of life on earth and the processes essential to its disciplinary and cultural boundaries, and demand
survival. Our planet’s biological resources are not far-reaching, coherent and collaborative solutions.
only shaped by natural evolutionary processes but One of the widely acknowledged shortcomings
are also increasingly transformed by anthropogenic of the Millennium Development Goals (MDGs)
activity, population pressures and globalizing and targets (the precursors of the SDGs) was the
tendencies. When human activity threatens these lack of cross-sectoral integration among social,
resources, or the complex ecosystems of which economic and environmental goals, targets and
they are a part, it poses potential risks to millions priorities (Haines et al. 2012). Opposing trends
of people whose livelihoods, health and well-being have been reported among the key indicators
are sustained by them. The increasingly complex for the MDGs, with many negative trends for
global health challenges that we face, including environmental indicators, including biodiversity
poverty, malnutrition, infectious diseases and (CBD 2014; Haines et al. 2012; WHO 2015).
the growing burden of noncommunicable diseases
(NCDs), are more intimately tied than ever to The World Health Organization (WHO) and
the complex interactions between ecosystems, the Secretariat of the Convention on Biological
people and socioeconomic processes. These Diversity (CBD) are working together to address
considerations are also at the heart of the post- these challenges.² This State of Knowledge Review
2015 Development Agenda and the Sustainable assembles expertise and insights from numerous
Development Goals (SDGs). researchers, practitioners, policy-makers

¹ The right to health is established as a fundamental right of every human being in Article 1 of the World Health Organization
Constitution (http://www.who.int/governance/eb/who_constitution_en.pdf). This was the first international instrument to
enshrine the “right to health” as the “enjoyment of the highest attainable standard of health”, also reflected in the Universal
Declaration of Human Rights in 1948. The right to health is understood as an inclusive right that extends beyond health
care to include the underlying determinants of health, such as access to water and food, essential medicines, etc.
² The World Health Organization and the Convention on Biological Diversity have been cooperating to promote greater
awareness about, and action on, the interlinkages between human health and biodiversity by convening experts from relevant
organizations, joint publications and organizing regional capacity-building workshops for experts from the biodiversity
and health sectors in the Americas and Africa (Romanelli et al. 2014). The Conference of the Parties to the Convention on
Biological Diversity has adopted a number of decisions in this regard (CBD 2010, 2012, 2014).

24 Connecting Global Priorities: Biodiversity and Human Health

and experts from the fields of biodiversity the evolving context of the SDGs and post-2015
conservation, public health, agriculture, nutrition, Development Agenda, as well as the Strategic Plan
epidemiology, immunology, and others to do the for Biodiversity 2011–2020 (see Box 1);
following:
• Facilitate cross-sectoral, interdisciplinary
• Provide an overview of the scientific evidence and transdisciplinary approaches to health
for linkages between biodiversity and human and biodiversity conservation, and promote
health in a number of key thematic areas; cooperation between different sectors and actors
in an effort to mainstream biodiversity in national
• Contribute to a broader understanding of the health strategies and mainstream health in
importance of biodiversity to human health in biodiversity strategies;

Box 1: Strategic Plan for Biodiversity 2011–2020

The Strategic Plan for Biodiversity 2011–2020 and its twenty Aichi Targets provide an agreed
overarching framework for action on biodiversity, and a foundation for sustainable development
for all stakeholders, including agencies across the United Nations (UN) system. The Strategic Plan
was adopted at the tenth meeting of the Conference of the Parties to the Convention on Biological
Diversity and has been recognized or supported by the governing bodies of other biodiversity-related
conventions, including the Convention on International Trade in Endangered Species of Wild Fauna
and Flora, the Convention on the Conservation of Migratory Species of Wild Animals, the Convention
on Wetlands of International Importance, the International Treaty on Plant Genetic Resources for Food
and Agriculture, the World Heritage Convention, as well as the UN General Assembly.

Governments at Rio 20 a rmed the importance of the Strategic Plan for Biodiversity 2011–2020
and achieving the Aichi Biodiversity Targets, emphasizing the role that the Strategic Plan plays for the
UN system, the international community and civil society worldwide to achieve the world we want. It
is primarily implemented by countries through national biodiversity strategies and action plans, with
Parties encouraged to set their own national targets within the framework of the Aichi Biodiversity
Targets. The UN General Assembly has encouraged Parties and all stakeholders, institutions and
organizations concerned to consider the Strategic Plan for Biodiversity 2011–2020 and the Aichi
Biodiversity Targets in the elaboration of the post-2015 UN Development Agenda, taking into account
the three dimensions of sustainable development.

The Strategic Plan for Biodiversity 2011–2020 includes a vision for 2050, ve strategic goals and
twenty Aichi Biodiversity Targets, mostly to be achieved by 2020. The 2050 Vision stresses the role
of biodiversity for human well-being: “biodiversity to be valued, conserved, restored and wisely used,
maintaining ecosystem services, sustaining a healthy planet and delivering bene ts essential for all
people . The ve goals include: to protect nature (Goal C), to maximize the bene ts for all people
(Goal D), to reduce pressures on biodiversity (Goal B), to address the underlying causes of loss (Goal
A), and to provide for enabling activities (Goal E). Under Goal D, Target 14 speci cally refers to human
health: “By 2020, ecosystems that provide essential services, including services related to water, and
contribute to health, livelihoods and well-being, are restored and safeguarded, taking into account
the needs of women, indigenous and local communities, and the poor and vulnerable.”

The Strategic Plan also includes means of implementation, monitoring, review and evaluation, as well
as support mechanisms (strategy for resource mobilization, capacity building, technical and scienti c
cooperation).

Connecting Global Priorities: Biodiversity and Human Health 25

 • Provide some of the basic tools necessary to Part Two examines how biodiversity is related
investigate how biodiversity may influence health to specific thematic areas at the biodiversity–
status or health outcomes, for given projects, health nexus, specifically addressing: water
policies or plans at varying levels (i.e. from and air quality; agricultural biodiversity and
community to the national, regional and global food security; nutrition and health; infectious
levels). diseases; microbial communities and NCDs; the
contribution of biodiversity to health care and
This work is aimed primarily at policy-makers, the impact of pharmaceuticals on biodiversity;
practitioners and researchers working in the traditional medicine; physical and mental health
fields of biodiversity conservation, public and well-being, and cultural ecosystem services.
health, development, agricultural and other
relevant sectors. Its findings suggest that greater Finally, Part Three discusses some critical cross-
interdisciplinary and cross-sectoral collaboration is cutting themes at the intersection of biodiversity
essential for the development of more coordinated and health, including climate change, disaster
and coherent policies aimed at addressing the risk reduction, and sustainable consumption and
tripartite challenge of biodiversity loss, the production. It also suggests broad strategies and
global burden of ill-health and development. approaches to integrate a consideration of the
Interdisciplinary scientific investigation and linkages between biodiversity and human health
approaches are critical to meeting these challenges. into public policy, and identifies preliminary
This volume demonstrates the need to foster tools and research gaps for further exploration.
greater synergy across scientific disciplines, social The volume concludes by highlighting how better
sciences and humanities, with more coherent consideration of the linkages between biodiversity
strategies across all levels of governance. The and human health will contribute to the post-2015
full involvement of all segments of society, Development Agenda.
including local communities, will also be needed
as we transition toward a new era of sustainable This State of Knowledge Review builds upon and
development. extends the health synthesis of the Millennium
Ecosystem Assessment (WHO 2005) and other
Some of the linked variables at the junction recent studies (Chivian & Bernstein 2008; Sala
of biodiversity and human health described et al. 2012). As further discussed in Chapter 2,
throughout this volume are schematically the review casts a wide net, considering the direct
represented in Figure 1. and indirect linkages between human health
and biodiversity (including its components and
This volume comprises three main parts. ecosystems).

Part One defines the concepts of biodiversity and Biodiversity plays a critical role in ecosystem
health, introduces concepts such as the social functioning and also yields direct and indirect
and environmental determinants of health, benefits (or ecosystem services) that support
biodiversity and ecosystem services, and provides human and societal needs, including good health,
a broad overview of the different ways in which food and nutrition security, energy provision,
biodiversity and health are linked. It also considers freshwater and medicines, livelihoods and
common drivers of change that impact on both spiritual fulfilment. These, in turn are mediated
global public health and biodiversity, and calls for by the social determinants of health (such as age,
the use of integrative, interdisciplinary framework gender and access to health care). Multidisciplinary
approaches that attempt to unite different fields approaches can help us to better analyse and
such as “One Health”, “Ecohealth” and the evaluate the interactions between these different
ecosystem approach. variables to better develop more coordinated,
coherent and integrated policies.

26 Connecting Global Priorities: Biodiversity and Human Health

ǡǤǢǰǭǠɻ Linkages and co-dependencies at the intersection of biodiversity and human health

BIODIVERSITY
Ecosystem goods
and services

Provisioning rminants o Cultural

services dete fh services
l e
ia ysical environme
nt
al

Ph
c
So

th

NASA
HEALTH
Poverty

Access

IMPACTS

A ge, ge n d e r
Regulating Supporting
services services

Connecting Global Priorities: Biodiversity and Human Health 27

LUIS ASCUI FOR ASIAN DEVELOPMENT BANK / FLICKR

2. Biodiversity and human health

linkages: concepts, determinants, drivers
of change and approaches to integration
1. BIODIVERSITY, HEALTH AND form the web of life, of which humans are an
integral part and upon which they depend for their
INTERACTIONS
very survival. It is the combination of these life
1.1 What is biodiversity? forms and their interactions with one another, and
with the surrounding environment, that makes
Biological diversity, most commonly used in its human life on earth possible (CBD 2006).
contracted form, biodiversity,¹ is the term used
to describe the variety of life on earth, including The Convention on Biological Diversity (CBD)
animals, plants and microbial species. It has defines biodiversity as: “the variability among
been estimated that there are some 8.7 million living organisms from all sources including,
eukaryotic species on earth,² of which some inter alia, terrestrial, marine and other aquatic
25% (2.2. million) are marine, and most of them ecosystems and the ecological complexes of which
have yet to be discovered (Mora et al. 2011). they are part; this includes diversity within species,
Biodiversity not only refers to the multitude of between species, and of ecosystems”.⁴ Biodiversity
species on earth, it also consists of the specific encompasses much more than the variety of life on
genetic variations and traits within species (such earth; it also includes biotic community structure,
as different crop varieties),³ and the assemblage of the habitats in which communities live, and the
these species within ecosystems that characterize variability within and among them.
agricultural and other landscapes such as forests,
wetlands, grasslands, deserts, lakes and rivers. Thus, biodiversity extends beyond the simple
Each ecosystem comprises living beings that measurement of species numbers to include the
interact with one another and with the air, complex network of interactions and biological
water and soil around them. These multiple structures that sustain ecosystems (McCann
interconnections within and between ecosystems 2007; Maclaurin and Sterelny 2008). Although

¹ It has been argued that the rapidly popularized term biodiversity was coined by Walter G. Rozen in 1986 (e.g. Maclaurin
and Sterelny 2008; Sarkar and Margules 2002).
² Eukaryotic cell species (including humans) are those that have a nucleus and internal compartments. Conversely, most
prokaryotic cell species are made up of a single cell.
³ For example, two species of rice contain over 120 000 genetically different varieties (CBD 2006).
⁴ Convention on Biological Diversity, Article 2.

28 Connecting Global Priorities: Biodiversity and Human Health

“species richness” is one of biodiversity’s key services that they provide to public health and to
components, the two terms are not synonymous. economic development alike (MA 2005a, b).
The widely accepted definition of biodiversity
adopted by the CBD is flexible, inclusive, and The findings of the Millennium Ecosystem
reflective of the levels and complexities of biotic Assessment and of large-scale national and
and abiotic interactions. It recognizes levels of regional assessments have made it clear that it
variability within species, between species, and is increasingly important for people in the public
within and between ecosystems as integral to the health sector to recognize that human health
ecological processes of which they are a part (Mace and well-being are influenced by the health and
et al. 2012). It is also understood that variability integrity of local ecosystems, and frequently by
manifests itself differently at various temporal and the health of local plant and animal communities.
spatial scales (Nelson et al. 2009; Thompson et The interactions between people and biodiversity
al. 2009). can determine the baseline health status of a
community, providing the basis for good health
The scope of the Convention is broader still; and secure livelihoods, or creating the conditions
its objectives – “the conservation of biological responsible for morbidity or mortality.⁵ In many
diversity, the sustainable use of its components cases, the long-term success and sustainability
and the fair and equitable sharing of the of public health interventions is determined by
benefits arising out of the utilization of genetic the degree to which ecological factors are taken
resources” – indicate an interest in the components into account. In the same way that economic
of biodiversity (including individual species) and factors must often be addressed, biodiversity and
genetic resources. its importance to the functioning of ecosystems
must also be considered. As noted in the earlier
1.2 What is health? definition of biodiversity, this concept must also
be explored at multiple geographical and temporal
The constitution of the World Health Organization scales for the health sector. Public health policies
(WHO) defines health as “a state of complete must also ensure that the relevance of biodiversity
physical, mental and social well-being and not is assessed and accounted for within various plans
merely the absence of disease or infirmity”. or projects. Similarly, biodiversity conservation
Health is a dynamic concept that is influenced by initiatives must also account for how such projects
a range of interacting social, biological, physical, may affect public health, whether the resulting
economic and environmental factors. As such, impacts are positive or negative. As the global
health is one of the most important indicators of community works towards the implementation
sustainable development. While social status and of the United Nations Sustainable Development
economic security are perhaps most important in Goals, the importance of biodiversity to
determining an individual’s capacity to manage her livelihoods, poverty eradication and human well-
or his health and to maintain a healthy lifestyle, being is also of paramount importance.
the role of environmental and ecosystem change
in determining health status are increasingly
1.3 Biodiversity–health interactions
recognized within the health, environment and
development communities. The 2005 reports Biodiversity and human health are linked in
of the Millennium Ecosystem Assessment many ways, and a broad scope is taken in this
have helped to increase understanding of the State of Knowledge Review. Further to Mace
relationships between the environment and and colleagues (2012), we look at “biodiversity”
human well-being. Together, these reports have in a broad sense, including not only species
marked a turning point in highlighting the richness and the genetic diversity within
importance of ecosystems and the goods and species (“biodiversity, narrow sense”) but also

⁵ Morbidity refers to the incidence of a disease across a population, while mortality refers to the rate of death in a population.

Connecting Global Priorities: Biodiversity and Human Health 29

 the components of biodiversity (species and crops and livestock, associated pollinators and
genotypes), and habitats and ecosystems. Thus, pest control organisms and in soils – support
the distribution and abundance of species, and the agricultural production. Ecosystem services in the
extent of natural habitats, are relevant, in addition wider landscape of biodiversity underpin a host
to diversity per se. Moreover, we consider not only of ecosystem services, including water provision
the direct effects of biodiversity or its components and erosion control. The functioning and integrity
on human health, but also the (indirect) effects of the biosphere at a planetary scale (i.e. global
that are due to biodiversity’s role in supporting level) is also understood to depend on biodiversity.
ecosystem processes and functioning (see section
3). Further, we examine drivers of change that
2. EQUITY AND SOCIAL
are common to both biodiversity loss (or change)
and health status. Finally, we are also concerned DIMENSIONS OF HEALTH AND
with the impacts of the interventions made in the BIODIVERSITY
health sector on biodiversity and vice versa. Thus, Human population health is determined, to a large
this State of Knowledge Review casts a broader extent, by the social, economic and environmental
net than other recent reviews (e.g. Hough 2014). determinants of health (United Nations Task
Team on Social Dimensions of Climate Change
Like Sandifer et al. (2015), we consider a broad
2011; WHO 2008). The social, economic and
range of pathways through which biodiversity may
behavioural aspects of the human condition
provide health and well-being benefit to people:
interact with the environment, including critical
psychological (e.g. green spaces and iconic wildlife;
elements of biodiversity, biodiversity losses and
see Chapter 12), physiological (directly through
gains, and ecosystem services.
the human microbiome, and indirectly through
exercise in green spaces, see Chapters 8 and 12), Biodiversity and its changes (losses and gains)
regulation of the transmission and prevalence are, to a great extent, the result of anthropogenic
of some infectious diseases (see Chapter 7), influences (Mora and Zapata 2013). The social
provision of food and good nutrition (Chapters dimensions of biodiversity are present both in
5 and 6), clean air and water (Chapters 3 and 4), relation to these drivers of change and in relation
the provision of traditional and modern medicines to how the impacts of biodiversity change are
(Chapters 9 and 11) and the impact of some mediated among groups of differing socioeconomic
pharmaceuticals on the environment (Chapter 11). status. Biodiversity loss is impacted by
anthropogenic drivers, such as overexploitation of
Box 1 and Figure 1 provide a typology of
natural resources, human-induced climate change
biodiversity–health interactions.
and habitat loss. Large-scale social and economic
processes and systems affect biodiversity, and the
The interactions between biodiversity and
social, economic and environmental dimensions of
health are manifested at multiple scales from
ecological sustainability at risk (UNESCO 2013).
individuals, through communities and landscapes
to a planetary scale (Figure 1). At the scale of the
Environmental determinants of health (such as air
individual person, the human microbiota – the
quality, food security, water security, freedom from
commensal microbial communities present in
disease, etc.) are interrelated and adversely affected
our gut, in our respiratory, oropharyngeal and
by the reduced ability of degraded ecosystems and
urogenital tracts and on our skin – contribute to
biota to adapt to the impacts of climate change, air
our nutrition, help regulate our immune system,
pollution, natural disasters or water scarcity. Many
and prevent infection. Interactions among family
of the dynamics between biodiversity and human
members and the wider environment may be
health are in the area of infectious, vector-borne
important in the maintenance and turnover of
diseases. In some cases, biodiversity loss (such as
this diversity. At the community level (such as
that associated with deforestation) may enhance
farms), many aspects of biodiversity – among
the risk of some diseases such as malaria (Chaves

30 Connecting Global Priorities: Biodiversity and Human Health

Box 1. A typology of biodiversity–health interactions

ǡǤǢǰǭǠɻ

!)#$%*





























%..-

 %#) &! $
























 %#) &! $

01











  

01






2

2

/


0
1

!$*$%
!!$

#!)$!  

2
$#)$

PHOTOS: ASIAN DEVELOPMENT BANK / FLICKR

(""!#& 


(%(#

(& 


$,


$,



$,
 

$,
 

$ƩUVWW\SHRILQWHUDFWLRQLVZKHUHELRGLYHUVLW\JLYHVULVHWRKHDOWKEHQHƩWV%LRGLYHUVLW\Î Health).

For example, di erent species (as well as crop varieties and livestock breeds) provide nutrients and
medicines. Biodiversity also underpins ecosystem functioning, which provides services such as water and
air puri cation, pest and disease control, and pollination. Biodiversity can also be a source of pathogens and
thus have negative impacts on health. Changes in biodiversity would lead to changes in the health bene ts.
Drivers of such changes extend the causal change upstream (Driver of change Î loss of biodiversity Î
reduction in health bene ts).

$VHFRQGW\SHRILQWHUDFWLRQDULVHVIURPGULYHUVRIFKDQJHWKDWDƨHFWERWKELRGLYHUVLW\DQGKHDOWKLQ
parallel. (Driver of change Î impacts on health and on biodiversity). For example, air and water pollution
can lead to biodiversity loss and have direct impacts on health. Deforestation (or other land-use change or
ecosystem disturbance) can lead to loss of species and habitats, and also increased disease risk for humans.
Conversely, moderated meat consumption can reduce the pressures on biodiversity (less land-use change;
lower greenhouse gas emissions) and also have health bene ts for individuals. In addition to the parallel
e ects of the driver on biodiversity and health, there may be additional impacts of the change in biodiversity
on health. For example, water pollution, in addition to harming health though loss of drinking water
uality, could lead to collapse of a uatic ecosystems through eutrophication leading to sh mortality and
conse uent negative e ects on nutrition.

(3) A third type of interaction arises from the impacts of health sector interventions on biodiversity (Health
intervention Î biodiversity) and of biodiversity-related interventions on health (Biodiversity intervention
Î health). For example, use of pharmaceuticals may lead to the release of active ingredients in the
environment and damage species and ecosystems. Again, these may have negative knock-on e ects on human
health. On the other hand, protected areas or hunting bans could deny access of local communities to bushmeat
and other wild foods, with negative nutritional impacts. Positive interactions of this type are also possible. For
example, establishment of protected areas may protect water supplies, with positive health bene ts.

Connecting Global Priorities: Biodiversity and Human Health 31

 et al. 2011; Hahn et al. 2014; Laporta et al. 2013), in isolation or through an interaction with other
while in others, biodiversity gains (such as that determinants) or indirectly (e.g. access to healthy
associated with reforestation) may also sometimes food).
increase the risk for other diseases (Levy 2013;
Ostfeld and Keesing 2000). Detrimental changes to biodiversity and the
resulting risks and burden of human health
In addition to environmental determinants, problems are inequitably distributed in specific
social and economic determinants also influence social–ecological settings. Populations exposed
the dynamics between biodiversity changes and to the greenest environments have been found
human health. The inequities of how society to also have the lowest levels of health inequality
is organized mean that the freedom to lead related to income deprivation, suggesting that
a flourishing life and to enjoy good health is healthy physical environments can be important
unequally distributed between and within for reducing socioeconomic health inequalities
societies. This inequity is seen in the conditions (Mitchell and Popham 2008). Equity issues are
of early childhood and schooling, the nature of not only important in relation to different groups
employment and working conditions, the physical within a country, but also in relation to different
form of the built environment, and the quality of vulnerabilities among countries. Developing
the natural environment in which people reside. countries are more reliant on biodiversity and
Depending on the nature of these environments, ecosystem services than developed ones, and their
different groups will have different experiences health systems are usually less prepared to protect
of material conditions, psychosocial support and the health of their populations, which leads to
behavioural options, which make them more or greater negative health impacts of biodiversity
less vulnerable to poor health. Social stratification change. Between countries, biodiversity loss is
likewise determines differential access to and related to income inequality (Mikkelson et al.
utilization of health care, with consequences for 2007). For example, over 1 billion people, mainly
the inequitable promotion of health and well- in developing countries, rely on fisheries as their
being, disease prevention, and recovery from primary source of animal protein (Gutiérrez et al.
illness and survival. This unequal distribution 2011).
of health-damaging experiences is not in any
sense a “natural” phenomenon but is the result Different gender roles in relation to biodiversity
of a toxic combination of poor social policies and management, conservation and use can also
programmes, unfair economic arrangements have an impact on human health, and more
and power relationships. (Commission on Social attention needs to be paid to these gender
Determinants of Health 2008). dimensions (WHO 2011, 2008). Access to, use
and management of biodiversity have different
Population groups more reliant on biodiversity health impacts on women and men and boys
and ecosystem services, especially on provisioning and girls, determined by gender norms, roles and
services such as timber, water and food, are usually relations (Gutierrez-Montes et al. 2012). Social
more vulnerable to biodiversity loss and those norms and values determine different gender
less covered by social protection mechanisms roles and relations, which in turn, are translated
(e.g. health insurance). Vulnerable groups include into different responsibilities, obligations, benefits
indigenous populations, specific groups dependent and rights in relation to biodiversity (Manfre and
on biodiversity and ecosystem services and, Ruben 2012). In addition to the lack of political
for example, subsistence farmers. Detrimental will, and frequently weak institutional capacity
changes to biodiversity and the resulting risks and and legal frameworks that fail to assess and
burden of human health problems are inequitably address different gender roles, there is a lack of
distributed in specific social–ecological settings. sex-disaggregated data on biodiversity access,
These inequalities affect both individual and use and control, which makes it very difficult to
community health either directly (whether it be conduct a gender analysis and therefore design

32 Connecting Global Priorities: Biodiversity and Human Health

adequate responses targeting specifically those Relevant tools that could be used to understand
most vulnerable population groups (Castaneda et the equity and social dimensions of health and
al. 2012). biodiversity for any relevant policy or programme
include social impact assessments, health impact
However, it is widely accepted that many of assessments and strategic impact assessments.
the adverse impacts of biodiversity loss are Whatever tool is used, it is key to ensure that all
impacting already vulnerable groups of people, health, environmental, and social considerations
specifically populations who are dependent and impacts are integrated within the assessment.
on biodiversity and ecosystem services (forest As discussed in section 5 of this chapter and
dwellers, indigenous populations, women and Part III of this volume, solutions to biodiversity
girls, etc.). Biodiversity losses in specific social– and health challenges also necessitate the
ecological settings and the resulting health effects sustained engagement of multiple stakeholders,
on marginalized populations are often triggered both in governments, civil society, and in
by large-scale processes beyond the control nongovernmental and international organizations.
of the populations at risk. Climate change or The social sciences are, therefore, important
large-scale mining or logging projects may have contributors to research and policy-making in
negative impacts on biodiversity, and increase biodiversity and health (UNESCO 2013), and to
social and economic inequalities. For example, the large-scale social and behavioural changes
it is estimated that 1 billion people only produce required to achieve the objectives of sustainable
3% of global greenhouse gas emissions. A social development.
justice perspective is, therefore, needed to address
the various equity dimensions in the biodiversity
and health dynamic (Walter 2003). 3. BIODIVERSITY, ECOSYSTEM
FUNCTIONS AND SERVICES
The social sciences are important contributors
Scientific knowledge of the impacts of
to research and policy-making in biodiversity
biodiversity loss on ecosystem functioning has
and health. In addition to gender analysis, a
increased considerably in the past two decades
multifaceted approach is needed to effectively
(Balvanera et al. 2014; Cardinale et al. 2012;
tackle the equity and social dimensions of health
Reis et. al. 2012; Naeem and Wright 2003;
and biodiversity. Social research illuminates
Loreau et al. 2001; Tilman et al. 1997), as well as
social vulnerabilities, and has the potential to
corresponding knowledge of its implications for
engage and mobilize people most affected by
public health (Myers et al. 2013). In this section,
biodiversity loss, e.g. indigenous populations.
we summarize key elements of the relationship
The social sciences also play an important role in
between biodiversity, ecosystems and ecosystem
determining policy options for health, biodiversity
functioning, its connection to ecosystem services,
and ecosystem management (Artner and Siebert
and the components that influence the quantity,
2006; Duraiappah and Rogers 2011; Gilbert et al.
quality and reliability of ecosystem services, and
2006). Inter-, multi- and transdisciplinary research
that contribute to ecosystem resilience.
can provide valuable insights into the drivers
of disease emergence and spread, contribute There is strong evidence of the relationship
to identifying previous patterns of disease risk, between biodiversity and ecosystem functioning
and help to predict future risks through the and, in some cases, we can directly link this to the
lens of social–ecological systems (Folke 2006; ecosystem services necessary to sustain human
Gilbert et al. 2006; UNESCO 2013). For example, health (Loreau et al. 2001; Balvanera et al. 2006;
interdisciplinary work on the social determinants Cardinale et al. 2012; Balvanera et al. 2014). In
of health can also provide valuable insights into other cases, we do not yet have complete evidence
the drivers of disease emergence and spread, of this relationship (Schwartz et al. 2000; Cardinale
contribute to identifying previous patterns of et al. 2012). While there is broad consensus within
disease risk and help to predict future risks. the scientific community on several aspects of

Connecting Global Priorities: Biodiversity and Human Health 33

 the relationship between biodiversity, ecosystem The specific components of biodiversity (e.g.
functioning and the consequences of its loss on genes, species) and attributes (e.g. variability,
the ability of ecosystems to provide services, composition) that underpin the ecosystem
the full range of impacts of biodiversity loss on services that, in turn, support human health
ecosystem functioning is not fully understood and well-being may differ among the services or
(Reiss et al. 2009; Hooper et al. 2005). goods in question, and on the processes upon
which they rely. The diverse functional traits of
3.1 Biodiversity, ecosystem processes species within a community can also influence
and properties ecosystem properties, and their examination
can contribute to understanding variations
Ecosystems comprise physical and chemical in ecosystem functions (Hooper et al. 2005;
biotic (e.g. plants, animals, humans) and abiotic Tilman et al. 1997; Haines-Young and Potschin
(e.g. light, oxygen, temperature, soil texture and 2010; Naeem and Wright 2003) and resilience
chemistry, nutrients) interactions (Currie 2011). (Mori et al. 2013; Elmqvist 2003). In this sense,
Ecosystem processes include decomposition, species’ functional characteristics can be critical
nutrient cycling (e.g. water, nitrogen, carbon to ecosystem services; their loss can result in
and phosphorus cycling), production (of plant permanent changes.
matter), as well as energy and nutrient fluxes.
A healthy ecosystem – one that performs its Twenty years of work on the relationship between
various functions well and where equilibrium is biodiversity and ecosystem functioning has
maintained – is dependent upon biodiversity. generated a number of controversies and spurred
This is often referred to as ecosystem integrity, efforts to develop scientific consensus. Cardinale
ecosystem stability or ecosystem health. et al. (2012) conclude that diverse communities
tend to be more productive both because they
Fluxes of energy, biogeochemical cycles such as contain key species that have a large influence on
nutrient cycling and oxygen production, and productivity, and because differences in functional
community dynamics such as predator–prey traits among organisms increase the total capture
interactions are regulated by the earth’s biota. The of resources (light, water). Thus, biodiversity
attributes (including composition and abundance) loss reduces the efficiency by which ecological
and interactions of biotic and abiotic components communities capture biologically essential
determine ecosystem processes and their properties, resources, produce biomass, and decompose
and they influence changes in each of the latter and recycle biologically essential nutrients. They
over space and time (Reiss et al. 2009). The report that the impact of biodiversity on any single
provision of essential goods and services, including ecosystem process is non-linear and saturating,
those essential to sustaining human life, is reliant such that change accelerates as biodiversity loss
on the properties, processes and maintenance of increases. They also point to mounting evidence
ecosystems (Naeem and Wright 2003; Balvanera that biodiversity increases the stability of
et al. 2006; Reiss et al. 2009, 2010). The quality, ecosystem functions through time.
quantity and security of the essential services
that we derive from ecosystems are determined
3.2 Ecosystem services
by several dynamic and interlinked factors,
including different components of biodiversity, Human health ultimately depends upon ecosystem
underlying physical and biological processes (each products and services (e.g. availability of fresh
with their own characteristics and thresholds), and water, food and fuel sources), which are required
complex responses to environmental stressors for good health and productive livelihoods.
such as pollution and climate change (Mace 2012; Many ecosystems, such as marine areas, forests,
Balvanera et al. 2006). grasslands and wetlands, contribute to regulation
of the world’s climate, and can also influence
local microclimates. People depend directly on

34 Connecting Global Priorities: Biodiversity and Human Health

ASIAN DEVELOPMENT BANK / FLICKR

ecosystems in their daily lives, including for the in ecosystem services affect livelihoods, income,
production of food, medicines, timber, fuel and local migration and, on occasion, may even cause
fibre, but also in ways that are not always apparent political conflict.
or appreciated. Our natural capital is not only the
source of our food, but also provides less tangible The first comprehensive scientific appraisal of the
benefits, such as spiritual enrichment, and areas condition and trends of ecosystem services for
for recreation and leisure. Ecosystems also play health and well-being, the Millennium Ecosystem
important roles in the water cycle, regulating Assessments,⁶ adopted four major categories of
the flow of water through the landscape, and ecosystem services: provisioning services such
the amount of sediments and contaminants as water, food and timber; regulating services
that affect important water resources. These such as pest control, climate regulation and
and other important benefits, called “ecosystem regulation of water quality; cultural services
goods and services”, are essential to our society, including recreational and spiritual benefits; and
our economic development, and our health and supporting services such as photosynthesis, soil
well-being. Biodiversity loss can have direct, and formation and nutrient cycling. Each category is
sometimes significant, human health impacts, vital for human and community health, as well
particularly if ecosystem services are no longer as ecosystem resilience. The study concluded that
adequate to meet social needs. Indirectly, changes ecosystems processes have changed more rapidly

⁶ While the Millennium Assessment has been instrumental in evaluating the conditions and trends of ecosystems for health,
the notion of ecosystem services can be traced as far back as the 1970s (Haines-Young and Potschin 2010). The impetus
for placing human needs at the centre of biodiversity management is also covered by the 12 principles of the ecosystem
approach adopted by the Convention on Biological Diversity (COP 5 decision the V/6).

Connecting Global Priorities: Biodiversity and Human Health 35

 since the mid-twentieth century than at any other be transformed if a change in ecosystem structure
time in recorded human history. Among the 24 crosses a given threshold. Structural changes
categories of ecosystem services assessed, 15 of may be manifested as a result of the removal
them were in a state of decline, the majority of of key predators or other species from the food
them regulating and supporting services (MA web (Thomson et al. 2012), the simplification of
2005). Declining services include pollination, vegetation or soil structure, increased or decreased
the ability of agricultural systems to provide pest aridity, species loss and many other factors.
control, the provision of freshwater, marine fishery Biodiversity loss is continuing, and in many cases
production, and the capacity of the atmosphere increasing (Butchart et al. 2010; Tittensor et al.
to cleanse itself of pollutants. Most ecosystem 2014). Biodiversity loss has been identified as one
services that were found to be increasing were of the most critical drivers of ecosystem change
provisioning services, including crops, livestock (Hooper et al. 2012). Changes in the diversity of
and aquaculture. Consumption was also increasing species that alter ecosystem function may directly
of all services across all four categories. These reduce access to ecosystem services such as food,
increases have helped to generate and sustain water and fuel, and also alter the abundance of
the increases in human health and well-being species that control critical ecosystem processes
seen over the same period. However, the decline essential to the provision of those services (Chapin
of many other ecosystem services – mostly the et al. 2000).
regulating and supporting services – threatens
to undermine this progress, presenting threats Ecosystem regime shifts, including “tipping
to human health and well-being (Chivian and points”, have been widely described and
Bernstein 2008; Haines-Young and Potschin 2010; characterized at local levels (for example,
McMichael and Beaglehole 2000), several of which eutrophication of freshwater or coastal areas
are described throughout this technical volume. due to excess nutrients; collapse of fisheries
due to overfishing; shifts of coral reefs to algae-
In general, aggregate terms, socioeconomic dominated systems; see Sheffer 2009; CBD 2010).
progress has benefited human health and well- There is growing concern that regime shifts
being, but at a cost to the underlying natural could occur at very large spatial scales over the
resource base. Raudsepp-Hearne et al. (2010) next several decades, as human–environment
examined several hypotheses to explain this systems exceed limits because of powerful and
apparent paradox and call for efforts to expand widespread driving forces that often act in
our understanding of the complex cross-scale combination: climate change, overexploitation of
interactions between ecosystem services, human natural resources, pollution, habitat destruction,
activities and human well-being. and the introduction of invasive species (Leadley
et al. 2014; Barnosky et al. 2012; Hughes et al.
3.3 Biodiversity loss, biosphere 2013). Cardinale et al. (2012) suggest that the
integrity and tipping points impacts of biodiversity loss on ecological processes
might be sufficiently large to rival the impacts of
Ecosystem management strategies aimed at climate change and many other global drivers of
maximizing conservation and public health environmental change.
co-benefits must consider that systems have
emergent properties that are not possessed by Leadley et al. describe scenarios for regional-scale
their individual components: they are more shifts that would have large-scale and profound
than the sum of their parts. One example is the implications for human well-being (Leadley
resilience of ecosystems to absorb shock in the et al. 2014). The unprecedented pressures of
face of disturbance (such as pests and disease, human activity on biodiversity and on the
climate change, invasive species, or the harvesting earth’s ecosystems may also lead to potentially
of crops, animals or timber) and return to their irreversible consequences at a planetary scale,
original structure and functioning. Ecosystems can and this prospect has led to the identification of

36 Connecting Global Priorities: Biodiversity and Human Health

processes and associated thresholds, and to the productive capacity, and concomitant pressures
development of various approaches⁷ to define on the earth’s biological resources may undermine
preconditions for human development on a the ability of ecosystems to provide life-sustaining
planetary scale (Rockström et al. 2009; Barnosky services (CBD 2010; McMichael and Beaglehole
et al. 2012, Steffen et al. 2015; see also Mace et 2000).
al. 2014). Global efforts to pursue sustainable
development will continue to be compromised if Social change and development biases (such
these critical pressures are not countered in a more as urbanization, poverty and inequity) further
rigorous, systematic and integrated fashion. influence the drivers of biodiversity loss and ill-
health. Macroeconomic policies and structures,
and public policies that provide perverse
4. DRIVERS OF CHANGE incentives or fail to incorporate the value of
In recent decades, the impact of human activity on biodiversity frequently compound the dual
the natural environment and its ecosystems has threat to biodiversity and public health. Both
been so profound that it has given rise to the term the impacts of biodiversity loss and ill-health
anthropocene, popularized by Nobel prize-winning are likely to be most pronounced among the
chemist Paul Crutzen, delimiting a shift into a new world’s poorest, most vulnerable populations,⁸
geological epoch, in which human activity has which are often those most immediately reliant
become the dominant force for environmental on natural resources for food, shelter, medicines,
change (Crutzen 2002). Anthropogenic pressures, spiritual and cultural fulfilment, and livelihoods
demographic change, and resulting changes in (MA 2005). As indicated above, these vulnerable
production and consumption patterns are also groups are also generally those least able to access
among the factors that contribute to biodiversity substitutes when ecosystem services are degraded.
loss, ill-health and disease emergence. These In addition to the immediate usefulness of natural
pressures have shown a “great acceleration”, resources, the intrinsic value of nature to so many,
especially in the past 50 years (Steffen et al. its cultural and spiritual contributions, and the
2015b). While some human-induced changes right of future generations to inherit a planet
have garnered public health benefits, such as the thriving with life also should not be overlooked.
provision of energy and increased food supply, in
many other cases they have been detrimental to The drivers (causes) of ill-health and human,
the environment, ecosystems and corresponding animal and plant disease often overlap with the
services, as well as human health (Myers et al. drivers of biodiversity loss. Some of the principal
2013; Cardinale et al. 2012; Balmford and Bond common drivers, identified in the third edition
2005; McMichael and Beaglehole 2000). In many of Global Biodiversity Outlook (GBO 3) and
cases, the ecological implications are immense and reiterated in its fourth edition, include: habitat
the need to address them pressing if our planet change, overexploitation and destructive harvest,
is to provide clean water, food, energy, timber, pollution, invasive alien species and climate
medicines, shelter and other benefits to an ever- change (CBD 2010, 2014), all of which may be
increasing population. The rise in demographic exacerbated by environmental changes.
pressures and consumption levels will translate
into unprecedented demands on the planet’s
⁷ Rockström and colleagues (2009), updated by Steffen et al. (2015), describe nine “planetary boundaries” that have been
identified: including biosphere integrity (terrestrial and marine); climate change; interference with the nitrogen and
phosphorus cycles; stratospheric ozone depletion; ocean acidification; global freshwater use; changes in land use; chemical
pollution; and atmospheric aerosol loading. The metrics used to define the biodiversity/biosphere integrity planetary
boundaries has been challenged, including biodiversity loss, for its measurement of biodiversity as “global species extinction
rate” and “the abundance, diversity, distribution, functional composition and interactions of species in ecosystems” were
not considered in its 2009 (Mace et al. 2014: 296).
⁸ For example, Butchart et al. (2010) indicate that more than 100 million of the world’s poor people, especially reliant on
biodiversity and the services it provides, live in remote areas within threatened ecoregions.

Connecting Global Priorities: Biodiversity and Human Health 37

 ASIAN DEVELOPMENT BANK / FLICKR
As the majority of human infectious agents much more systematic assessment as well as more
have originated in animals (known as “zoonotic structured, coherent, and cross-cutting policies
diseases”), including the infection leading to and strategies. These critical linkages should
HIV/AIDS (from chimpanzees hunted for human be translated into concrete policy targets as we
consumption), animal and environmental links embark on a new series of global commitments
to human infectious diseases are highly relevant on sustainable development as the MDGs reach
(Taylor et al. 2001). While the ties between their term in 2015.
infectious diseases and biodiversity are perhaps
the most frequently cited, biodiversity loss also 4.1 Habitat change
has significant and myriad implications for
noncommunicable diseases (NCDs) and the Land-use change (e.g. full or partial clearing
socioeconomic determinants of health. Examples for agricultural production or natural resource
of these are highlighted for each of the major extraction, such as for as timber, mining and oil) is
drivers of biodiversity loss identified above. the leading driver of biodiversity loss in terrestrial
ecosystems. Alteration of native habitats may also
The pressing need to jointly address both social reduce resilience; for example, deforested areas
and environmental determinants of health may experience soil erosion, increasing ecological
(Bircher and Kuruvilla 2014) has been widely risks of extreme weather events such as sudden
acknowledged through various multilateral flooding, and limited food production potential
agreements. However, the role of biodiversity as a from reduced soil enrichment. Furthermore,
mediating influence on human health (through the habitat changes such as deforestation directly
loss of ecosystem services, which are themselves alter the capacity of carbon sinks and thus further
mediated by ecological processes), while gaining increase the risks of climate change.
more widespread attention since Rio, merits

38 Connecting Global Priorities: Biodiversity and Human Health

Land-use change is also the leading driver of risks. Intensification of harvest and exploitative
disease emergence in humans from wildlife practices, such as the mixing of wildlife and
(Jones et al. 2008). Changes to habitats, including domestic species in markets, as well as the mixing
through altered species composition (influenced and spread of their pathogens, can create global
by conditions that may more favourably support epidemics, as seen with the 2003 outbreak of
carriers of disease, as seen with malaria- severe acute respiratory syndrome (SARS).
harbouring vectors in cleared areas of the Amazon)
and/or abundance in an ecosystem (and thus 4.3 Pollution
potential pathogen dispersion and prevalence),
and the establishment of new opportunities for Environmental pollution poses direct threats to
disease transmission in a given habitat, have both biodiversity and human health in many ways.
major implications for health. Human-mediated Pollutant exposure risk is potentially increased
changes to landscapes are accompanied by human for top-of-the-chain consumers such as humans
encroachment into formerly pristine habitats, and marine mammals through bioaccumulation
often also accompanied by the introduction of along the food chain, as seen with mercury. Air
domestic animal species, enabling new types pollution exposure presents risks of respiratory
of interactions among species and thus novel diseases. Other so-called “lifestyle diseases” (such
pathogen transmission opportunities. as obesity and diabetes) may be influenced by
access to physical fitness, which may be limited
by outdoor and indoor air pollution levels.
4.2 Overexploitation and destructive
Chemicals, such as pharmaceuticals or plastics
harvest containing endocrine-disrupting substances, may
Overexploitation of biodiversity and destructive be dispersed on entering water sources and other
harvesting practices reduce the abundance of the environmental settings, posing acute, chronic or
populations of species concerned, and in some recurring exposures in humans and animals. Wide-
cases, can threaten the survival of the species itself. scale application of antimicrobials for human and
Demand for wild-sourced food is increasing in animal medicine and food production, much of
some areas. The wildlife trade, for purposes such as which is excreted into the environment, is resulting
supplying the pet trade, medicinal use, horticulture in rapid changes to microbial composition, as
and luxury goods, is increasing globally, well as driving development of antimicrobial-
exacerbating pressures on wild populations. resistant infections. Contaminated water may
Practices for harvest, including unregulated enable persistence of human infectious agents
administration of chemicals for the capture of and their diseases, such as cholera-causing Vibrio
animals (e.g. the release of cyanide or trawling and parasitic worm-transmitted schistosomiasis.
practices for fishing) may also have impacts on
non-target species, and/or unsustainable harvests 4.4 Invasive alien species
may alter ecological dynamics, such as diminished
potential for seed dispersion and implications Invasive alien species (IAS) pose direct threats to
for food chains (affecting also the humans who native and/or endemic species. The introduction of
depend on them). As native biodiversity declines, IAS may result in invasive species out-competing
local protein sources from subsistence hunting or important food and traditional medicine sources for
gathering may be diminished, causing inadequate human populations, as well as causing fundamental
nutrition if alternatives are unavailable or lack impacts on ecosystems that may influence health
necessary nutrients. Additionally, bushmeat processes. Examples of this include impaired water
hunting and consumption, sometimes in areas quality from the introduction of zebra mussel in
that have not been previously targeted for food the United Kingdom and North America, altered
sourcing (for example, in newly established soil quality through the spread of weeds, and the
mining camps in formerly pristine habitat) may reduced species decomposition facilitated by feral
pose direct novel infectious disease transmission pigs grazing on native plants as well as agricultural

Connecting Global Priorities: Biodiversity and Human Health 39

 land. In addition to these detrimental impacts, IAS (recent immigrants) might not have immunity to
pose risks of disease introduction and spread for zoonotic diseases endemic to the area, making
native wildlife, agricultural species and humans. them particularly susceptible to infection. Women
As global trade and travel continues to increase, so who are required to butcher harvested wildlife, or
do the health risks; changing climactic conditions men who hunt the game, may be particularly at
may also enable establishment of IAS where risk. Moreover, those sectors of society that lack
climate would have previously limited survival, adequate income to purchase market alternatives
demonstrated with alarming clarity in the case may be more likely to access forest resources
of the pine mountain beetle invasion in western (including wildlife) for food and trade. Thus,
Canada. there are likely socioeconomic and gender-specific
relationships to these types of disease risks and
4.5 Climate change exposures (WHO 2008). Disease may also worsen
the economic status of a population; vector-borne
The direct and indirect impacts of climate change and parasitic diseases, the burden of which is
also pose risks for biodiversity and health; driven by ecological conditions, have been shown
for example, shifts in species ranges may also to worsen the poverty cycle (Bonds et al. 2012).
facilitate changes in pathogen distribution and/
or survival, as projected for Nipah virus (Daszak
4.7 Urbanization as a challenge and
et al. 2013). Climate change also contributes to
ocean acidification, coral bleaching and diseases
an opportunity to manage ecosystem
in marine life, as reef-building coral species are services
threatened with extinction. These in turn have Urbanization, the demographic transition from
significant implications for the large biological rural to urban, is associated with shifts from an
communities that coral reefs support and that agriculture-based economy to mass industry,
sustain human health (Campbell et al. 2009). More technology and service.⁹ With the majority of the
extreme weather patterns and rising sea levels world’s population now living in urban areas and
(e.g. drought, flooding, early frost) may also be this proportion expected to increase, it is expected
detrimental to food and water security, especially that urban health should become a major focus
for populations dependent on subsistence farming at the intersection of global public health and
and natural water sources. Human populations conservation policy.¹⁰ Urbanization is also closely
may also suffer acute health impacts from extreme linked with the social determinants of health,
weather (e.g. heat or cold exposure injuries). including development, poverty and well-being.

While urbanization is often associated with

4.6 Demographic factors, including
increasing prosperity and good health, urban
migration
populations also demonstrate some of the world’s
In addition to the direct drivers of biodiversity most prominent health disparities, in both low-
loss, large-scale societal and demographic and high-income countries. Rapid migration from
changes, or intensified reliance on ecosystems rural areas as well as natural population growth are
for subsistence or livelihoods, often linked to putting further pressure on limited resources in
biodiversity changes, may also impact vulnerability cities, and in particular, in low-income countries.¹¹
to disease. For example, new human inhabitants
⁹ For the first time in history, the majority of the world’s population lives in cities, and this proportion continues to grow.
One hundred years ago, 20% of the people lived in urban areas. By 2010, this proportion increased to more than half. By
2030, it is expected that the number of people in urban areas will increase to 60%, and in 2050, to 70%. For example, see
World Health Organization Global Health Observatory (GHO) data: urban population growth. (www.who.int/gho/urban_
health/situation_trends/urban_population_growth_text/en/, accessed 30 May 2015).
¹⁰ To exemplify this trend and consequent shifts in health, WHO has been coordinating initiatives such as the “World Health
Day” and “Urban Health”.
¹¹ World Health Organization. Urban health. (http://www.who.int/topics/urban_health/en/, accessed 30 May 2015).

40 Connecting Global Priorities: Biodiversity and Human Health

Much of the natural and migration growth in and health in research and policy, the adoption
urban populations is among the poor. More than of multidisciplinary approaches that incorporate
1 billion people – one third of urban dwellers – live contributions from both the social and natural
in slum areas, which are often overcrowded and sciences is needed. The EcoHealth, One Health
are affected by life-threatening conditions (UNDP and “one medicine” approaches are part of a family
2005). In low-income countries, disparities will of approaches that aim to bridge human health
continue to rise as the combination of migration, and the health of other species or ecosystems
natural growth and scarcity of resources makes it (whether defined as disease outcomes, and/or the
more difficult to provide the services needed by functioning of an ecosystem/provisioning of its
city dwellers (UN-Habitat 2013).¹² Poorly planned services) to address complex challenges faced by
or unplanned urbanization patterns also have the global health and environmental communities.
negative consequences for the health and safety of In this volume, they are referred to as “One Health
people, including decreased physical activity and approaches”.
unhealthy diets, which lead to increased risks for
NCDs such as heart disease, cancer, diabetes and They are also closely related to the ecosystem
chronic lung disease (WHO 2010). approach adopted under the CBD.¹⁴ While
evolving from different sectors (the one medicine
Urbanization also creates new challenges for approach from veterinary and human medicine,
biodiversity conservation; the development of with a focus on comparative medicine and links
cities is one of the most important drivers of between livelihoods, nutrition and health; the
land-use change.¹³ Moreover, it was estimated Ecosystem and EcoHealth approach from the
that up to 88% of protected areas likely to be ecology and biodiversity communities, focusing
affected by new urban growth are in countries on ecosystem, societal and health links; and the
of low-to-moderate income (McDonald et al. One Health approach primarily from conservation
2008). While cities typically develop in proximity medicine, with a focus on public and animal
to the most biologically diverse areas (Seto et al. health, development and sustainability) (Zinsstag
2011), relatively little attention has been paid et al. 2011), at their core they share the common
to how cities can be more biodiverse or to the goal of a more comprehensive understanding of
importance of maintaining biodiverse ecosystems the ecosystem-based dynamics of health (e.g.
for human health (Andersson et al. 2014). Several socioecological systems) than can be yielded
health benefits can potentially be derived from through a single-species perspective alone.
integrating biodiversity into urban planning Given the integral links between biodiversity
schemes, and broader conservation and public and human health, these approaches consider
health policies. the connections between humans, animals and
the environment, and can thus promote a more
complete understanding of mutual dependencies,
5. INTEGRATING BIODIVERSITY
risks and solutions. These perspectives allow us to
AND HUMAN HEALTH: move beyond single-silo viewpoints (e.g. human
APPROACHES AND FRAMEWORKS or veterinary medicine exclusively) to a broader
In large part, the biodiversity and health and more upstream consideration of the drivers,
sectors have worked separately to achieve their detection, control and prevention of disease.
respective goals. To better integrate biodiversity

¹² World Health Organization. WHO Global Health Observatory (GHO) data: urban population growth. (www.who.int/gho/
urban_health/situation_trends/urban_population_growth_text/en/, accessed 30 May 2015).
¹³ For each new resident, rich countries add an average of 355 square meters of built-up area, middle-income countries 125
square meters, and low-income countries 85 square meters (McDonald et al. 2008).
¹⁴ https://www.cbd.int/ecosystem/

Connecting Global Priorities: Biodiversity and Human Health 41

 The value of One Health approaches is increasingly move from our currently reactive public health
being appreciated for infectious disease prevention measures to more preventive actions; similarly,
and control, seeing application for zoonotic this may benefit biodiversity and maintenance
diseases such as avian influenza and rabies (Gibbs of ecosystem services through consideration
et al. 2014), and based on the overlapping drivers of another potential aspect of impacts to an
of disease emergence and spread and biodiversity ecosystem.
loss, as well as domestic animal–wildlife and
human transmission cycles (GBO3; Jones et al. Involvement of the social sciences, including
2008). In addition, One Health and Ecosystem disciplines such as economics and anthropology,
approaches have wider potential applications and can help to further address socioecological
benefits, including the following: challenges, incorporating the social as well as
environmental determinants of health. Synergies
1) to help inform our understanding of the across these and other sectors may lead to cost–
health services provided by biodiversity, as well effective and more upstream disease prevention
as how anthropogenic changes to an ecosystem or and management strategies, as well as have
biodiversity may impact disease risks. Ecosystems implications for biodiversity. In addition to
may provide health-benefiting functions, such as interdisciplinary and cross-sectoral collaboration,
toxin remediation by filtration mechanisms in addressing the common challenges faced by the
wetlands (Blumenfeld et al. 2009). These functions global health and biodiversity conservation
and their underlying mechanisms may be missed communities also necessitates the engagement
when focusing on a single species; of many stakeholders, including governments,
civil society, nongovernmental and international
2) to provide important knowledge for organizations, as well as indigenous peoples
conservation and agricultural  efforts, given and local communities. Through integrated
the impacts of disease on agricultural and wild approaches such as the One Health approach,
species. Several disease risks for human and researchers, practitioners, policy-makers and
domestic animals also pose risks for biodiversity; other stakeholders are better able to unravel the
for example, while primarily maintained by intricate web of challenges that they jointly face,
domestic dogs, wildlife represents the majority and generate new insights and knowledge to find
of species susceptible to rabies, with some wild common solutions or, when these are not possible,
canid populations suffering severe declines from carefully assess and manage trade-offs (Romanelli
the disease (Machalaba and Karesh 2012); et al. 2014a,b).

3) for assessment of environmental health Recently, the Intergovernmental science-policy

exposures and outcomes; in addition to being Platform for Biodiversity and Ecosystem Services
possible links in the food chain, wildlife may serve has developed a conceptual framework linking
as sentinels for ecosystem changes and potential biodiversity, ecosystem services and human well-
human risks, as seen with Ebola (Karesh and Cook being (Díaz et al. 2015 a,b). The framework draws
2005) as well as toxin exposures (Buttke 2011). upon the Millennium Assessment framework, but
As shown in Figure 1, this may lead to earlier goes further in highlighting the role of institutions,
detection and possible prevention and mitigation and in explicitly embracing different disciplines
opportunities (Karesh et al. 2012). and knowledge systems (including indigenous
and local knowledge) in the co-construction of
Implementation of a One Health approach brings assessments of the state of the world’s biodiversity
multiple sectors together to view our shared health and the benefits it provides to humans.
across an ecosystem or specific disease challenge.
Employing multispecies disease surveillance or
risk analysis, with data sharing across human,
agriculture and environment experts, can help

42 Connecting Global Priorities: Biodiversity and Human Health

6. CONCLUSION: A THEMATIC ecosystem processes and services, and the
APPROACH TO COMMON ultimate impacts on human health, which are
not easily reduced to simple causal chains.
LINKAGES These links are frequently non-linear¹⁵ (Kremen
There is a pressing need to better understand 2005), difficult to predict, and are sometimes
the relationship between biodiversity and irreversible as biotic–abiotic interactions largely
public health, and this volume seeks to make a occur at the level of ecological processes rather
contribution to this imperative. We already know than in the delivery of the services themselves¹⁶
that biodiversity and corresponding ecosystem (Carpenter et al. 2009; Mace 2012). The difficulties
services, and public health intersect on numerous inherent in determining these causal links in no
fronts and these linkages are further explored in way diminishes the importance of seeking to
each of the thematic sections that follow. identify them.

This demands an understanding of biodiversity’s Understanding the links between the weakening
fundamental contribution to essential life- of ecosystem services and human health is
supporting services, such as air and water quality essential to shaping robust policies, expanding
and food provision. It also requires mapping the our scientific understanding of the health needs
role of biodiversity in human health on many of human communities, and to meeting new and
other fronts, including nutritional composition; existing challenges to public health in the face of
micro- and macronutrient availability and NCDs; global environmental change (McMichael and
its applicability in traditional medicine and Beaglehole 2000).
biomedical research that relies on plants, animals
and microbes to understand human physiology; Although the links between biodiversity and
and its relationship with processes affecting human health are fundamental, they are often
infectious disease reservoirs. We also need to diffused in space and time, and there are a number
further explore the role of microbial diversity in of actors that moderate the critical underlying
our internal biomes in human health and disease; relationships. To date, work at the biodiversity–
the threats of IAS to ecosystems and human health nexus has been insufficient, which may at
health; the positive feedback loops associated least in part be explained by these diffuse links.
with climate change; and many other associations. While One Health and similar approaches have
Our current state of knowledge of these and other begun to garner greater international acceptance,
themes is explored in greater detail in each of the primary focus of interventions in the public
the thematic sections included in Part II of this health sector continue to tend toward curative
technical volume. interventions rather than preventive (upstream)
interventions, which also consider the social and
While there has been considerable scientific environmental determinants of health. A powerful
progress in understanding these linkages, much argument can be made for the critical need to
more interdisciplinary and cross-sectoral work is incorporate these dimensions to improve public
needed to assess the full breadth of causal links health outcomes.
between environmental change, biodiversity,

¹⁵ As Carpenter et al. (2009) have noted, some drivers may affect human health without affecting biodiversity or the services
it provides, or some ecosystem processes may affect drivers directly.
¹⁶ This difficulty has been attributed to the fact that causal links can be non-linear or bypass some processes altogether.

Connecting Global Priorities: Biodiversity and Human Health 43

COMSTOCK/THINKSTOCK
PART II
Thematic Areas in
Biodiversity & Health
 3. Freshwater, wetlands,
SAM PHELPS/UNHCR/ FLICKR

biodiversity and human health

1. Introduction on unimproved water supplies that are believed
to have high levels of pathogen contamination
The centrality of water to human and ecosystem (WHO 2013; WHO and UNICEF 2012; Prüss-
health is readily apparent, yet often neglected. Ustün et al. 2014).¹ This reinforces the ongoing
Manipulating and adapting to changes in water importance of ensuring freshwater quality and
levels – dealing with water scarcity, flooding or supply from natural ecosystems for the control
storms – has been instrumental for civilizational and regulation of waterborne and water-related
survival, and this will continue as climate change diseases, in particular for the world’s poorest,
proceeds. The immense demand for water posed most vulnerable populations, who already carry
by modern industry, agriculture, aquaculture, a disproportionate portion of the global burden
forestry, mining, energy generation and human of disease.
consumption combine to exacerbate pressures
on water quality and quantity. Such threats to As discussed in this chapter and in the wide
freshwater and other aquatic ecosystems cannot breadth of scientific research in this area, the
be viewed in isolation from their impacts on ecosystems that sustain our water resources are
human health and well-being (Carr and Neary complex, and the often irreversible harm that they
2008). sustain can be linked to public health outcomes.
More judicious management and use of our water
In addition to direct health impacts (such as resources and aquatic ecosystems, coupled with
water-related illnesses), degradation caused by improved access to clean water, sanitation and safe
human activity (such as unsustainable agricultural energy sources are critical, intimately related goals
practices) also affects access to sanitation, increases (and challenges). As the last section of this chapter
the time invested in reaching water resources, and reiterates, these will demand the application of
hinders the capacity for local food production. a holistic, cross-sectoral approach, such as the
Based on recent World Health Organization ecosystem or One Health approach, and equally
(WHO) estimates, some 768 million people, the integrated solutions that transcend disciplinary,
majority from low-income countries, still rely sectoral and political boundaries.

¹ As defined by the WHO/UNICEF Joint Monitoring Programme for Water and Sanitation (Prüss-Ustün et al. 2014).

46 Connecting Global Priorities: Biodiversity and Human Health

2. Water resources: an essential bacteria, cryptosporidium, fungal pathogens)
ecosystem service of water resources, and preventing salinization
(Cardinale et al. 2012; CBD 2012). Analyses of
Freshwater is a provisioning ecosystem service flood frequency in low-income countries have
(MA, 2005a) and is important for several aspects found that the slope, amount of natural/non-
of human health. All terrestrial freshwater natural forest cover and degraded area explain
ecosystems, forests, wetlands, soil and mountain 65% of variation in flood frequency (Bradshaw et
ecosystems play a role in underpinning the water al. 2007), and is linked to the number of people
cycle, including regulating nutrient cycling and displaced and killed by such events, though
soil erosion (Russi et al. 2012; Coates and Smith associations with larger flooding events linked to
2012), and managing pollution (Schwarzenbach et extreme weather are not conclusive (van Dijk et al.
al. 2010; Horwitz et al. 2012). Many of the world’s 2009). This has implications for the development
major rivers begin in mountain highlands, and of improved disaster risk reduction strategies (see
more than half of the human population relies on also the chapter on resilience and disaster risk
fresh water flowing from these areas (MA 2005b). reduction in Part III of this volume).
It has been estimated that mountain ecosystems
contribute between 32% and 63% to the mean It is widely accepted that water purification services
annual river basin discharge, and supply around provided by biodiverse ecosystems underpin
95% of the total annual river discharge in some water quality, which is a universal requirement
arid areas (Viviroli et al. 2003). Biodiversity is for maintaining human health. For example, the
central to the ecological health of mountain hydrological, chemical and biological processes of
ecosystems and river basins. wetlands significantly ameliorate water quality.²
Groundwater is also a major source of water for
Water and soil conservation services of forests drinking and/or irrigation but also a potential
vary among biomes, landscapes and forest types. source of pathogenic microorganisms (Gerba
In many regions, forests improve surface soil and Smith 2005; Lapworth et al. 2012). While
protection and enhance soil infiltration, prevent biodiversity, including species diversity, may be a
soil erosion and landslides, protect riverbanks source of disease emergence, in some cases, high
against abrasion, and regulate microclimate species diversity in vertebrate hosts of vectors can
(CBD 2012; Naiman and Décamps 1997). For play a beneficial role by impeding dominance by
example, cloud forests can increase dry season particular species that act as key reservoirs of the
flow and total water yield (see e.g. Hamilton pathogens (Ostfeld and Keesing 2000).³
1995; Bruijnzeel 2004; Balmford and Bond 2005).
Natural forests enhance river water quality by
2.1 The role of species diversity
preventing soil erosion, trapping sediments,
and removing nutrient and chemical pollutants, The loss of species hinders the ability of
reducing microbial contamination (fecal coliform ecosystems to provide ecosystem services such

² For example, based on a thorough review of 169 studies examining hydrological functions of wetlands, Bullock and Acreman
(2003) reported that (1) wetlands significantly influence the global hydrological cycle, (2) wetland functions vary among
different wetland hydrological types, (3) floodplain wetlands reduce or delay floods, (4) some wetlands in the headwaters
of rivers increase flood flow volumes, sometimes increasing flood peaks, (5) some wetlands increase river flows during the
dry season, and (6) some wetlands, such as floodplain wetlands hydrologically connected to aquifers, recharge groundwater
when flooded. Mangrove wetlands are also effective in removing heavy metals from water (Marchand et al. 2012).
³ Increased species diversity can reduce disease risk in some cases by regulating the abundance of an important host species
(Rudolf & Antonovics 2005), or by redistributing vector meals in the case of vector-borne diseases (Van Buskirk and Ostfeld
1995; Norman et al. 1999; LoGiudice et al. 2003). In practice, transmission reduction can occur when adding species reduces
pathogen load or the pathogen’s titre (i.e. the concentration of an antibody, as determined by finding the highest dilution
at which it is still able to cause agglutination of the antigen) within the host (Keesing et al. 2006). For a more thorough
review on the role of biodiversity in disease emergence, see the chapter on infectious diseases in this volume.

Connecting Global Priorities: Biodiversity and Human Health 47

 as the filtering of pollutants. Numerous scientific Mazepova 1998) and plant species enhance the
studies have shown that filter feeders play an purity of water. For example, Moringa oleifera seeds
important role in the elimination of suspended and Maerua decumbens roots are used for clarifying
particles from water and its purification (Newell and disinfecting water in Kenya (PACN 2010). Yet,
2004; Ostroumov 2005, 2006). Bivalve molluscs habitat degradation and biodiversity loss often
of both marine and freshwater environments continue to hamper the ability of ecosystems to
have the ability to filtrate large amounts of water provide water purification services and to decrease
(Newell 2004; Ostroumov 2005). It has also been the quality of water available.⁵
found that molluscs may reduce pharmaceuticals
and drugs of abuse from urban sewage (Binellia 2.2 Social costs of impaired water
et al. 2014). The mussel species Diplodon chilensis quality
chilensis (Gray 1828), Hyriidae, native of Chilean
and Argentinean freshwater habitats, play a key Ecosystems play an essential role in regulating
role in reducing eutrophication, both by reducing water quantity and quality, which are also primary
total phosphorus (PO4 and NH4) by about one factors affecting food production, essential for
order of magnitude and also by controlling sustaining human health and livelihoods. For
phytoplankton densities. These mussels also example, wetlands directly support the health
contribute to increasing bottom heterogeneity and livelihood of many people worldwide through
and macrocrustacean abundance, and attract the provision of important food items such as
predatory fish. Thus, the mussels provide energy rice and fish (Horwitz et al. 2012). There are
and a nutrient source to the benthic and pelagic multiple mental health benefits of experiencing a
food webs, contributing to more rapid recycling natural environment, including, for example, the
of organic matter and nutrients (Soto and Mena contribution of spiritual and recreational values of
1999). wetlands to human psychological and social well-
being (see also chapter 12 in this volume).
Economic valuations of water as a habitat for
freshwater species diversity have been carried out.⁴ Impaired water quality results in significant social
The first estimate of the global values of ecosystem and economic costs, and ecosystem degradation
goods (e.g. food in the form of aquatic species), is a major cause of declines in water quality.
services (e.g. waste assimilation), biodiversity Rectifying poor-quality water through artificial
and cultural considerations yielded a value of US$ means (such as water treatment plants) requires
6579 x 109/year for all inland waters, exceeding substantial investment and operational costs. Left
the worth of all other non-marine ecosystems untreated, poor-quality water results in massive
combined (US$ 5740 x 109/year), despite the far burdens on human health, with women, children
smaller extent of inland waters (Costanza et al. and the poor being the most affected. Reflecting
1997). It follows that biodiversity conservation this priority, many protected areas and special
or restoration can be an effective, efficient and reserves have also been established to protect
cost–effective way of improving water quality water supplies, including fresh water for urban
and wastewater management. Plant and algae areas (Blumenfeld et al. 2009). For example, 33 of
species diversity enhances the uptake of nutrient 105 of the world’s largest cities source their clean
pollutants from water and soil (e.g. Cardinale et water from protected areas (Ervin et al. 2010; see
al. 2012), and some animals (such as copepod also Box 1).
Epischura baikalensis in Lake Baikal, Russia; see

⁴ Some of these studies also indicate that the services that such diversity provides are an essential driver of behavioural change.
See the section on behavioural change in the chapter on Sustainable Development Goals and the post-2015 Development
Agenda in Part III of this volume.
⁵ Moreover, while water quality can be monitored through chemical analysis, long-term trends in freshwater ecosystems may
be best monitored using the diversity of aquatic organisms (such as benthic invertebrates) as proxy indicators for measuring
water quality and ecosystem health.

48 Connecting Global Priorities: Biodiversity and Human Health

 Box 1. The Catskills: an ecosystem service for over 10 million people

The Catskills mountains were named a forest reserve in 1885 and are one of several important
examples of the fact that cost–e ective biodiversity and health co-bene ts are achievable. In the
three decades that followed the creation of the forest reserve, the high value of the life-supporting
services provided by the mountains became apparent; rather than investing large sums of money
on ltering water supplies, the state of New ork invested in creating reservoirs in the Catskills park,
beginning with the Ashokan Reservoir in 1898. Today, the New ork watershed provides the largest
un ltered water supply in the United States and provides an estimated 1.3 billion gallons of drinking
water to over 10 million residents daily. To this day, water quality standards mandated by the United
States (US) Environmental Protection Agency have been met without the need for water ltration
services, whose estimated costs would have run into billions of US dollars. It has been estimated that
New ork city avoided 6–8 billion in expenses over a 10 year period, by protecting its watersheds.

More recently, the important role of the Catskills as a breeding site for sh has also been recognized.
The Catskill Center for Conservation and Development was founded in 1969, and has been
advocating for the park since. To this day, the Catskills provide much of New ork State s highest-
quality drinking water as well as a relaxing recreational site for tourists and locals alike. E orts to ban
high-volume hydraulic fracturing for shale oil in the surrounding areas stem from concerns about its
impact on water quality. There are also serious concerns about the potential of drought related to
climate change having a signi cant impact on this vital ecosystem service.

Sources: Frei et al. 2002; MA 2005a; see also http://www.catskillmountainkeeper.org/no_time_to_stop_on_fracking

3. Dual threats to freshwater on infectious diseases in this volume), including

ecosystems and human health neglected tropical diseases such as trachoma,
onchocerciasis (Hotez and Kamath 2009),
Altered waterways and human development (e.g. lymphatic filariasis (Erlanger et al. no date), or
construction of dams, irrigation canals, urban guinea-worm disease (Fenwick 2006).
drainage systems, encouraging settlements close
to water bodies) can all provide benefits to human Freshwater ecosystems, such as rivers, lakes and
communities. However, related infrastructure wetlands, face disproportionately high levels of
may not only be costly to build and maintain, threats to biodiversity due largely to demands on
but is also often accompanied by new risks to the water (for a recent comprehensive review of the
environment (e.g. flood risk from degradation state of the world’s wetlands and their services to
of coastal wetlands) and public health, including people, see Garner et al. 2015). In some regions, up
emergence of disease (Horwitz et al. 2012; Myers to 95% of wetlands have been lost and two thirds
and Patz, 2009).⁶ These activities can diminish of the world’s largest rivers are now moderately
native biodiversity and increase waterborne or to severely fragmented by dams and reservoirs
water-related illnesses, such as schistosomiasis or (UNEP 2012). Freshwater species have declined
malaria (discussed in section 3; see also chapter at a rate faster than any other biome, with the

⁶ Waterborne diseases have been classified into four types: those spread through contaminated drinking water such as cholera;
those linked to poor sanitation such as typhoid; those transmitted by vectors reliant on freshwater bodies for at least one
stage in their life-cycles, such as malaria; and those that involve an aquatic animal to serve as an intermediate host, such
as schistosomiasis (e.g. Resh 2009).

Connecting Global Priorities: Biodiversity and Human Health 49

 sharpest decline in tropical freshwater biomes.⁷ hormones can lead to bioaccumulation, and have
More than one third of the accessible renewable been linked to endocrine disruption (Caliman and
freshwater on earth is consumptively used for Gavrilescu 2009) and reproductive dysfunction
agriculture, industrial and domestic purposes (Khan et al. 2005), all of which pose dual threats
(Schwarzenbach et al. 2006), which often leads to biodiversity and to the health of people who are
to chemical pollution of natural water sources, a reliant on freshwater resources (see also chapter
cause for major concern in many parts of the world on biodiversity, health care, and pharmaceuticals
(Schwarzenbach et al. 2010). It has been estimated in this volume). As discussed in subsection 3.4,
that approximately 67% of global water withdrawal other causes of bioaccumulation include human
and 87% of consumptive water use (withdrawal activities such as mining.
minus return flow) is for irrigation purposes
(Shiklomanov 1997; see also Box 2 case study 3.1: Eutrophication, human health and
on cotton). This has drained wetlands, lowered ecosystem healthƿ
water tables and salinized water sources through
intrusion and diminished water flows in key river Eutrophication, caused by the input of nutrients
systems; some of these, such as the Colorado delta in water bodies and characterized by excessive
(Glenn et al. 1996) and Yellow river, China (Chen plant and algal growth, is both a slow, naturally
et al. 2003) now periodically fail to reach the sea. occurring phenomenon and a process accelerated
The oceans are similarly challenged: an estimated by human activity (cultural eutrophication). The
38% decline in coral reefs has occurred since 1980, latter is caused by excessive point source (from
largely as a result of climate change, which is also a single identifiable source of contaminants) and
causing changes in ocean habitat and sea levels, non-point source (without a specific point of
concurrent with ocean acidification (UNEP 2012). discharge) pollution; the most common causes
include leaching from fertilized agricultural
As discussed in the subsections that follow, threats areas, sewage from urban areas and industrial
to water resources and ecosystems (both freshwater wastewater.
and marine) often present equally significant
threats to human health. Other human activity, The input of nutrients most commonly associated
such as the use of pharmaceuticals or antibiotics, with eutrophication – phosphorus (e.g. in
dam construction and mining activities also have detergents) and nitrogen (e.g. agricultural run-
significant direct and indirect, albeit unintended, off) – into lakes, reservoirs, rivers and coastal
consequences on water resources and public marine ecosystems, including coral reefs, have
health. Ecotoxicological data on environmental been widely recognized as a major threat to both
exposure to pharmaceuticals and persistent water ecosystems and human health. In freshwater
substances such as anti-inflammatory drugs, environments, cultural eutrophication is known
antiepileptics, beta-blockers, antidepressants, to greatly accelerate algal blooms. In marine
antineoplastics, analgesics and contraceptives and estuarine systems, the enhanced inputs of
indicate a range of negative impacts on freshwater phosphorus and nitrogen often result in a rise of
resources, ecosystems, living organisms and, cyanobacteria and dinoflagellates. The effects of
ultimately, some aspects of human health (see eutrophication include the following:
Santos et al. 2010; Lapworth et al. 2012). The
use of sex hormones and veterinary growth • toxic cyanobacteria poisonings (CTPs)

⁷ Based on data on the freshwater Living Planet Index (LPI), the decline in freshwater species was greater than any other
biome between 1970 and 2008, although global terrestrial marine indices have also sharply declined. The freshwater LPI
considers 2849 populations of 737 species of fish, birds, reptiles, amphibians and mammals found in temperate and tropical
freshwater lakes, rivers and wetlands. Among them, tropical freshwater species declined more than any other biome. Data
prior to 1970 are not captured due to insufficient data (WWF 2012). For further discussion on the global status of species
declines, see also Global Biodiversity Outlook, fourth edition (CBD 2014).
⁸ Shaw et al. 2003; Carmichael, 2001; EEA 2005; Shaw and Lam 2007; Chorus and Bartram 1999; WHO 1999

50 Connecting Global Priorities: Biodiversity and Human Health

• increased biomass of phytoplankton and Medical facilities are only one of several potential
macrophyte vegetation routes of exposure to human toxicity from
cyanotoxins; others include the recreational
• increased biomass of consumer species use of lakes and rivers, and the consumption of
drinking water, algal dietary supplements and
• shifts to bloom-forming algal species that food crops, among others. In addition to Brazil,
might be toxic or inedible health problems attributed to the presence of
cyanotoxins in drinking water have been reported
• increase in blooms of gelatinous zooplankton in a number of countries, including Australia,
(marine environments)
China, England, South Africa and the United
States.
• increased biomass of benthic and epiphytic
algae
3.2 Proliferation of cyanobacteria
• changes in species composition of macrophyte caused by eutrophication
vegetation
The discharge of nutrients in waterways can lead
• decline in coral reef health and loss of coral reef to eutrophication. Under eutrophic conditions,
communities nutrient loading indirectly decreases the amount
of oxygen in the water and eventually eliminates
• increased incidence of fish kills certain species. In oxygen-depleted water, fecal
pathogens may proliferate and the risk of enteric
• reduction in species diversity of harvestable disease transmission increases (Fuller et al. 1995).
fish and shellfish In addition, wherever conditions of temperature,
light and nutrient status are conducive, surface
• water treatment and filtration problems waters may host increased growth of algae or
cyanobacteria. This phenomenon is referred to
• oxygen depletion as an algal or cyanobacterial bloom (see section
3.1). Problems associated with cyanobacteria
• decreases in perceived aesthetic value of the are likely to increase in eutrophic areas, such as
water body. those with high sewage discharge and agriculture
practices (WHO 1999). Species of cyanobacteria
It was found that eutrophication occurs in
may produce toxins that affect the neuromuscular
approximately 54% of Asia-Pacific, 53% of
system and liver, and can be carcinogenic to
European, 48% of North American, 41% of
vertebrates, including humans.
South American and 28% of African lakes.
Eutrophication can cause considerable harm to Among the 14 000 species of continental algae,
freshwater, marine ecosystems, and terrestrial about 2000 are cyanobacteria and 19 genera
ecosystems and the life that inhabits them; produce toxins. Cyanotoxins show specific toxic
these impacts can range from wild and domestic mechanisms in vertebrates, some of which
animal illness and death to equally far-ranging are strong neurotoxins (anatoxin-a, anatoxin-
consequences for human health. For example, a(s), saxitoxins) and others are primarily
in 1996, a routine haemodialysis treatment toxic to the liver (microcystins, nodularin
at a dialysis centre in Caruaru, Brazil led to an and cylindrospermopsin). Microcystins are
outbreak of cyanotoxin human toxicosis. Among geographically most widely distributed in
130 patients affected, almost 90% experienced freshwaters (WHO 1999). They bioaccumulate in
visual disturbances, nausea and vomiting, 100 of common aquatic vertebrates and invertebrates,
them developed acute liver failure and 70 died; including fish, mussels and zooplankton (Ibelings
53 of these deaths were attributed to what is now and Chorus 2007). Cases were reported in the Latin
known as the “Caruaru syndrome.” American and Carribbean region. For example, in

Connecting Global Priorities: Biodiversity and Human Health 51

 UNITED NATIONS PHOTO / FOTER / CC BY-NC-ND
a hypertrophic reservoir in Argentina, if a 70 kg similarly be low if control measures are in place for
person would consume 100 g of fish (Odontesthes times of bloom formation. If regular monitoring
bonariensis), the equivalent of approximately of source phytoplankton is in place, waters
0.49 mg/kg body weight/day would be consumed presenting no significant cyanotoxin risk may
(Cazenave et al. 2005), which is in excess of the be easily identified (see review in WHO 1999).
range of the seasonal tolerable daily intake (TDI) Substantially less is known about the removal of
(0.4 mg/kg/day). In Brazil, concentrations of neurotoxins and cylindrospermopsin than about
microcystins in edible parts of Tilapia rendalli were microcystins, thus toxin monitoring of treatment
examined during the cyanobacterial bloom season. steps and finished water is especially important.
Concentrations varied between 0.0029 and 0.337 Methods such as adsorption by some types of
mg/g muscle tissue. Consumption of 300 g of fish granular activated carbon and oxidation can be
with this highest concentration would exceed the effective in cyanotoxin removal (WHO 1999).
seasonal TDI by four times. The amount of toxin in
Tilapia livers has been found to reach levels as high 3.3 Multiresistant bacteria: new
as 31.1 mg/g wet weight (Freitas de Magalhães et approaches in sewage treatment
al. 2001), so that in a typical meal, an adult could
be exposed to hundreds of times the seasonal The use of antibiotics in hospitals, for swine and
TDI. Common advice given by water authorities poultry production, and in fish farms can result
is that the viscera of the fish should not be eaten, in routes of dissemination of multiresistant
but caution should be exercised in all cases where bacteria and their genes of resistance into the
major toxic blooms occur. environment, thus contaminating water resources
and having a serious negative impact on public
Where bloom formation is well characterized health. Antibiotics are widely used to protect the
in terms of annual cycles, the health risk may health of humans and domesticated animals, and/

52 Connecting Global Priorities: Biodiversity and Human Health

or to increase the growth rate of animals as food of organic matter, which can remobilize Hg from
additives. The use of antibiotics may accelerate the soil into the food chain (Passos and Mergler
the development of antibiotic resistance genes 2008). ASGM activities account for approximately
(ARGs) in bacteria and other pathogens, which 12% of all gold produced worldwide (Veiga et
pose health risks to humans and animals (Kemper al. 2014), and to produce 1 mg of gold, 2.5–3.5
2008; see also the chapter on health care and mg of Hg are used, of which approximately 50%
impact of pharmaceuticals on biodiversity in this reaches streams and rivers as suspended sediment
volume). The introduction of these new genes can (UNEP 2013). Metallic Hg is also emitted into the
alter the biology of pathogens because ARGs can atmosphere as a result of ASGM activities, and is
be transmitted to other species of bacteria (Heuer reduced into inorganic Hg and precipitated into
et al. 2002; Tennstedt et al. 2003). Therefore, even terrestrial and aquatic ecosystems.
common strains of pathogens may incorporate
these genes and become resistant to antibiotics. While Hg remains in the soil, it is often in its
The only way to detect multiresistant bacteria is by inorganic form, less toxic, but when it reaches
performing a DNA microarray. However, this kind water courses, microorganisms may transform
of procedure is not yet common in health centres. it to a more toxic form, methyl Hg (Hacon and
Azevedo 2006). Methyl Hg can bioaccumulate
Perhaps the most effective and direct approach in the tissue of organisms and through the food
to reduce the possibility of the introduction and chain, as they are consumed by other species. It
spread of ARGs is the controlled use of antibiotics can also reach human populations through fish
in health protection and agriculture production. consumption (Passos and Mergler 2008). In
New and effective wastewater treatment processes human populations, methyl Hg is neurotoxic and
are also needed to improve removal efficiency of prenatal exposure can affect brain development,
ARGs in sewage treatment plants. Additionally, even at low doses of exposure⁹. Children exposed
irrigation using wastewater has to be discussed to methyl Hg may have delayed and impaired
thoroughly, considering possible introduction of neurodevelopment, and exposed adults may have
ARGs in the soil and groundwater (Zhang et al. impaired motor coordination, visual fields, speech
2009). and hearing (UNEP, UNICEF, WHO 2002).

Methyl Hg was found in high concentrations

3.4 Bioaccumulation: the impact of
in fish and shellfish, which are also the primary
mining
sources of exposure to human populations (Veiga
Many mining activities discharge mercury et al. 1994; Porvari 1995; Fearnside 1999). In
(Hg) and methyl Hg in aquatic ecosystems, the Guri hydroelectric reservoir in Venezuela,
thereby contaminating water, ecosystems and from 219 fish samples, 93 specimens showed
aquatic species with a correspondingly negative levels above 0.5 ppm Hg and up to 90% of the
repercussion on human health. (For a recent most appreciated piscivore fish in the region
review of freshwater fish species in Africa please (Rhaphiodon vulpinus) showed average Hg levels
see Hannah et al. 2015.) of 2.7 ppm (0.17–8.25 ppm) (UNIDO 1996) –
higher than those found in detritivorous and
There are many ways by which Hg can reach herbivorous fish species. Contamination through
aquatic ecosystems. Major anthropogenic sources methyl Hg is particularly high in the Amazonian
are artisanal and small-scale gold-mining (ASGM) region. Several Amazonian communities have
activities, which use Hg to amalgamate with gold Hg levels considered to be critical for optimal
(Veiga et al. 2014), and deforestation and burning neurological development. Dietary Hg intake has

⁹ For a summary of the health impacts associated with mercury exposure and the identification of potential pathways for
strategic action see also World Health Organization: http://www.who.int/phe/news/Mercury-flyer.pdf. For guidance on
assessing the risk of mercury exposure to humans see also WHO-UNEP (2008), available at http://www.who.int/foodsafety/
publications/chem/mercuryexposure.pdf?ua=1

Connecting Global Priorities: Biodiversity and Human Health 53

 been estimated to be 1–2 μg/kg/day, considerably Natural vegetation cover in buffers along rivers is
higher than the WHO recommendation (0.23 μg/ critical to the regulation of water flow, retention of
kg/day) (Passos and Mergler 2008). nutrients, and capture of pollutants and sediments
across landscapes (reviewed in Osborne and
The reduction or elimination of Hg use in Kovacic 1993). The removal of trees and natural
ASGM has been receiving widespread attention habitats in landscapes affects soil directly, as well
(Veiga 2014). Less damaging options include as the quantity and quality of water draining
amalgamating a gold concentrate rather than the from agricultural systems. Riparian buffers of
whole ore and using “mercury-free artisanal gold”, non-crop vegetation are widely recommended as
in which gold is isolated by centrifuges and the a tool for removing non-point source pollutants,
gangue materials magnetically removed (Drace particularly nutrients (nitrates, phosphorus,
et al. 2012). Awareness and education about Hg potassium) from agricultural areas, especially
poisoning in ASGM communities is also essential those carried by surface run-off (Lee et al. 2003;
to ensuring adherence to such changes in ASGM Brüsch and Nilsson 1993; Daniel and Gilliam
technology. 1996; Glandon et al. 1981; Nakamura et al. 2001).
In field studies, even buffers of switchgrass along
4. Impacts of agriculture on water fields removed 95% of the sediment, 80% of the
total nitrogen (N), 62% of the nitrate nitrogen
ecosystems and human health (NO3-N), 78% of the total phosphorus (P), and
Unsustainable agricultural practices have 58% of the phosphate phosphorus (PO4-P). If the
significant impacts on human health, and water buffer included woody species, it removed 97%
pollution from fertilizers, pesticides and herbicides of the sediment, 94% of the total N, 85% of the
remains a serious problem (see the chapter on NO3-N, 91% of the total P, and 80% of the PO4-P
agricultural biodiversity and food security in in the run-off (Lee et al. 2003).
this volume). Better use of ecosystem services,
underpinned by biodiversity, in agricultural Nutrient run-off from agricultural sources into
production systems provides considerable waterways has been blamed for the production of
opportunities to reverse these impacts on health hypoxia, popularly termed (aquatic) “dead zones”
while simultaneously improving food security. (Diaz 2001). These destroy local fisheries in many
coastal areas, which communities rely on for the
Agriculture accounts for about 70% of global intake of protein and other nutrients. Dead zones
water use, and physical water scarcity is already a have now been reported in more than 400 systems,
problem for more than 1.6 billion people (IWMI affecting a total area of more than 245 000
2007). It is increasingly recognized that the square kilometres (Diaz and Rosenburg 2008;
management of land and water are inextricably see Figure 1). These are concentrated along the
linked (e.g. DEFRA 2004). In England, for eastern seaboard of North America, and European
example, up to 75% of sediment loading in rivers and Japanese coastlines, where human ecological
can be attributed to agriculture, while 60% of footprints and agriculture intensities are highest
nitrate pollution and 25% of phosphates in surface (Diaz and Rosenburg 2008, see Figure 1).
waters originates from agriculture (DEFRA 2007).
Agricultural practices can also contribute to the Agricultural practice and its demand for water
spread of water-related and waterborne disease. have reduced both the amount and quality of
For example, significant E. coli loads have been drinking water available for human consumption.
found in run-off from land grazed by cattle and At the same time, lack of irrigation in many low-
treated with livestock wastes (Oliver et al. 2005), income countries is a leading cause of poor crop
all of which impact the quality of water for human production and yield gaps (Lobell et al. 2009). By
consumption and use. 2002, irrigated agricultural land comprised less
than one fifth of all cropped area but produced
40–45% of the world’s food (Döll and Siebert

54 Connecting Global Priorities: Biodiversity and Human Health

2002). Integrated water management practices reduce the negative impacts of current water use
that maintain and use biodiversity to support practices on human health and contribute to its
ecosystem services that improve water use improvement.
efficiency and water quality will be needed to

ǡǤǢǰǭǠɻ Eutrophication-associated dead zones, 2008

Hypoxic system
Human footprint
0- 1
1 - 10
10 - 20
20 - 30
30 - 40
40 - 60
60 - 80
80 - 100

Global distribution of over 400 systems that have scienti cally reported accounts of being eutrophication-associated dead zones.
Source: Diaz and Rosenberg 2008

Box 2. Case study: Water consumption and cotton production

Cotton is a particularly important global crop and the most important natural bre used in textile
industries worldwide, accounting for 40% of textile production, but it is also a major consumer of
water: over half of all cotton production is dependent on heavy irrigation (Soth et al 1999; Chapagain
2006). In the period 1960–2000, an environmental disaster unfolded as the Aral Sea in Central
Asia lost approximately 60% of its area and 80% of its volume (Glantz 1998; Pereira et al. 2002)
as a result of the annual withdrawal of water from its main feeder rivers, the Amu Darya and the Syr
Darya, for cotton agriculture in the desert (Cosgrove and Rijsberman 2014). This depletion of water
a ected local sheries and livelihoods (Micklin 2007), as well as water quality both from harvesting
and processing (Bednar et al. 2002; Chapagain et al. 2006). As cotton is a global commodity, its
consumption takes place in areas remote from its growth. One study concluded that about 84% of
the “water footprint” of cotton consumption in Europe is located outside the continent, with “major
impacts in India and Uzbekistan” (Chapagain et al. 2006). E orts to improve the production of cotton
have focused on the development of transgenic Bacillus thuringiensis (Bt) cotton, which reduces
insecticide use (Cattaneo et al. 2006), as well as improvements in water e ciency through drip
irrigation furrow, and other e orts to reduce the negative environmental and human health impacts.
Despite these e orts, cotton production, itself a source of agricultural biodiversity reduction, remains
a major consumer of global freshwater with a pronounced impact on freshwater biodiversity.

* Whereas the term “ecological footprint” denotes the area (ha) needed to sustain a population, the “water footprint” rep-
resents the water volume (cubic metres per year) required, including dilution water necessary to restore polluted water to
internationally agreed water quality standards.

Connecting Global Priorities: Biodiversity and Human Health 55

 5. Waterborne and water-related of them among young children (Prüss-Üstün et al.
diseases 2008; WHO 2003a).¹²

Long before the advent of modern medical care, Factors that have been found to increase the
industrialized countries decreased their levels of water- incidence of waterborne diseases include
related disease through good water management. urbanization and high population densities
Yet, even in these countries, outbreaks of waterborne of people, agriculture and industry (Patz et al.
disease continue to occur, sometimes with lethal 2004). Habitat destruction or modification also
consequences. In developing countries, water-related plays a major role. For example, dam-related
disease blights the lives of the poor. Gro Harlem reservoir construction increases the prevalence
Brundtland, former WHO Director-General, 2001. and intensity of human schistosomiasis in Africa
(e.g. N’Goran et al. 1997; Zakhary 1997) and
Surface freshwaters are among the most altered elsewhere (Myers and Patz 2009), as described in
ecosystems on the planet and, coupled with Box 3. Climate change and the spread of aquatic
associated biodiversity loss, have been linked invasive species (see section 5.1) may facilitate
to increased incidence of infectious diseases, transmission of human pathogens (such as the
including waterborne illnesses (Carpenter et al. Asian tiger mosquito Aedes albopictus) and can
2011; see also the chapter on infectious diseases transmit viruses such as dengue, LaCrosse, West
in this volume for a detailed discussion). Although Nile and chikungunya (Benedict and Levine 2007).
the global disease burden of many formerly
devastating waterborne illnesses (e.g. cholera, A strong relationship between the human
typhoid fever) has declined considerably, others development index (HDI), access to drinking
continue to affect a significant proportion of the water services and sanitation with mortality by
global population, especially in the world’s lowest- diarrhoea was found in some parts of the world,
income regions, such as sub-Saharan Africa, where particularly low-income countries. Almost half
the highest concentration of poverty occurs (Hotez of the population in these countries is at risk
and Kamath 2009). of exposure to waterborne diseases, including
gastroenteric diseases such as dysentery,
The presence of pathogenic (disease-causing) giardiasis, hepatitis A, rotavirus, typhoid fever and
microorganisms in freshwater can lead to the cholera. Less economically developed countries
transmission of waterborne diseases,¹⁰ many of such as Haiti, for example, had the lowest water
which cause diarrhoeal illness, a leading cause of and sanitation coverage levels, coupled with the
mortality in children under 5 years of age, and lowest HDI values and highest child mortality
among the most prevalent waterborne illnesses, rates, in contrast to Chile, Costa Rica, Cuba and
particularly in low- and middle-income countries Uruguay, among others, which had higher values
(Prüss-Ustün et al. 2014; WHO 2013; WHO and and coverage (PAHO 2012).
UNICEF 2012; UNESCO 2009; Prüss-Üstün and
Corvalán 2006).¹¹ Unsafe drinking water itself Human alteration of hydrological regimes has
accounts for 88% of diarrhoeal disease worldwide often been motivated by concerns for human
(including cholera, typhoid and dysentery) and health and well-being (Myers et al. 2013). While
results in 1.5 million deaths each year, the majority altered waterways (e.g. dams, irrigation canals,
urban drainage systems) have indeed provided

¹⁰ The contamination of surface waters with fecal material from humans, livestock or wildlife has been identified as an
important (albeit not exclusive) pathway for the transmission of waterborne diseases (Prüss-Üstün and Corvalán 2006;
US EPA 2003; Ragosta 2010).
¹¹ See also http://www.who.int/mediacentre/factsheets/fs330/en/; http://www.cdc.gov/healthywater/wash_diseases.html
¹² Children under 5 years of age living in poor dwellings with inadequate access to health services are the most susceptible
to diarrhoeal disease and account for the overwhelming majority of all deaths attributed to these diseases (WHO 2004).
Relatively little is known about the pathogens that account for diarrhoeal disease themselves (Yongsi 2010).

56 Connecting Global Priorities: Biodiversity and Human Health

valuable benefits to human communities (e.g. vectors of schistosomiasis. This disease affects
energy, employment, access to food), they are over 200 million people worldwide, of which 88
costly to build and maintain, have frequently million are under 15 years of age, with the heaviest
been accompanied by unintended consequences to infections being reported in the 10–14 years’
ecosystems¹³ and have had negative repercussions age group in Africa and South America (UNEP,
on public health, in some cases considerably UNICEF & WHO 2002).
increasing the availability of habitats for disease
organisms and their vectors (de Moor 1994) Other species, such as aquatic plants, are also
and exacerbating waterborne disease outbreaks affected by shifting environmental conditions,
(Dudgeon et al. 2006; Hotez and Kamath 2009; which in turn may favour mosquito breeding,
Myers et al. 2014). including mosquitoes of the genus Anopheles,
potential vectors of a protozoan – genus
It has been estimated that some 2.3 billion people Plasmodium – causing malaria (Thiengo et al.
suffer from diseases related to water, and diseases 2005). Many studies have reported the increase
transmitted by freshwater organisms kill an in malaria cases after the construction of large
estimated 5 million people per year. Unsustainably dams. From the Chiapas hydroelectric power
managed ecosystems, such as wetlands, may plant in Mexico to Itaipu Binacional in Brazil/
harbour waterborne and vector-borne pathogens Paraguay, thousands of malaria cases were linked
such as plasmodium and human schistosoma; the to dam construction (Couto 1996). In South
latter is described in Box 3 (Horwitz et al. 2012; America, almost 60% of all reservoirs were built
Dale and Connelly 2012; Dale and Knight 2008; since the 1980s. Prevalence of other diseases
Fenwick 2006). may also increase with river damming. In the
area of influence of the Yacyreta dam (Paraná
The habitat degradation that often accompanies River, Argentina/Paraguay), Culicoides paraensis
human development activities, and corresponding mosquitoes were found (Ronderos et al. 2003).
simplification of natural species assemblages, have These are known vectors of Oropouche fever –
been found to foster the proliferation of disease which registered epidemics in many urban centres
vectors. The maintenance of natural freshwater in the Pará State of Brazil (Barros 1990).
communities and ecosystem integrity, where
possible, may correspondingly contribute to a Biological and chemical threats (e.g. agricultural
reduction in conditions for the transmission of run-off, pharmaceuticals) to water resources,
diseases, including those related to water (Dudgeon as well as the development of water-related
et al. 2006). The development of dams and infrastructure and urbanization, have also had
irrigation projects, for example, can contribute to their share of detrimental impacts on both
expanding habitats for mosquitoes, aquatic snails biodiversity and human health by diminishing
and flies, which can spread disease among resettled native biodiversity and sometimes increasing the
agricultural populations. River damming changes potential for waterborne illnesses.
physical and chemical conditions, altering the
original biodiversity (Tundisi et al. 2002). Reduced The global community has widely acknowledged
water current creates favourable conditions for the importance of access to clean water, sanitation
molluscs from the genus Biomphalaria, potential and hygiene as critical development interventions

¹³ Human activities can hamper the ecological balance of wetlands and thereby alter existing disease dynamics or introduce
novel disease problems (Horwitz et al. 2012). For example, flood risk may also increase as a result of degradation of coastal
wetlands, demonstrated with Hurricane Katrina’s impact on New Orleans, and extant deforestation exacerbated the health
impact of the 2010 earthquake in Haiti.

Connecting Global Priorities: Biodiversity and Human Health 57

 in several goals and targets of the Millennium life-supporting services that sustain our water
Development Goals (MDGs).¹⁴ It was estimated (and other) resources.
that over one sixth¹⁵ of the world’s population
did not have access to safe water at the time The provision of clean water and sanitation to the
the MDGs¹⁶ were adopted (Prüss-Üstün et al. world’s poor, who are particularly vulnerable and
2004). While considerable progress had been ill-equipped to cope with further loss of ecosystem
achieved by 2010,¹⁷ much work is still needed to services, garners health benefits. The sustainable
meet global targets, particularly in low-income management of resources can also alleviate pres-
regions, including sub-Saharan Africa (WHO sures caused by the unsustainable use of wetland
and UNICEF 2012). Subjacent to the fulfilment and other ecosystems, reducing waste flows while
of these objectives is the need to sustainably also improving the overall quality of fresh and
manage the ecosystems that provide the critical coastal waters essential to health and well-being.

Box 3. Ecosystem disturbance and waterborne disease: the case of schistosomiasis

While ecosystems can act as disease reservoirs, there is abundant scienti c literature to support
the claim that these cannot be viewed in isolation from the human activity that alters them.
Schistosomiasis is a waterborne disease that a ects some 200 million people worldwide. It can
cause grave damage to internal tissues, including the liver, intestines and bladder, and has been
found to undermine growth and development in children.

While schistosomiasis has been closely related to ecosystem disruption and the unsustainable use of
biological resources, it is also sustained in a setting of poverty. A systematic review of schistosomiasis
and water resource development carried out by Steinmann et al. (2006) estimated that among
200 million infected, an estimated 93% (192 million cases) occur in sub-Saharan Africa, including
29 million in Nigeria, 19 million in the United Republic of Tanzania, and 15 million each in the
Democratic Republic of the Congo and Ghana. Approximately 76% of the population in sub-Saharan
Africa lives near rivers, lakes and other contaminated water bodies.

Schistosomiasis is caused by parasitic worms (Schisotoma spp.), which spend a portion of their life-
cycle in some species of freshwater snails that act as intermediate hosts for the disease. People
become infected with the parasitic worms when they enter contaminated waters and the parasitic
worms leave their host to penetrate human skin, thus infecting the subject. In Lake Malawi, it was
found that over shing caused an increase in abundance of Bulinus nyassanus, a snail species that
acts as the intermediate host of the schistosome parasite.

¹⁴ See MDG 7 (Ensure environmental sustainability) Targets 9, 10, 11; MDG 4 (Reduce child mortality) Target 5; MDG 6
(Combat HIV/AIDS, malaria, and other diseases) Target 8.
¹⁵ It is estimated that 1.1 billion people did not have access to safe drinking water and 2.4 billion lacked access to improved
sanitation when these goals and targets were first adopted.
¹⁶ When the MDGs were first adopted, approximately 3.1% of annual deaths (1.7 million) and 3.7% of the annual health
burden of disability-adjusted life years (DALYs) worldwide (54.2 million) were attributed to unsafe water, sanitation and
hygiene, all of them in low-income countries and 90% of them in children (WHO 2003). Major enteric pathogens in affected
children include: rotavirus, Campylobacter jejuni, enterotoxigenic Escherichia coli, Shigella spp. and Vibrio cholerae O1, and
potentially enteropathogenic E. coli, Aeromonas spp., V. cholerae 0139, enterotoxigenic Bacteroides fragilis, Clostridium difficile
and Cryptosporidium parvum (Ashbolt 2004; WHO 2003a).
¹⁷ By 2010, some 884 million people still did not use improved sources of drinking water (WHO 2010a). Additionally, 2.6 billion
people did not use improved sanitation.

58 Connecting Global Priorities: Biodiversity and Human Health

 In Cameroon, schistosomiasis has been associated with an increase in deforestation. The increase in
the amount of sunlight penetration, altered water rates and ow levels, and increase in vegetation
growth caused by deforestation altered the ecology of freshwater snail populations in the area.
Bulinus truncatus, a competent host for the parasitic worm Schistosoma haematobium (responsible for
an estimated two thirds of all schistosoma infections in sub-Saharan Africa and an important cause of
severe urinary tract disease), displaced another type of freshwater snail, Bulinus forskalii, which itself
hosted a non-pathogenic schistosome but was less able to thrive in cleared habitat.

In Kenya, the prevalence of urinary schistosomiasis in children rose to a staggering 70% ten years
after the start of the Hola irrigation project (prevalence was 0% prior to the start of the project). The
irrigation project led to the introduction of a new snail vector well suited to the altered environment.
The prevalence of schistosomiasis further increased to 90% by 1982. (Malaria is another disease that
has been closely associated with the construction of dams and irrigation projects.)

In the Nile Delta of Egypt, dam construction in 1965 also led to an increase in schistosomiasis by
increasing the habitat for Bulinus truncates, leading to an increase of almost 20% in the 1980s from
6% prior to dam construction. The increase in disease prevalence was even greater in other parts of
the country.

Sources: Myers and Patz 2009 (and references therein); Evers 2006; Molyneux et al. 2008; Steinmann et al. 2006; Hotez and
Kamath 2009.

5.1 Aquatic invasive alien species that eutrophication also played a role in the mass
extinction event recorded by observers in Lake
Invasive alien species (IAS) are a major threat to
Victoria, and that the Nile perch is now on the
biodiversity (Simberloff et al. 2005; McGeoch et
decline (Stearns and Stearns 2010; Goudswaard
al. 2010). Aquatic invasive species are among the
et al. 2008). While the introduction of alien
most pernicious, often travelling across the globe
species may sometimes be beneficial, the case of
before introduction. While some introductions are
the Nile perch remains a very good example of
purposeful, such as the introduction of the Nile
how irreparable harm can be done to a complex
perch (Lates niloticus) to Lake Victoria, which has
ecosystem and why commercial introductions
caused disastrous and irreparable harm, many
should be viewed with the utmost caution for
others are incidental. The perch was introduced
potential consequences.¹⁸
for commercial reasons, and it proceeded to
dominate the lake and led to the extinction of In contrast, many aquatic invasives have arrived
up to 200 species of endemic haplochromine after surreptitiously travelling on cargo ships and
cichlids (Goldschmidt et al. 1993). Recent oil tankers, which use ballast water to balance
evidence suggests that there has been some their hulls.¹⁹ The zebra mussel worked its way
recovery of aquatic biodiversity in the area, and into the North American Great Lakes via Russia

¹⁸ Invasive species Limnoperna fortunei (Dunker 1857), Mytilidae, is considered as a major problem for hydroelectrical power
plants because of their high growth rates, which obstruct the pipes. However, their filtering rates are among the highest for
suspension-feeding bivalves, reaching as high as 125–350 ml individual–1 h–1. The high filtration rates, associated with the
high densities of this mollusc (up to over 200 000 ind m–2) in the Paraná watershed – where there are many dams, including
Itaipu Binacional, one of the largest in the world – suggest that its environmental impact may be swiftly changing ecological
conditions in the areas colonized, which include four countries, Brazil, Paraguay, Uruguay and Argentina (Sylvester et al. 2005).
¹⁹ Other means of accidental introduction include pet, aquaculture and aquarium releases or escapes, seaway canals, and even
irresponsible research activities.

Connecting Global Priorities: Biodiversity and Human Health 59

 in 1986, while the comb jelly went in the opposite on struggling native species populations, further
direction, from the United States (US) to the reinforcing the spread of aquatic IAS through
Caspian Sea, with devastating impacts on fisheries common vectors such as ship traffic and tourism.²²
there (Chivian and Bernstein 2008: 49). The zebra For example, melting sea ice opens new vectors for
mussel has had a complex impact on the water bioinvasion in the Arctic (and indeed, melting ice
quality of the Great Lakes. While these bivalves can itself can release previously unknown pathogens,
give lake water a clearer appearance as they filter locked into ice formations for thousands of years,
various particles, including some forms of algae, into the Arctic environment). Increasing levels of
they also consume phytoplankton (the building photo-degraded microplastic can also serve as a
block of the marine food system), and they give vector for microbial communities (Zettler et al.
harmful blue–green algae a competitive advantage, 2013).
contributing to new dead zone growth.²⁰ Ricciardi
(2006) estimated that one new species had been While the impact of IAS on biodiversity and
discovered in the North American Great Lakes ecosystems is well documented (e.g. Charles
every 28 weeks during the 1990s; while Cohen 2007), resultant impacts on human health are
and Carlton (1998) found even higher rates an important area for further research (see Pysek
of introduction in the San Francisco Bay area. and Richardson 2010). Deleterious waterborne
International efforts to prevent ballast water- pathogens, such as those that cause cholera, are
related introductions, through the International often classified as invasive species (see the chapter
Maritime Organization and others, are having on infectious diseases in this volume). Other
some impact, but this remains a serious focus of aquatic invasive species, such as the zebra mussel
concern. Plants can be aquatic invasive species described above, not only disrupt local food
as well: witness the water hyacinth, Eichhornia security networks but can also act as causative
crassipes, which spreads over lake surfaces, choking agents of harmful algal blooms (Hallegraeff 1998;
local vegetation and reducing oxygen availability; Coetzee and Hill 2012), threaten the availability
it is a major hindrance in Africa in particular, of clean water supplies, and pose other significant
though it does appear to have some natural limits health threats (McNeely 2001). Invasive bivalves
to its cyclical spread (Albright et al. 2004).²¹ can clog machinery vital for the operation of
energy plants and well as fishing boat equipment.
Climate change will further exacerbate the problem Water hyacinth (Eichhornia crossipes) can make
of aquatic invasive species as temperatures small-scale freshwater fishing next to impossible,
increase and the range of invasive species, such directly lowering food security and nutrition levels
as zebra mussels and Asian carp, are extended. for local communities. Moreover, its introduction
Another example is the European green crab, in Lake Victoria has also been found to contribute
harmful to native species in the US and parts of to the spread of waterborne diseases (Pejchar and
Africa and Australia; it has been slow to spread Mooney 2009 and reference therein). Efforts to
northward because of colder water temperatures, eradicate aquatic IAS can also carry health hazards
but this is slowly changing with global warming if they employ lampricides and other agents that
(Floyd and Williams 2004). In some cases, climate can contaminate water supplies (though sea
change will join invasive species as major stressors lamprey eradication efforts in North America

²⁰ See http://www.ec.gc.ca/inre-nwri/default.asp?lang=En&n=832CDC7B&xsl=articlesservices,viewfull&po=0E367B85. The

relationship with climate change is also complex: warmer temperatures will extend the range northward; and zebra mussels
release carbon dioxide into the aquatic environment.
²¹ For a recent discussion on the impact of water hyacinth in South Africa, see for example Coetzee et al. (2014), and for a
discussion on the role of eutrophication in its biological control, see Coetzee and Hill (2012).
²² As a major EPA report suggested in 2008, in order “to effectively prevent invasions that might result from or be influenced
by climate-change factors, a first step should be to identify specific aquatic invasive species threats, including new pathways
and vectors, which may result as environmental conditions such as water and air temperatures, precipitation patterns, or
sea levels change” (EPA 2008:61).

60 Connecting Global Priorities: Biodiversity and Human Health

have been relatively successful with limited on Water concluded that climate change would
controversy). Moreover, the losses posed by IAS have multiple impacts, including:
can be harmful to the well-being of communities
whose sense of place may be disrupted in areas • physical changes such as increased water
affected by IAS (McNeely 2001). It is vital that temperature, reduced river and lake ice cover,
efforts are made to avoid introductions whenever more stable vertical stratification and less mixing
possible, and to employ the precautionary of water of deep-water lakes, and changes in water
principle when contemplating future purposeful discharge, affecting water level and retention time;
introductions.
• chemical changes, such as increased nutrient
concentrations and water colour, and decreased
6. Ways forward and additional oxygen content (DOC);
considerations
It is clear that healthy freshwater systems
• biological changes, including northwards
migration of species and alteration of habitats,
are central to the protection of biodiversity
affecting the structure and functioning of
as well as to the promotion of human health
freshwater ecosystems (European Topic Centre
and well-being. It is also evident that there are
on Water 2010: 5)
severe threats to water security and ecosystem
health; and that waterborne diseases, the loss It is clear that all of these changes will affect human
of aquatic biodiversity, and the disruption of security in terms of our physical and emotional
complex ecosystems represent major public connections with water, and the ecosystem
health challenges. A concerted effort to conserve services provided by aquatic ecosystems. We will
freshwater resources is necessary on a global need to adapt to them, but we can also be more
scale. While this chapter has focused primarily proactive by promoting biodiversity conservation
on freshwater systems, it is equally apparent and restoration.
that oceans and related biodiversity face threats
from pollution, climate change, coral bleaching, Water resources will remain central to human
acidification and other anthropocentric factors, and community development. The biodiversity–
and that an international effort to conserve them health nexus is readily apparent in this context.
is vital (Stoett 2012:107–28). These impacts However, much remains to be done regarding the
extend to human health, an area that clearly management and equitable use of water resources,
merits greater scientific attention. The European including preventive measures to avoid increased
Marine Board recently published a position paper waterborne disease and aquatic invasive species.
to this effect on “Linking oceans and human The WHO Guidelines for drinking-water quality
health: a strategic research priority for Europe”,²³ establish a basis for the pursuit of a healthier
which highlights the substantive and complex human species (WHO 2010b). Recognition of
interactions between the marine environment the key role played by biodiversity in freshwater
and human health and well-being (Flemming et systems is an important element in that pursuit
al. 2014). as well. Recent laboratory research suggests that
there is a positive correlation between species
Moreover, we are only beginning to understand diversity and the ability of water systems to filter
the impact climate change will have on aquatic nutrient pollutants such as nitrate (Cardinale
ecosystems and human health (see the chapter 2011) as well as pharmaceuticals (Binellia et
on climate change in this volume). In a recent al. 2014). More than ever, the biodiversity and
background report written for the European global public health communities, including key
Environmental Agency, the European Topic Centre decision-makers and private sector actors, need
to work together towards a healthier blue planet.

²³ http://www.marineboard.eu/images/publications/Oceans%20and%20Human%20Health-214.pdf

Connecting Global Priorities: Biodiversity and Human Health 61

 Some meaningful (but by no means exhaustive) greenhouse gas emissions should receive
considerations include the following: extra attention, given the centrality of water
biodiversity to human health. This calls for more
We must take stock of our ecological capital in scientific research, including taxonomic studies
ways that will benefit human health. Water and focusing on the use of bioindicators to assess
other ecosystem services must be linked to broader ecosystem condition (Buss et al. 2015), and more
frameworks that consider public health concerns studies linking the impacts of biodiversity loss on
within broader ecosystem restoration and human health, as well as serious regulatory policy
conservation frameworks, such as the ecosystem development.
or One Health approach. Knowledge exchange and
cross-sectoral collaboration will be critical to share The impact of water quality and quantity on
and mutually learn from experiences. human health is one of several critical areas
described in this volume, which underscores the
The Ramsar Convention on Wetlands is a critical need to develop robust, cross-sectoral integrated
instrument in the pursuit of water security. As of approaches, such as the ecosystem or One Health
early 2015, 2186 sites, encompassing 208 449 277 approach to water management and to the
hectares of surface area, have been classified as broader management of ecosystems (including
wetlands of international importance. The Ramsar agroecosystems). Researchers, policy-makers and
Convention, in force since 1975, advocates the those that manage natural resources must also
“wise use” of wetlands, defined as “the maintenance work to compile and share regionally specific data
of their ecological character, achieved through the on how functional metrics vary over space and
implementation of ecosystem approaches, within time (Palmer and Febria 2012) and produce a more
the context of sustainable development”.²⁴ composite idea of related water footprints (see
Box 2 on cotton production). Applying a holistic
The pollution of freshwater lakes and the oceans framework to water and food security, and other
must be halted to protect their indigenous critical themes at the biodiversity–health nexus,
biodiversity. Micro-plastics are a particularly makes it possible to manage ecosystems (including
pernicious pollutant, harming wildlife as they water and agroecosystems) that are more resilient,
enter the food chain and providing vectors for sustainable and productive, that remain productive
invasive species. International efforts to stop the in the long term, and that yield a wide range of
pollution and clean oceans, lakes and rivers will ecosystem services. A socioecological perspective
be pivotal in the near future if we are to avoid will further ensure that vulnerable populations
the further development of what scientists have most affected by the global disease burden and
referred to as the “plastisphere” (Zettler et al. ecosystem degradation are also considered. These
2013). considerations will be imperative as we move from
the MDGs toward the Sustainable Development
The impact of climate change on water biodiversity
Goals and the post-2015 Development Agenda.
must be closely monitored and efforts to reduce

²⁴ http://www.ramsar.org/cda/en/ramsar-home/main/ramsar/1_4000_0

62 Connecting Global Priorities: Biodiversity and Human Health

 4. Biodiversity, air quality and
UNDP BANGLADESH / FLICKR

human health
1. Introduction million in 2012 (WHO 2014¹). This was equivalent
to 1 in every 8 deaths globally, making air pollution
Air pollution is a significant problem in cities the most important environmental health risk
across the world. It affects human health and worldwide (WHO 2014a). Other diseases affected
well-being, ecosystem health, crops, climate, by air pollution include cardiovascular disease,
visibility and human-made materials. Health immune disorders, various cancers, and disorders
effects related to air pollution include its of the eye, ear, nose and throat such as cataract and
impact on the pulmonary, cardiac, vascular and sinusitis. Epidemiological evidence suggests that
neurological systems (Section 2). Trees affect air prenatal exposure to certain forms of air pollution
quality through a number of means (Section 3) can harm the child, affecting birth outcomes and
and can be used to improve air quality (Section infant mortality. Childhood exposure to some
4). However, air pollution also affects tree health pollutants also appears to increase the risk of
and plant diversity (Section 5). Bioindicators can developing health problems in later life, affecting
be useful for monitoring air quality and indicating the development of lung function and increasing
environmental health (Section 6). Understanding the risk for development of chronic obstructive
the impacts of vegetation biodiversity on air pulmonary disease (COPD) and asthma.
quality and air quality on vegetation biodiversity
is essential to sustaining healthy and diverse Several respiratory illnesses caused or otherwise
ecosystems, and for improving air quality and affected by air pollution are on the rise. These
consequently human health and well-being. include bronchial asthma, which affects between
100 and 150 million people worldwide, with
$LUSROOXWLRQDQGLWVHƨHFWVRQ another 65 million affected by some form of
COPD. Other human health problems from air
human health
pollution include: aggravation of respiratory and
Air pollution can significantly affect human and cardiovascular disease, decreased lung function,
ecosystem health (US EPA 2010). Recent research increased frequency and severity of respiratory
indicates that global deaths directly or indirectly symptoms (e.g. difficulty in breathing and
attributable to outdoor air pollution reached 7 coughing, increased susceptibility to respiratory

¹ World Health Organization, 2015. Health and the Environment: Addressing the health impact of air pollution. Sixty-eighth
World Health Assembly, Agenda item 14.6. A68/A/CONF./2 Rev.1 26 May 2015. http://apps.who.int/gb/ebwha/pdf_files/
WHA68/A68_ACONF2Rev1-en.pdf (last accessed June 2015)

Connecting Global Priorities: Biodiversity and Human Health 63

 infections), effects on the nervous system (e.g. pollution also affects the earth’s climate by either
impacts on learning, memory and behaviour), absorbing or reflecting energy, which can lead to
cancer and premature death (e.g. Pope et al. climate warming or cooling, respectively.
2002). People with pre-existing conditions (e.g.
heart disease, asthma, emphysema), diabetes, and Indoor air pollution is primarily associated with
older adults and children are at greater risk for particulates from combustion of solid fuel (wood,
air pollution-related health effects. In the United coal, turf, dung, crop waste, etc.) and oil for heating
States (US), approximately 130 000 particulate and cooking, and gases from all fuels (including
matter (PM)2.5-related deaths and 4700 ozone natural gas) in buildings with inadequate
(O3)-related deaths in 2005 were attributed to air ventilation or smoke removal. The World Health
pollution (Fann et al. 2012). Organization (WHO) reports that over 4 million
people die prematurely from illness attributable to
Air pollution comes from numerous sources. household air pollution from cooking with solid
Major causes of gaseous and particulate outdoor fuels. More than 50% of premature deaths among
air pollution with a direct impact on public health children under 5 years of age are due to pneumonia
include the combustion of fossil fuels associated caused by particulate matter (soot) inhaled from
with transport, heating and electricity generation, household air pollution. It is estimated that
and industrial processes such as smelting, 3.8 million premature deaths annually from
concrete manufacture and oil refining. Other noncommunicable diseases (including stroke,
important sources include ecosystem degradation ischaemic heart disease, lung cancer and COPD)
(including deforestation and wetland drainage) are attributable to exposure to household air
and desertification. pollution (WHO 2014b).

Plants provide an important ecosystem service Some pollutants, both gaseous and particulate, are
through the regulation of air quality. Although directly emitted into the atmosphere and include
the effects of plants on air quality are generally sulfur dioxide (SO2), nitrogen oxides (NOx),
positive, they can also to some degree be negative carbon monoxide (CO), particulate matter (PM)
(as discussed in section 3 below). Likewise, air and volatile organic compounds (VOC). Other
quality can have both positive and negative pollutants are not directly emitted; rather, they are
impacts on plant populations. These various formed through chemical reactions. For example,
impacts are partially dependent upon the diversity ground-level O3 is often formed when emissions
of the plant species, vegetation assemblages and of NOx and VOCs react in the presence of sunlight.
size classes. This chapter explores the role of Some particles are also formed from other directly
biodiversity in regulating air quality in positive emitted pollutants.
and negative terms, including a discussion of
current knowledge gaps and recommendations.
3. Impacts of vegetation on air
Air pollution also affects the environment. Ozone quality
and other pollutants can damage plants and trees, There are three main ways in which plants affect
and pollution can lead to acid rain. Acid rain can local air pollution levels: via effects on local
harm vegetation by damaging tree leaves and microclimate and energy use, removal of air
stressing trees through changing the chemical pollution, and emission of chemicals. Each of
and physical composition of the soil. Particles these are described below.
in the atmosphere can also reduce visibility. The
typical visual range in the eastern US parks is
(ƨHFWVRISODQWVRQORFDO
15–25 miles, approximately one third of what it
would be without human-induced air pollution.
microclimate and energy use
In western USA, the visual range has decreased Increased air temperature can lead to increased
from 140 miles to 35–90 miles (US EPA 2014). Air energy demand (and related emissions) in the

64 Connecting Global Priorities: Biodiversity and Human Health

summer (e.g. to cool buildings), increased air winter-time heating energy demand by tending
pollution and heat-related illness. Vegetation, to reduce cold air infiltration into buildings. On
particularly trees, alters microclimates and the negative side, reductions in wind speed can
cools the air through evaporation from tree reduce the dispersion of pollutants, which will
transpiration, blocking winds and shading various tend to increase local pollutant concentrations. In
surfaces. Local environmental influences on air addition, with lower wind speeds, the height of the
temperature include the amount of tree cover, atmosphere within which the pollution mixes can
amount of impervious surfaces in the area, time be reduced. This reduction in the “mixing height”
of day, thermal stability, antecedent moisture tends to increase pollutant concentrations, as the
condition and topography (Heisler et al. 2007). same amount of pollution is now mixed within a
Vegetated areas can cool the surroundings by smaller volume of air.
several degrees Celsius, with higher tree and shrub
cover resulting in cooler air temperatures (Chang 2) Removal of air pollutants
et al. 2007). Trees can also have a significant
impact on wind speed, with measured reductions Trees remove gaseous air pollution primarily by
in wind speed in high-canopy residential areas uptake through the leaves, though some gases
(77% tree cover) of the order of 65–75% (Heisler are removed by the plant surface. For O3, SO2
1990). and NO2, most of the pollution is removed via
leaf stomata.³ Healthy trees in cities can remove
2Temperature reduction and changes in wind significant amounts of air pollution. The amount
speed in urban areas can have significant effects of pollution removed is directly related to the
on air pollution. Lower air temperatures can lead amount of air pollution in the atmosphere (if
to lower emission of pollutants, as pollutant there is no air pollution, the trees will remove no
emissions are often related to air temperatures air pollution). Areas with a high proportion of
(e.g. evaporation of VOCs). In addition, reduced vegetation cover will remove more pollution and
urban air temperatures and shading of buildings have the potential to effect greater reductions in
can reduce the amount of energy used to cool air pollution concentrations in and around these
buildings in the summer time, as buildings are areas. However, pollution concentration can be
cooler and air conditioning is used less. However, increased under certain conditions (see Section 4).
shading of buildings in winter can lead to increased Pollution removal rates by vegetation differ among
building energy use (e.g. Heisler 1986).² In addition regions according to the amount of vegetative
to temperature effects, trees affect wind speed and cover and leaf area, the amount of air pollution,
mixing of pollutants in the atmosphere, which in length of in-leaf season, precipitation and other
turn affect local pollutant concentrations. These meteorological variables.
changes in wind speed can lead to both positive
and negative effects related to air pollution. On There are numerous studies that link air quality
the positive side, reduced wind speed due to to the effects on human health. With relation
shelter from trees and forests will tend to reduce to trees, most studies have investigated the

² This altered energy use consequently leads to altered pollutant emissions from power plants used to produce the energy
used to cool or heat buildings. Air temperatures reduced by trees can not only lead to reduced emission of air pollutants
from numerous sources (e.g. cars, power plants), but can also lead to reduced formation of O3 ,as O3 formation tends to
increase with increasing air temperatures.
³ Trees also directly affect particulate matter in the atmosphere by intercepting particles, emitting particles (e.g. pollen) and
resuspending particles captured on the plant surface. Some particles can be absorbed into the tree, though most intercepted
particles are retained on the plant surface. Many of the particles that are intercepted are eventually resuspended back to the
atmosphere, washed off by rain, or dropped to the ground with leaf and twig fall. During dry periods, particles are constantly
intercepted and resuspended, in part, dependent upon wind speed. During precipitation, particles can be washed off and
either dissolved or transferred to the soil. Consequently, vegetation is only a temporary retention site for many atmospheric
particles, though the removal of gaseous pollutants is more permanent as the gases are often absorbed and transformed
within the leaf interior.

Connecting Global Priorities: Biodiversity and Human Health 65

 magnitude of the effect of trees on pollution averages around 0.51% for particulate matter,
removal or concentrations, while only a limited 0.45% for O3, 0.44% for SO2, 0.33% for NO2, and
number of studies have looked at the estimated 0.002% for CO. However, in areas with 100%
health effects of pollution removal by trees. In tree cover (i.e. contiguous forest stands), air
the United Kingdom, woodlands are estimated pollution improvement is on an average around
to save between 5 and 7 deaths, and between 4 four times higher than city averages, with short-
and 6 hospital admissions per year due to reduced term improvements in air quality (1 hour) as
pollution by SO2 and particulate matter less high as 16% for O3 and SO2, 13% for particulate
than 10 microns (PM10) (Powe and Willis 2004). matter, 8% for NO2, and 0.05% for CO (Nowak et
Modelling for London estimates that 25% tree al. 2006).
cover removes 90.4 metric tons of PM10 pollution
per year, which equates to a reduction of 2 deaths 3) Emission of chemicals
and 2 hospital stays per year (Tiwary et al. 2009).
Nowak et al. (2013) reported that the total amount Vegetation, including trees, can emit various
of particulate matter less than 2.5 microns (PM2.5) chemicals that can contribute to air pollution.
removed annually by trees in 10 US cities in 2010 Because some vegetation, particularly urban
varied from 4.7 t in Syracuse to 64.5 t in Atlanta. vegetation, often requires relatively large inputs
Estimates of the annual monetary value of human of energy for maintenance activities, the resulting
health effects associated with PM2.5 removal emissions need to be considered. The use and
in these same cities (e.g. changes in mortality, combustion of fossil fuels to power this equipment
hospital admissions, respiratory symptoms) leads to the emission of chemicals such as VOCs,
ranged from $1.1 million in Syracuse to $60.1 CO, NO2 and SO2, and particulate matter (US EPA
million in New York City. Mortality avoided was 1991).
typically around 1 person per year per city, but was
Plants also emit VOCs (e.g. isoprene,
as high as 7.6 people per year in New York City.
monoterpenes) (Geron et al. 1994; Guenther 2002;
Trees and forests in the conterminous US Nowak et al. 2002; Lerdau and Slobodkin 2002).
removed 22.4 million t of air pollution in 2010 These compounds are natural chemicals that make
(range: 11.1–31.0 million t), with human health up essential oils, resins and other plant products,
effects valued at US$ 8.5 billion (range: $2.2– and may be useful in attracting pollinators or
15.6 billion). Most of the pollution removal repelling predators. Complete oxidation of VOCs
occurred in rural areas, while most of the health ultimately produces carbon dioxide (CO2), but
impacts and values were within urban areas. CO is an intermediate compound in this process.
Health impacts included the avoidance of more Oxidation of VOCs is an important component
than 850 incidences of human mortality. Other of the global CO budget (Tingey et al. 1991); CO
substantial health benefits included the reduction also can be released from chlorophyll degradation
of more than 670 000 incidences of acute (Smith 1990). VOCs emitted by trees can also
respiratory symptoms (range: 221 000–1 035 contribute to the formation of O3. Because VOC
000), 430 000 incidences of asthma exacerbation emissions are temperature dependent and trees
(range: 198 000–688 000) and 200 000 days of generally lower air temperatures, increased tree
school loss (range: 78 000–266 000) (Nowak et cover can lower overall VOC emissions and,
al. 2014). consequently, O3 levels in urban areas (e.g.
Cardelino and Chameides 1990). Ozone inside
Though the amount of air pollution removed by leaves can also be reduced due to the reactivity
trees may be substantial, the per cent air quality with biogenic compounds (Calfapietra et al. 2009).
improvement in an area will depend upon on
the amount of vegetation and meteorological Trees generally are not considered as a source
conditions. Air quality improvement by trees of atmospheric NOx, though plants, particularly
in cities during daytime of the in-leaf season agricultural crops, are known to emit ammonia.

66 Connecting Global Priorities: Biodiversity and Human Health

Emissions occur primarily under conditions of automobiles), and altered O3 chemistry such that
excess nitrogen (e.g. after fertilization) and during concentrations of O3 increased. Another model
the reproductive growth phase (Schjoerring 1991). simulation of California’s South Coast Air Basin
They can also make minor contributions to SO2 suggests that the air quality impacts of increased
concentration by emitting sulfur compounds such urban tree cover may be locally positive or negative
as hydrogen sulfide (H2S) and SO2 (Garsed 1985; with respect to O3. However, the net basinwide
Rennenberg 1991). H2S, the predominant sulfur effect of increased urban vegetation is a decrease
compound emitted, is oxidized in the atmosphere in O3 concentrations if the additional trees are low
to SO2. Higher rates of sulfur emission from plants VOC emitters (Taha 1996).
are observed in the presence of excess atmospheric
or soil sulfur. However, sulfur compounds also Modelling the effects of increased urban tree cover
can be emitted with a moderate sulfur supply on O3 concentrations from Washington, DC to
(Rennenberg 1991). In urban areas, trees can central Massachusetts revealed that urban trees
additionally contribute to particle concentrations generally reduce O3 concentrations in cities, but
by releasing pollen and emitting volatile organic tend to slightly increase average O3 concentrations
and sulfur compounds that serve as precursors regionally (Nowak et al. 2000). Modelling of the
to particle formation. From a health perspective, New York City metropolitan area also revealed
pollen particles can lead to allergic reactions (e.g. that increasing tree cover by 10% within urban
Cariñanosa et al. 2014). areas reduced maximum O3 levels by about 4 ppb,
which was about 37% of the amount needed for
attainment (Luley and Bond 2002).
2YHUDOOHƨHFWRIYHJHWDWLRQRQDLU
pollution
There are many factors that determine the
4. The role of plant biodiversity in
ultimate effect of vegetation on pollution. Many regulating air quality
plant effects are positive in terms of reducing The impacts of vegetation on air quality depend
pollution concentrations. For example, trees can in part on species and other aspects of plant
reduce temperatures and thereby reduce emissions biodiversity. Plant biodiversity in an area is
from various sources, and they can directly remove influenced by a mix of natural and anthropogenic
pollution from the air. However, the alteration of factors that interact to produce the vegetation
wind patterns and speeds can affect pollution structure. Natural influences include native
concentrations in both positive and negative vegetation types and abundance, natural biotic
ways. In addition, plant compound emissions interactions (e.g. seed dispersers, pollinators, plant
and emissions from vegetation maintenance can consumers), climate factors (e.g. temperature,
contribute to air pollution. Various studies on O3, precipitation), topographic moisture regimes, and
a chemical that is not directly emitted but rather soil types. Superimposed on these natural systems
formed through chemical reactions, have helped in varying degrees is an anthropogenic system
to illustrate the cumulative and interactive effects that includes people, buildings, roads, energy use
of trees. and management decisions. The management
decisions made by multiple disciplines within an
One model simulation illustrated that a 20% loss in urban system can both directly (e.g. tree planting,
forest cover in the Atlanta area due to urbanization removal, species introduction, mowing, paving,
led to a 14% increase in O3 concentrations for a watering, use of herbicides and fertilizers) and
day (Cardelino and Chameides 1990). Although indirectly (e.g. policies and funding related to
there were fewer trees to emit VOCs, an increase vegetation and development) affect vegetation
in Atlanta’s air temperatures due to the increased structure and biodiversity. In addition, the
urban heat island, which occurred concomitantly anthropogenic system alters the environment (e.g.
with tree loss, increased VOC emissions from changes in air temperature and solar radiation,
the remaining trees and other sources (e.g.

Connecting Global Priorities: Biodiversity and Human Health 67

 air pollution, soil compaction) and can induce In urban areas, land use, population density,
changes in vegetation structure (Nowak 2010). management intensity, human preferences and
socioeconomic factors can affect the amount of
Much is generally known about plant distribution tree cover and plant diversity (Nowak et al. 1996;
globally, but less is known about factors that affect Hope et al. 2003; Kunzig et al. 2005). These factors
the distribution of plant diversity and human are often interrelated and create a mosaic of tree
influences on plant biodiversity (Kreft and Jetz cover and species across the city landscape. Land
2007). Variations in urban tree cover across use is a dominant factor affecting tree cover
regions and within cities give an indication of the (Table 1). However, land use can also affect species
types of factors that can affect urban tree structure composition, as non-managed lands (e.g. vacant)
and consequently biodiversity, with resulting tend to be dominated by natural regeneration of
impacts on human health. One of the dominant native and exotic species. Within areas of managed
factors affecting tree cover in cities is the natural land use, the species composition tends to be
characteristics of the surrounding region. For dictated by a combination of human preferences
example, in forested areas of the US, urban tree for certain species (tree planting) and how much
cover averages 34%. Cities within grassland areas land is allowed to naturally regenerate (Nowak
average 18% tree cover, while cities in desert 2010).
regions average only 9% tree cover (Nowak et al.
2001). Cities in areas conducive to tree growth Tree diversity, represented by the common
naturally tend to have more tree cover, as non- biodiversity metrics of species richness (number of
managed spaces tend to naturally regenerate species) and the Shannon–Wiener diversity index
with trees. In forested areas, tree cover is often (Barbour et al. 1980), varies among and within
specifically excluded by design or management cities and through time. Based on field sampling
activities (e.g. impervious surfaces, mowing). In of various cities in North America (Nowak et al.
the US, while the per cent tree cover nationally 2008; Nowak 2010), species richness varied from
in urban (35.0%) and rural areas (34.1%) are 37 species in Calgary, Alberta, Canada, to 109
comparable, urbanization tends to decrease overall species in Oakville, Ontario, Canada (Figure 1).
tree cover in naturally forested areas, but increase Species diversity varied from 1.6 in Calgary to
tree cover in grassland and desert regions (Nowak 3.8 in Washington, DC (Figure 2). The species
and Greenfield 2012). richness in all cities is greater than the average
species richness in eastern US forests by county
(26.3) (Iverson and Prasad 2001). Species diversity

7DEOH0HDQSHUFHQWWUHHFRYHUDQGVWDQGDUGHUURU6(IRU86FLWLHVZLWKGLƨHUHQW
potential natural vegetation types (forest, grassland, desert) by land use (from Nowak
et al. 1996)

Forest Grassland Desert

Land use Mean SE Mean SE Mean SE
Park 47.6 5.9 27.4 2.1 11.3 3.5
Vacant/wildland 44.5 7.4 11.0 2.5 0.8 1.9
Residential 31.4 2.4 18.7 1.5 17.2 3.5
Institutional 19.9 1.9 9.1 1.2 6.7 2.0
Other 7.7 1.2 7.1 1.9 3.0 1.3
Commercial/industrial 7.2 1.0 4.8 0.6 7.6 1.8

Includes agriculture, orchards, transportation (e.g., freeways, airports, shipyards), and miscellaneous.

68 Connecting Global Priorities: Biodiversity and Human Health

in these urban areas is also typically greater than People often plant trees in urban areas to
found in eastern US forests (Barbour et al. 1980). improve aesthetics and/or the physical or social
Tree species diversity and richness is enhanced environment. Some non-native species can be
in urban areas compared with surrounding introduced via transportation corridors or escape
landscapes and/or typical forest stands, as native from cultivation (e.g. Muehlenbach 1969; Haigh
species richness is supplemented with species 1980).
introduced by urban inhabitants or processes.

ǡǤǢǰǭǠɻ Species richness and values for tree populations in various cities. Numbers in parentheses are
sample size based on 0.04 hectare plots. (A) Dark line indicates average species richness in eastern US
forests by county (26.3).

Atlanta, Georgia (205)

Baltimore, Maryland (200)

Boston, Massachusetts (217)

Calgary, Alberta (350)

Freehold, New Jersey (144)

Jersey City, New Jersey (220)

Minneapolis, Minnesota (110)

Moorestown, New Jersey (206)

Morgantown, West Virginia (136)

New York City, New York (206)

Oakville, Ontario (372)

Philadelphia, Pennsylvania (210)

San Francisco, California (194)

Syracuse, New York (198)

Tampa, Florida (201)

Washington DC (201)

Wilmington, Delaware (208)

Woodbridge, New Jersey (215)

0 20 40 60 80 100 120
Number of Tree Species

Source: Nowak 2010

ɯǝɰ Shannon–Wiener Diversity Index values. Shaded area indicates typical range of diversity values for
forests in the eastern US (1.7–3.1).

Atlanta, Georgia (205)

Baltimore, Maryland (200)

Boston, Massachusetts (217)

Calgary, Alberta (350)

Freehold, New Jersey (144)

Jersey City, New Jersey (220)

Minneapolis, Minnesota (110)

Moorestown, New Jersey (206)

Morgantown, West Virginia (136)

New York City, New York (206)

Oakville, Ontario (372)

Philadelphia, Pennsylvania (210)

San Francisco, California (194)

Syracuse, New York (198)

Tampa, Florida (201)

Washington DC (201)

Wilmington, Delaware (208)

Woodbridge, New Jersey (215)

0 0.5 1 1.5 2 2.5 3 3.5 4

Index Value

Source: Nowak 2010

Connecting Global Priorities: Biodiversity and Human Health 69

 forest stands compared to the outside of the forest
One of the most important vegetation attributes stands (e.g. Dasch 1987; Cavanagh et al. 2009).
in relation to air quality is the amount of leaf
area. Leaf area varies by plant form, with leaf area The biodiversity of plant types within an area
indices (m² leaf surface area per m² ground) of affects the total amount of leaf area and the
agricultural areas typically around 3–5 and leaf vegetation design. Following biodiversity related
area indices of forests typically between 5 and to plant form, species diversity also affects air
11 (Barbour et al. 1980). Thus, the magnitude quality, as different species have different effects
and distribution of vegetation types (e.g. grasses, based on species characteristics. In general, species
shrubs, trees) affect air quality. In general, plant with larger growth forms and size at maturity
types with more leaf area or leaf biomass have a have greater impacts, either positive or negative,
greater impact, either positive or negative, on air on air quality. The following are the types of air
quality.⁴ quality impacts that can be affected by species and
therefore species diversity:
The second most important attribute related to
air quality is vegetation configuration or design. Pollution removal: in addition to total leaf area
Though reduction in wind speeds can increase of a species, species characteristics that affect
local pollution concentrations due to reduced pollution removal are tree transpiration and leaf
dispersion of pollutants and mixing height of the characteristics. Removal of gaseous pollutants
atmosphere, altering of wind patterns can also is affected by tree transpiration rates (gas
have a potential positive effect. Tree canopies exchange rates). As actual transpiration rates are
can potentially prevent pollution in the upper highly variable, depending upon site or species
atmosphere from reaching ground-level air space. characteristics, limited data exist on transpiration
Measured differences in O3 concentration between rates for various species under comparable
above- and below-forest canopies in California’s conditions. However, relative transpiration factors
San Bernardino mountains have exceeded 50 ppb for various species can be gauged from estimated
(40% improvement) (Byternowicz et al. 1999). monthly water use (Costello and Jones 1994).
Under normal daytime conditions, atmospheric Particulate matter removal rates vary depending
turbulence mixes the atmosphere such that upon leaf surface characteristics. Species with
pollutant concentrations are relatively consistent dense and fine textured crowns and complex,
with height. Forest canopies can limit the mixing small and rough leaves would capture and retain
of upper air with ground-level air, leading to more particles than open and coarse crowns, and
below-canopy air quality improvements. However, simple, large, smooth leaves (Little 1997; Smith
where there are numerous pollutant sources below 1990). Species ranking of trees in relation to
the canopy (e.g. automobiles), the forest canopy pollution removal are estimated in i-Tree Species
could increase concentrations by minimizing the (www.itreetools.org). In addition, evergreen trees
dispersion of the pollutants away at ground level. provide for year-round removal of particles.
This effect could be particularly important in
heavily treed areas near roadways (Gromke and VOC emissions: emission rates of VOCs vary
Ruck 2009; Wania et al. 2012; Salmond et al. 2013; by species (e.g. Geron et al. 1994; Nowak et al.
Vos et al. 2013). However, standing in the interior 2002). Nine tree genera that have the highest
of a forest stand can offer cleaner air if there are standardized isoprene emission rate, and therefore
no local ground sources of emissions (e.g. from the greatest relative effect on increasing O3,
automobiles). Various studies have illustrated are beefwood (Casuarina spp.), Eucalyptus spp.,
reduced pollutant concentrations in the interior of sweetgum (Liquidambar spp.), black gum (Nyssa
spp.), sycamore (Platanus spp.), poplar (Populus

⁴ Within forests, leaf area also varies with tree age/size, with large healthy trees greater than 30 inches in stem diameter in
Chicago having approximately 60–70 times more leaf area than small healthy trees less than 3 inches in diameter (Nowak
1994).

70 Connecting Global Priorities: Biodiversity and Human Health

spp.), oak (Quercus spp.), black locust (Robinia life span (e.g. shorter lived species require more
spp.) and willow (Salix spp.). However, due to frequent planting and removal).
the high degree of uncertainty in atmospheric
modelling, results are currently inconclusive as to Pollution sensitivity: sensitivity to various
whether these genera contribute to an overall net pollutants vary by plant species. For example,
formation of O3 in cities (i.e. O3 formation from Populus tremuloides and Poa annua are sensitive to
VOC emissions is greater than O3 removal). O3, but Tilia americana and Dactylis glomerata are
resistant. Pollutant sensitivity to various species
Pollen: not only do pollen emissions and is given in Smith and Levenson (1980).
phenology of emissions vary by species, but pollen
allergenicity also varies by species. Examples of
5. Impacts of air quality on plant
some of the most allergenic species are Acer
negundo (male), Ambrosia spp., Cupressus spp., communities
Daucus spp., Holcus spp., Juniperus spp. (male), Air pollution can affect tree health. Some
Lolium spp., Mangifera indica, Planera aquatica, pollutants under high concentrations can damage
Ricinus communis, Salix alba (male), Schinus spp. leaves (e.g. SO2, NO2, O3), particularly of pollutant-
(male) and Zelkova spp. (Ogren 2000). sensitive species. For NO2, visible leaf injury would
be expected at concentrations around 1.6–2.6 ppm
Air temperature reduction: similar to for 48 hours, 0 ppm for 1 hour, or a concentration
gaseous air pollution removal, species effects of 1 ppm for as many as 100 hours (Natl. Acad.
on air temperatures vary with leaf area and of Sci. 1977a). Concentrations that would induce
transpiration rates. Leaf area affects tree shading foliage symptoms would be expected only in the
of ground surfaces and also overall transpiration. vicinity of an excessive industrial source (Smith
Transpiration from the leaves helps to provide 1990).
evaporative cooling. Both the shade and
evaporative cooling, along with effects on wind Eastern deciduous species are injured by exposure
speed, affect local air temperature and therefore to O3 at 0.20–0.30 ppm for 2–4 hours (Natl. Acad.
pollutant emission and formation. of Sci. 1977b). The threshold for visible injury of
eastern white pine is approximately 0.15 ppm for
Building energy conservation: although 5 hours (Costonis 1976). Sorption of O3 by white
the effects of trees on building energy use is birch seedlings shows a linear increase up to 0.8
dependent upon a tree’s position (distance and ppm; for red maple seedlings the increase is up
direction) relative to the building, tree size also to 0.5 ppm (Townsend 1974). Severe O3 levels in
plays a role on building energy effects (McPherson urban areas can exceed 0.3 ppm (Off. Technol.
and Simpson 2000). Changes in building energy Assess. 1989). Injury effects can include altered
use affect pollutant emission from power plants. photosynthesis, respiration, growth and stomatal
function (Lefohn et al. 1988; Shafer and Heagle
Maintenance needs: like building energy
1989; Smith 1990).
conversation, species maintenance needs have
a secondary effect on air quality. Plant species Toxic effects of SO2 may be due to its acidifying
with greater maintenance needs typically require influence and/or the sulfite (SO3²-) and sulfate
more human interventions (planting, pruning, (SO4²-) ions that are toxic to a variety of biochemical
removal) that utilize fossil fuel-based equipment processes (Smith 1990). Stomata may exhibit
(e.g. cars, lawn mowers, chain saws). The more increases in either stomatal opening or stomatal
fossil fuel-based equipment is used, the more closure when exposed to SO2 (Smith 1984; Black
pollutant emissions are produced. Plant attributes 1985). Acute SO2 injury to native vegetation does
that affect maintenance needs include not only not occur below 0.70 ppm for 1 hour or 0.18 ppm
plant adaptation to site conditions but also plant for 8 hours (Linzon 1978). A concentration of 0.25
ppm for several hours may injure some species

Connecting Global Priorities: Biodiversity and Human Health 71

 (Smith 1990). Indirect anthropogenic effects can costs (often by orders of magnitude per study
alter species composition. For example, in a natural site). Biodiversity metrics, such as the number
park in Tokyo, Japanese red pine (Pinus densiflora) of sensitive species, relative abundance of
was dying and being successionally replaced functional groups, or genotypic frequencies,
with broad-leaved evergreen species (Numata for example, are successfully employed for air
1977). This shift in species composition has been quality biomonitoring in many nations (Markert
attributed to SO2 air pollution, with the broad- et al. 1996; Aničić et al. 2009; Cao et al. 2009).
leaved species being more resistant to air pollution. Measuring pollutant concentrations in lichen
and bryophyte tissues is another means of air
Particulate trace metals can be toxic to plant leaves. quality mapping (Augusto et al. 2007; Augusto
The accumulation of particles on leaves also can et al. 2010; Liu et al. 2011; Root et al. 2013).
reduce photosynthesis by reducing the amount of Most studies focus on environmental health
light reaching the leaf. Damage to plant leaves can (i.e. evaluating pollutant-mediated harms to the
also occur from acid rain (pH <3.0). Acid rain and natural environment) to guide land management
air pollution (NAPAP 1991) can be a source of the and air quality regulation (Hawksworth and Rose
essential plant nutrients of sulfur and nitrogen, 1970; Cape et al. 2009; Geiser et al. 2010). Health
but also can reduce soil nutrient availability and bioindicator experts often suggest utilizing
through leaching or toxic soil reactions. Particles bioindicators in public health assessments to
can also affect tree pest/disease populations. overcome the lack of systematic air quality
Given the pollution concentration in most cities, measurements from instrumented monitoring
these pollutants would not be expected to cause networks and for detecting chronic low levels of
visible leaf injury, but could in cities or areas with pollution below the detection limits of monitoring
high pollutant concentrations. instruments (Brauer 2010; Augusto et al. 2012).
Tissue-based bioindicators enable high spatial
6. Bioindicators resolution mapping of toxic pollutants that are not
frequently measured by instrumented networks.
A bioindicator is a quality of an organism, Nonetheless, it is rare for research to actually
population, community or ecosystem used for integrate bioindicator and public health data.
indicating the health or status of the surrounding
environment. Bioindicators, especially lichens Taking cues from the environment to assess air
and bryophytes, are widely used for monitoring quality is a relatively old science. Lichens were first
air quality. The benefits of direct measurements described as “health meters for the air” in 1866,
of air quality include long-term integration of when a Finnish botanist noted that certain species
pollution levels over time and lower operational were restricted to a large city park in Paris (Nylander
1866). While many organisms exhibit a measurable
response to pollution, lichen and bryophytes (i.e.
mosses and liverworts) are the most widely utilized
bioindicators in both environmental and human
health studies. Lichen and bryophytes lack root
structures and the capacity to store water, creating
a dependence on moisture and nutrients scavenged
from the atmosphere. By also lacking a protective
cuticle, they absorb water and contaminants much
like a sponge.

Biodiversity-based indices, including richness,

UNITED NATIONS PHOTO / FLICKR

relative abundance or dominance of sensitive lichen

and bryophyte species are commonly used for
mapping deposition of nitrogen (N)- and sulphur

72 Connecting Global Priorities: Biodiversity and Human Health

(S)-containing pollutants. Species’ sensitivities to are growing. This information is not likely to be
H2S, SO2, acidic deposition, HNO3, NH3, NOy, and obtained through other monitoring methods,
the N- and S-containing aerosols have been well which solely represent physicochemical measures
established through field studies and controlled of pollutants. None of these research barriers
fumigation experiments (Riddell et al. 2008; are insurmountable. The main issue appears to
Riddell et al. 2012). Biodiversity indices usually be bringing together the right mix of skills. The
correlate well with instrumented measurements proposed ways forward include the following:
of pollutant deposition (Gadsdon et al. 2010;
Jovan et al. 2012), although some indices are Cross-sectoral collaboration is needed to
intentionally non-specific, meaning they are not foster information exchange and collaboration
calibrated to track specific pollutants. In this between bioindicator specialists and public
case, biodiversity measures are interpreted as health scientists. There is little crossover in the
an integrated response to ‘air quality’ in general professional activities of these groups at present,
(Castro et al. 2014), which may provide a useful and interdisciplinary workshops and meetings
representation of human exposure as the human could further reduce this gap.
body integrates pollution from multiple sources.
Future research should highlight the need to
Nitrogen, S, as well as metals (Wolterbeek 2002), calibrate bioindicators with existing air monitoring
radionuclides (Seaward 2002) and persistent stations or passive samplers, which are more
organic pollutants (POPs) like polycyclic aromatic flexible. While expensive to collect, investment in
hydrocarbons (PAHs), dioxins and furans calibration data will facilitate the use of pollutant
(PCDD/Fs), polychlorobiphenyls (PCBs) and thresholds in bioindicator maps and also help
polybrominated diphenyl ethers (PBDEs) (Augusto define what time frame the bioindicator reflects,
et al. 2013; Harmens et al. 2013) accumulate over including how seasonal variations or sudden
time in lichen and bryophyte tissues, allowing pollution episodes contribute to bioindicator
their use as in-situ passive deposition monitors. values. Even if causality or mechanism cannot
Lichens and bryophytes tolerate exposure to be established, an affordable bioindicator with
many non-nutrient pollutants (e.g. heavy metals, the capacity to predict human health outcomes
radionuclides, POPs), and so typical biodiversity- remains valuable for further research.
based indices cannot be utilized for this group.
For large health research institutions, maintaining
staff dedicated to data dissemination is critical for
6.1 Air quality bioindicators: ways enabling access to detailed personal public health
forward data. These intermediaries often help, for instance,
There is clearly great potential for utilizing by spatially joining bioindicator and health data, to
bioindicators in human health research; yet few keep confidential addresses for private residences.
scientists have done so. The use of bioindicator
data in health studies has barely been explored, Research that utilizes and cross-links resources
despite potential to overcome some of the most that are already available, such as high-resolution
persistent data gaps in public health research on maps from air quality and public health monitoring
air quality. This potential can be explained by studies, should be encouraged. Also, lichens and
the fact that obtaining spatially and temporally bryophytes form the backbone of large-scale air
representative air quality measurements is one quality monitoring programmes in both Europe
of the most pervasive issues in health studies (the International Co-operative Programme on
(Brauer 2010; Ribeiro et al. 2010) yet, for the Assessment and Monitoring of Air Pollution Effects
most part, health research utilizes bioindicator on Forests operating under the UNECE Convention
maps tangentially or not at all. Bioindicators have on Long-range Transboundary Air Pollution) and
the advantage of being living organisms and thus the US (the US Department of Agriculture’s Forest
biologically reflecting the environment where they Inventory and Analysis Program).

Connecting Global Priorities: Biodiversity and Human Health 73

 7. Knowledge gaps and ways strategies to help improve air quality include the
forward following:

There are numerous gaps in knowledge related • Increase the amount of healthy vegetation
to biodiversity, including plant biodiversity (increases pollution removal).
(species-specific effects) and air quality. As there
are numerous species globally, these gaps are • Sustain the existing vegetation cover (maintains
felt across the world. However, leaf area is the pollution removal levels).
dominant characteristic that affects many aspects
of air quality. Thus, general magnitudes of impact • Maximize the use of low VOC-emitting species
can be assessed among plant communities based (reduces O3 and CO formation).
on leaf area. The individual species effects are
most important in determining variations within • Sustain large, healthy trees (large trees have
plant communities, understanding the impacts of greater per-tree effects).
biodiversity and guiding vegetation management.
There are gaps in all aspects of plant species effects
• Use long-living tree species (reduces long-term
pollutant emissions from planting and removal).
on air quality, but some of the better-researched
aspects are related to VOC emissions, which • Use low-maintenance species (reduces pollutant
are species or genera dependent. Estimates and emissions from maintenance activities).
comparisons of pollen allergenicity among plant
species also exist (e.g. Pettyjohn and Levetin • Reduce fossil fuel use in maintaining vegetation
1997; Ogren 2000; Cariñanosa et al. 2014). (reduces pollutant emissions).
One of the least understood aspects related to
individual species characteristics and air quality • Plant trees in energy-conserving locations
effects relates to species-specific removal rates (reduces pollutant emissions from power plants).
(deposition velocities) for various pollutants. In
addition, while there are various studies relating • Plant trees to shade parked cars (reduces
air pollution to human health, there are few vehicular VOC emissions).
studies relating vegetation impacts to pollution
concentrations and human health effects. • Supply ample water to vegetation (enhances
pollution removal and temperature reduction).
To facilitate air quality improvements through
biodiversity and management of vegetation, • Plant vegetation in polluted or heavily
there are various steps that managers and policy- populated areas (maximizes pollution removal and
makers could take. The first step could be to assess air quality benefits; however, specific vegetation
the local species composition and biodiversity as designs need to be considered so that they do not
a basic foundation for understanding the local increase local pollutant concentrations, such as
vegetation structure. The second could be to assess near roadways).
what impacts this current vegetation structure
has on air quality (e.g. estimating pollution • Avoid pollutant-sensitive species (improves
removal, VOC emissions, impacts on building plant health).
energy conservation and emissions, etc). To aid in
understanding the vegetation ecosystem services,
• Utilize evergreen species for particulate matter
(year-round removal of particles).
various models exist (e.g. i-Tree). Policy-makers
could also facilitate increased research to better Through proper design and management, plant
understand the effects and impact of individual systems and biodiversity can be utilized to
species on air quality. enhance air quality and provide numerous other
ecosystem services, and consequently improve the
Local vegetation management decisions can help
health and well-being of people and ecosystems
improve air quality. Vegetation management
across the globe.

74 Connecting Global Priorities: Biodiversity and Human Health

 5. Agricultural biodiversity, food
security and human health
CRAIG HANSEN

1. Introduction 2014). The improvements in food production (and

consequent benefits in overall human health in
The world’s population has increased from roughly many areas) have also generally been accompanied
2.5 billion people in 1950 to more than 7 billion by a loss of biodiversity in agro-ecosystems, and
today (USCB 2013) and is anticipated to exceed led to new public health challenges.
9 billion by 2050. This development, in parallel
with global affluence and associated dietary shifts An adequate supply of safe and nutritious food is
(Alexandratos and Bruinsma 2012; Tilman et al. one of the cornerstones of human health, and the
2011), has been accompanied by a parallel rise in ways in which biodiversity and food production
demand for food and other agricultural products are interrelated and influence each other are key
(Godfray et al. 2010). Food production is expected aspects of this relationship. Agriculture and food
to have to rise by a further 70–100% by 2050 production are also significantly implicated in
(Tilman et al. 2001; Foley et al. 2005; Green et the extent to which planetary boundaries have
al. 2005). Global food production systems have been or are likely to be exceeded with respect to
largely kept pace with population growth over nitrogen flows, water usage, and land use change
the past 50 years due to conversion of natural (Rockstrom et al. 2009; Steffen et al. 2015), and
ecosystems to agriculture, intensification of in the negative effects of loss of biodiversity on
farming practices on existing agricultural lands, human health described in other chapters of this
improved varieties of crops and breeds of animals, volume.
and improved agronomic practices (Wilby et
al. 2009). From 1980 to 2001, global cereal This chapter focuses on the links between
production increased by 36% with a simultaneous agricultural biodiversity, food security and human
increase of 34% in areas under permanent crop health. It covers both direct impacts, such as the
and in the use of nitrogen fertilizers (FAO loss of arable land and natural habitat, and health
2003). While increases in food production have outcomes associated with modern agricultural
contributed to feeding an additional 4 billion practices. The relationships between biodiversity
people, improved human nutrition and reduced and nutrition are dealt with in a related chapter
hunger prevalence from 33% to 18% over the in this volume.
past 40 years (Sanchez et al. 2005), the number of
chronically or acutely malnourished people remain
stubbornly high, still exceeding 800 million (FAO

Connecting Global Priorities: Biodiversity and Human Health 75

 2. Agricultural biodiversityƸ benefits agricultural biodiversity can provide (MA
2005; Frison et al. 2011; Lockie and Carpenter
2.1 The contribution of agricultural 2010). All too often, the food used for human
biodiversity to human health consumption and the nutritional and health
benefits biodiversity provides have been ignored
Agricultural biodiversity (often referred to as
(De Clerck et al. 2011). When these links are
agrobiodiversity) includes all the components
considered, biodiversity, agriculture and health
of biological diversity of relevance to food and
can form a common path leading to enhanced food
agriculture, and those that constitute the agro-
security and nutrition (Toledo and Burlingame
ecosystem: the variety and variability of animals,
2006).
plants and microorganisms at the genetic,
species and ecosystem levels, which sustain the It has been estimated that some 7000 plant
functions, structure and processes of the agro- species have been used by humans at one time or
ecosystem (FAO/PAR 2011). Created, managed another although some 82 crop species provide
or influenced by farmers, pastoralists, fishers and 90% of the energy currently consumed by humans
forest dwellers, agricultural biodiversity continues (Prescott-Allen and Prescott-Allen 1990). From
to provide many rural communities throughout this total, 40% is provided by only three crops.
the world with stability, adaptability and resilience Despite this homogenization of production
in their farming systems and constitutes a key systems, there remain several hundred neglected
element of their livelihood strategies (Altieri and and underutilized crops with significant potential
Merrick 1987; Brush 1999; Jarvis et al. 2011). to support diversification, improve adaptability
to change and increase resilience (Kahane et al.
Agricultural biodiversity plays a critical role in
2013). In contrast, about 40 livestock species in
global food production and the livelihoods and
total contribute to today’s agriculture and food
well-being of all, regardless of resource endowment
production and only five species provide 95% of
or geographical location. As such, it is an essential
the total (FAO, 2007; Heywood 2013).
component of any food system. Productive agro
ecosystems, both wild and managed, are the For aquaculture, it has been estimated that over
source of our food and a prerequisite for a healthy 230 spp. of finfish, molluscs and crustaceans are
life, and agricultural biodiversity contributes to all utilized but that 31 species are responsible for
four pillars of food security.² The sustainability of 95% of production (85% of which takes place in
agroecosystems is dependent on the conservation, Asia) (FAO 1996).³ As discussed in the chapter
enhancement and utilization of biodiversity. on nutrition in this volume, crop, animal and
Agricultural biodiversity provides the basic aquaculture species diversity also contribute
resources needed to adapt to variable conditions in to dietary diversity, the variety of macro- and
marginal environments and the resources required micronutrients needed by humans, and multiple
to increase productivity in more favourable livelihood benefits.
settings. Further, with global, especially climate,
change, there will be increasing interdependence Genetic diversity plays a particularly important
between farmers and communities all over the role in agriculture (FAO 2010). The development
world, who will be ever more reliant on the global of new varieties and breeds depends on the use of

¹ In this chapter, agriculture is taken to include crop and animal production, and freshwater aquaculture for food and other
goods and services. It does not include marine aquaculture and wild fish harvesting and covers forest production systems
only insofar as they contribute to food production.
² The Committee on Food Security describes food security as existing when all people, at all times, have physical, social and
economic access to sufficient, safe and nutritious food that meets their dietary needs and food preferences for an active
and healthy life. It identifies four pillars of food security – availability, access, utilization and stability, and notes that
the nutritional dimension is integral to the concept of food security. See: http://www.fao.org/fileadmin/templates/cfs/
Docs0910/ReformDoc/CFS_2009_2_Rev_2_E_K7197.pdf
³ See ftp://ftp.fao.org/docrep/fao/011/i0283e/i0283e02.pdf

76 Connecting Global Priorities: Biodiversity and Human Health

 Box 1. Risks to animal genetic resources

A total of 7616 livestock breeds from 180 countries are mentioned in the Food and Agriculture
Organization (FAO) s Global Databank for Animal Genetic Resources for Food and Agriculture. It
has been estimated that 30% of these are at risk of extinction. In contrast to crops plants where
signi cant populations of potentially valuable crop relatives exist in the wild, The state of the world’s
animal genetic resources for food and agriculture (FAO 2007) notes that “with the exception of the
wild boar (Sus scrofa), the ancestors and wild relatives of major livestock species are either extinct
or highly endangered as a result of hunting, changes to their habitats, and in the case of the wild red
jungle fowl, intensive cross-breeding with the domestic counterpart. Thus, domestic livestock are the
depositories of the now largely vanished diversity” (FAO 2007:6).

Box 2. Aquatic agroecosystems and human health

Aquatic agroecosystems, such as sh–rice systems of South and South-East Asia, contain a rich
diversity of edible species. For many rural populations living in these areas, rice and sh are the
main dietary staple. Aquatic animals are often the most important source of animal protein and are
essential during times of rice shortages, providing essential nutrients that may otherwise not be
adequate (Halwart 2006). Thus, wild and gathered foods from aquatic habitats provide important
diversity, nutrition and food security. Recent studies on the utilization of aquatic biodiversity from
rice-based ecosystems during one season only in Cambodia, China, Laos and Viet Nam found that
145 species of sh, 11 species of crustaceans, 15 species of molluscs, 13 species of reptiles, 11
species of amphibians, 11 species of insects and 37 species of plants were caught or collected
(Halwart 2013; Halwart 2006; Halwart and Bartley 2005).

Bangladesh contains a great variety of inland water bodies, including beels, ponds, rivers, canals,
ditches and rice paddy elds, which contain more than 267 freshwater sh species (Rahman 1989).
In particular, small indigenous sh species (Parambassis baculis, Parambassis ranga, Rohtee cotio,
Esomus danricus, Corica soborna, Chanda nama, Amblypharyngodon mola, Channa punctatus, Puntius
ssp.) are a rich source of highly bioavailable nutrients, animal protein and some, with a high fat
content, contain bene cial polyunsaturated fatty acids. Indigenous sh species, such as darkina
(Esomus danricus), have a high iron, zinc and vitamin A content (Thilsted 2013; see also the chapter
on nutrition).

Integrated aquatic agroecosystems demonstrate the many bene cial interactions between the
di erent elements of biodiversity that enhance food production and the ecosystem services that
support it while signi cantly increasing agricultural biodiversity and reducing production risks.
Rice plants contribute to improved water quality and ensure temperatures for optimum prawn and
sh production. Plants provide habitat and shelter for sh, reducing the risk of predation. Foraging
on aquatic sediments, including pests and weeds, and the consumption of phytoplankton by sh
enhances nutrient exchange between water and soil, and reduces the need for pesticides and
fertilizers. Small indigenous sh species also tend to be preferred by farming households and
constitute an important source of minerals, micronutrients and vitamins (Bunting and Ahmed 2014).

⁴ See also Climate change and adaptation and prawn-fish-rice agroecosystems, Landscapes Blog for People, Food and Nature
http://blog.ecoagriculture.org/2014/07/14/climate-change-adaptation-and-prawn-fish-rice-agroecosystems/

Connecting Global Priorities: Biodiversity and Human Health 77

 the genetic diversity present in the target species. terrestrial landscape has been converted for
The continuing increases in productivity achieved agriculture, with the majority (26%) of converted
over the past century have depended to a signifi- land dedicated to livestock production (Foley
cant extent on the continuing improvements made et al. 2011). In addition to food production
by plant and animal breeders. The development from agriculture, between 1% and 5% of food is
and maintenance of different crop varieties, animal produced in natural forests (Wood et al. 2000).
breeds and aquatic species’ populations provide Ellis and Ramankutty (2008) have estimated
the variety of food products that human societies that more than 75% of the earth’s ice-free land
require. Their continued improvement provides shows evidence of alteration as a result of human
the basis for meeting increased food demands and residence and land use. Over 1.1 billion people,
adaptability to changing production conditions and mostly dependent on agriculture, live within the
practices. The importance of maintaining genetic world’s 25 biodiversity “hot spots” (Cincotta and
diversity is reflected in the global concern with the Engelman 2000; Myers et al. 2002). The ways in
conservation and use of genetic resources, as evi- which humankind has influenced or managed the
denced by the publication of reports on the state different biomes around the world has resulted
of the world’s plant, animal and forestry genetic in a wide diversity of production systems (Ellis
resources (FAO 2007, 2010, 2014; see also Box 1), et al. 2010), and each production system or
the work of the FAO Commission on Genetic combination has different features, both in terms
Resources for Food and Agriculture, the estab- of the biodiversity found within the system and
lishment of the Global Crop Diversity Trust and associated impacts on human health.
the entry into force of the International Treaty on
Plant Genetic Resources for Food and Agriculture. Changes in land use and agricultural intensification
have been two of the most important drivers of
Genetic diversity within production systems is biodiversity loss in both natural and agricultural
essential for the provision of ecosystem services productions systems (MA 2005). In the section
(Hajjar et al. 2008). Although production systems that follows, the major effects of these changes
have become increasingly uniform, and dominated on agricultural biodiversity and human health are
by a few varieties of major crops, many small-scale summarized, and alternative pathways to ensuring
farmers grow and maintain a number of different adequate food production in ways that support
traditional varieties or breeds. Reasons for main- co-benefits are identified.
taining genetic diversity include: stability and risk
avoidance; adaptation and adaptability to variable, 3.1 Land use, land conversion and
difficult or marginal environments and to environ- LQWHQVLƩFDWLRQ
mental change; provision of key ecosystem services
such as pest and disease control, pollinator diver- 3.1.1 Land use and the expansion of
sity, below-ground diversity and soil health; meeting arable land
changing market demands, coping with distance
to market and adult labour availability; dietary or Heterogeneous patterns in land cover change
nutritional value; and meeting cultural and religious have followed human settlement and economic
needs (see review by Jarvis et al. 2011). development (Richards 1990; Grigg 1974;
Roberson 1956). Over the past three centuries,
roughly 12 million km² of forest and woodlands
3. Agricultural production, land have been cleared, and 5.6 million km² of grassland
use, ecosystem services and and pastures have been converted (Richards
human health 1990). At the same time, cropland areas have
increased by 12 million km², and some 18 million
Agricultural crops or planted pastures have become km² (equivalent to the size of South America) are
the dominant form of land use, comprising almost under some form of cultivation (Ramankutty and
onethird of terrestrial land (Scherr and McNeely Foley 1998).
2008). Today more than one third (38%) of the

78 Connecting Global Priorities: Biodiversity and Human Health

With land conversion has come significant tropics has come from the clearing of forests
biodiversity losses as complex forest, grassland (Gibbs 2010). Forest and woodlands are important
and wetland communities were converted carbon sinks, they play an important role in the
into highly simplified cropping landscapes. In regulation of climate (Shvidenko et al. 2005),
addition to the health effects of simplification and water flow and water quality (Shvidenko et al.
homogenization, land conversion affects human 2005) and are important sources of fibre and fuel
health in five primary ways: for numerous communities (Sampson et al. 2005).

i) Change in the delivery of supporting and Land use change, particularly deforestation for
regulating services from natural habitat agriculture, is a leading contributor of carbon
important for agricultural production; dioxide (CO2), the greenhouse gas that is the
primary contributor to climate change. An
ii) The loss of habitat for wild species, which estimated 1.3 T 0.7 Pg C year-¹ of CO2 is emitted
contribute to diets in many parts of the world as a result of tropical land-use change (Pan et al.
(reviewed in the chapter on nutrition); 2011), and land-use change accounts for 20–24%
of all CO2 emissions annually (IPCC 2014).
iii) Increased interaction with disease host, Although there is currently little agreement on
vectors and reservoirs (discussed briefly here the net biophysical effect of land-use changes on
and reviewed in the chapter on infectious the global mean temperature, its biogeochemical
diseases); effects on radiative forcing through greenhouse
gas (GHG) emissions was found to be positive
iv) Loss of medicinal plants (reviewed in the
(Working Group I Chapter 8; Myhre and Shindell
chapter on traditional medicine);
2013). The impacts of climate change are expected
to both affect and be affected by the agricultural
v) Cultural ecosystem services and mental well-
sector, with rising global temperature exceeding
being associated with interactions with nature
the thermal tolerance of certain crops (Bita and
and landscapes (see the chapter on mental
Gerats 2013), more erratic precipitation patterns
health in this volume).
(Rosenzwieg et al. 2001) and greater incidence of
Most land conversion is currently taking place disease outbreaks (Rosenzwieg et al. 2001).
in tropical forest regions, home to some of the
With the most fertile lands already used
highest levels of biodiversity globally and a critical
for farming, land conversion for agriculture
biome regulating global ecosystem services. Since
increasingly brings marginal and/or fragile lands
the 1980s, 55% of new agricultural land in the

Box 3. Soil health and agricultural biodiversity

The importance of agricultural biodiversity in supporting soil health and associated regulating and
supporting ecosystem services has been reviewed by Swift et al. (2004). The importance of diversity
of soil biota and of the maintenance of all components of the soil food web, and of diversity within
di erent levels has been described by Beed et al. (2011), Gliessman (2007) and M der et al. (2002).
However, the amount of diversity that is needed or desirable is the subject of some debate and some
authors have argued that, in functional terms, saturation is reached at fairly low levels of species
diversity. There is growing evidence that natural and less intensive agricultural production systems
have higher levels of diversity than those under intensive agriculture and that higher levels of
diversity are associated with improved delivery of key ecosystem services. Swift et al. (2004) have
noted the importance of maintaining total system diversity and of practices, such as conservation
agriculture, and mulching, which ensure higher diversity levels in the soil.

Connecting Global Priorities: Biodiversity and Human Health 79

 under cultivation. Conversion of forested hillsides a forest transition with the return of significant
and the further expansion of arable farming into areas of natural vegetation and biodiversity with
nutrient-poor tropical soils may lead to poor yields, land abandonment and replanting (Rudel et al.
with large losses in biodiversity (see Box 3 on soil 2005).
health). It is expected that land conversion will
continue to increase in some areas, particularly 3.1.ã !ntensiÍ;ation and e;osQsteE
in biodiversity hotspots around the tropics where serNi;es
human population pressures are mounting (Myers
2000). This can also lead to increased incidence of Farmers are bringing more land under cultivation
infectious diseases, covered in a separate chapter in and intensifying land use on existing farmlands
this volume. Other areas may see abandonment of by removing fallow periods, hedgerows, ditches
marginal agricultural lands (Grau et al. 2004), and and green spaces, enlarging fields and expanding
land under permanent cultivation (Stoate et al.

%R[/LYHVWRFNLQWHQVLƩFDWLRQ

As global incomes increase, diets increasingly shift from the protein derived from plant products
to increased consumption of meat, dairy and eggs, adding pressure on farming systems to increase
livestock production (Tilman et al. 2011). Global meat production is projected to more than double
from 229 million tonnes in 1999/2001 to 465 million tonnes in 2050, while milk output is set to
climb from 580 to 1043 million tonnes (FAO 2006). Already livestock production uses 30% of the
earth s entire land surface, mostly permanent pasture but also including 33% of the global arable
land used to produce feed for livestock (FAO 2006; Cassidy et al. 2013). While livestock makes an
important contribution to food security, its increased consumption is also a contributing factor to the
increase in noncommunicable diseases (NCDs) and can have negative impacts on biodiversity (as
discussed in the chapter on nutrition in this volume).

Livestock feed crops (maize, soya) in low-diversity and high-intensity cultivation systems are a very
ine cient use of resources and crop calories. For every kilogram of beef produced, 1 kg of feed is
needed (USDA 2002). At present, 36% of calories produced by cropping systems is used for animal
feed of which only 12% are ultimately used for human consumption (Cassidy et al. 2013). It has
been estimated that if these calories were consumed by people directly, the current global food
production system could feed an additional 4 billion (Cassidy et al. 2013), meeting our estimated
population growth forecasts for 2050.

The conversion of land for pasture is a major driver of deforestation. For example, in Latin America,
some 70% of former Amazonian forest has been turned over to grazing (FAO 2006). Widespread
overgrazing disturbs water cycles, reducing replenishment of above-and below-ground water
resources. Beyond land conversion, the livestock sector can also be deleterious to increasingly scarce
water resources with negative implications for human health (McMichael et al. 2007). Animal wastes
antibiotics and hormones, chemicals from tanneries, fertilizers and the pesticides used to spray feed
crops contribute substantially to water pollution, eutrophication and the degeneration of coral reefs,
while also posing health risks, such as antibiotic resistance (FAO 2006; Horrigan et al. 2002). The use
of these products not only a ects biodiversity but also has health consequences, for example, by
a ecting drinking water quality, increasing the risks for several types of cancer, undermining local
sheries – another important source of dietary protein – and contributing to endocrine disruption
and reproductive dysfunction (Horrigan et al. 2002; see also chapter on freshwater in this volume).

80 Connecting Global Priorities: Biodiversity and Human Health

2001; Wilby et al. 2009; Frison et al. 2011), as ranges and dispersal movements of the mobile
well as use of more agro-chemicals and inputs (see agents (Kremen et al. 2007). Two examples of
section 3.3.1). Although small in size, fragments the contribution of agricultural biodiversity to
of natural habitat within agricultural landscapes ecosystem services are pollination and pest and
are important for the provision of a number of disease control.
agricultural ecosystem services (Mitchell et al.
2013) and for maintaining wildlife habitats and 3.2 Pollination
corridors, which can contribute to sustainability
and conservation. The supporting and regulating The importance of insect pollination for
services upon which agriculture depends include agriculture is unequivocal, and yet global
pollination, pest control, soil health, water pollinator populations are in significant decline
regulation and nutrient cycling, largely provided by (Potts et al. 2010) with potential consequences for
associated biodiversity in and around production pollination-dependent crop yields. Globally, 35%
systems (Kremen et al. 2007). of crops depend on pollinators (Klein et al. 2007)
with an additional 60–90% of wild plant species
It has been estimated that, based on current trends also requiring animal pollination (Husband and
of greater agricultural intensification in richer Schemske 1996; Kearns et  al. 1998; Ashman
nations and greater land clearing (extensification) et al. 2004). Pollination services also contribute
in poorer nations, an estimated 1 billion ha of to the livelihoods of many farmers. It has been
land may be cleared globally by 2050 (Tilman et estimated that in 2005, the total economic value of
al. 2011). However, according to FAO estimates, pollination worldwide was €153 billion, equivalent
only about 70 million ha of additional land is likely to 9.5% of the value of the world agricultural
to be used by 2050 (FAO/PAR, 2011). In contrast, production used for human consumption. In
if the crop demand in 2050 was met by moderate terms of welfare, the consumer surplus loss was
intensification focused on existing croplands in estimated at between €190 and €310  billion
countries where potential exists, combined with (Gallia et al. 2009).
the use of appropriate technologies, only some
0.2 billion ha would be needed. Many of the crops for which pollination is
essential, including fruits and vegetables, are
The scale and nature of land conversion is important sources of micronutrients and vitamins
also important to the continuing provision of (Eilers et al. 2011). Pollinated crops contribute
ecosystem services. Many essential ecosystem 90% of the vitamin C, 100% of lycopene and
services are delivered by organisms that depend almost all of the antioxidants β-cryptoxanthin
on habitats that are segregated spatially or and β-tocopherol, the majority of the lipid vitamin
temporally from the location where services are A and related carotenoids, calcium and fluoride,
provided, such as farmed fields (Kremen et al. and a large portion of folic acid in our diets (Eilers
2007; Mitchell et al. 2013). Fine-scale green spaces et al. 2011). In terms of calories, approximately
such as hedgerows, ditches, green strips are critical one third of the human diet comes from insect-
habitats for important agricultural biodiversity pollinated plants (USDA 2002; Tscharntke et al.
such as bees, birds, arthropods and mammals, 2012). Many forage crops for livestock (e.g. clover)
and a source of many of the ecosystems services are also pollination dependent (see the chapter on
important for agriculture (Ricketts 2004, 2008; nutrition for a case study on pollination).
Kremen et al. 2007, 2012; Kremen and Miles
2012; Horrigan et al. 2002; Mitchell et al. 2013). For pollinated crop species, field size and distance
Management of organisms contributing to to natural habitat edges is a strong predictor of
ecosystem services requires consideration not fruit set (Klein et al. 2003; Ricketts et al. 2004,
only of the local scale where services are delivered 2008). As hedgerows and green spaces have been
(i.e. farmed fields), but also the distribution of eliminated from farming landscapes, and pesticide
resources at the landscape scale, and the foraging use has expanded, problems of ensuring adequate

Connecting Global Priorities: Biodiversity and Human Health 81

 pollination have increased. There is an increasing habitat types are important for the provision
trade in honey bees to provide pollination services, of pest control services. In structurally complex
although this is facing problems that appear to landscapes, Thies and Tscharntke (1999) showed
result from an unknown combination of habitat that parasitism was higher and crop damage
loss (Naug 2009), chemical use (neonicotinoids) was lower than in simple landscapes. Landscape
(Maus et al. 2003) and disease resulting in colony diversity can also be an effective way to control
collapse (reviewed in Ratnieks and Carreck 2010). non-native introduced crop pests (an emerging
Wild insect pollinators are often much more threat for many agricultural systems) through
effective than honey bees but their delivery of enhanced pest control services by native wildlife
this essential ecosystem service is also strongly (Gardiner et al. 2009).
compromised by habitat loss, land conversion and
chemical usage. The value of diversity and the importance of
maintaining natural prey/predator relations for
pest control have been demonstrated in many
3.3 Pest control
crops (Hajjar et al. 2008). Gurr et al. (2003) list
A major health concern associated with examples that range from the local field level to
agricultural intensification is the increased use of landscapes, and integrated pest management
pesticides. Among them, direct exposure to some (IPM) programmes in Asia have shown that
pesticides have been associated with neurological, conserving arthropod diversity is a key ingredient
reproductive and genotoxic effects (Sanborn et al. of their effectiveness. Pretty et al. (2006) analysed
2007) and, in some cases, prolonged exposure to 62 IPM projects in 21 countries and found that in
certain pesticides has been found to increase the 47 of them yields increased by an average of 42%
risks for certain cancers, including non-Hodgkin while pesticide use declined by 71%.
lymphoma, leukaemia, brain and prostate cancers,
among others (Bassil et al. 2007). Genetic diversity can also make a significant
contribution (Finckh and Wolfe 2006) to pest
The simplification of landscapes through the and disease control. Large-scale deployment
enlargement of fields and loss of natural habitat of mixtures of crop varieties in barley and rice
areas also influences natural pest control services have demonstrated that, even with relatively
provided by associated biodiversity. These services few components, improvements in both yield
help to reduce pest population numbers without and yield stability can be achieved (Wolfe et al.
the use of pesticides. Non-crop areas such as 1981; Zhu et al. 2000). Further work by Jarvis and
meadows, hedgerows and forest patches provide collaborators (e.g. Mulumba et al. 2012) has shown
a habitat for a wide range of natural enemies that diversity of traditional crop varieties in crops
of crop and animal pests and diseases (birds, as diverse as banana, maize and bean improves
aphids, etc.). Interspersion of natural habitats in the stability of production without a reduction in
the landscape matrix promotes the movement the crop productivity. Tooker et al. (2012) have
of natural enemies between crop and non-crop described the use of genotypically diverse variety
habitats, which is lost in landscapes dominated mixtures for insect pest management. The use of
by arable cropland (Bianchi et al. 2006). genetic diversity to reduce the impact of epidemics
has been described by De Vallavieille-Pope (2004).
In a review of studies, Bianchi et al. (2006) showed The use of diversity-based approaches to pest
that in 74% and 45% of cases, respectively, natural management in Africa are also described in Abate
enemy populations were higher and pest pressure et al. (2000).
lower in complex landscapes versus simple
landscapes. Pest predator activity was equally Crop management practices can also influence the
associated with herbaceous habitats, wooded efficiency of pest control services. Intercropping
habitats and landscape patchiness (Bianchi et and inclusion of non-crop strips within fields
al. 2006), suggesting that maintaining all three have been shown to increase the abundance

82 Connecting Global Priorities: Biodiversity and Human Health

of spiders (important pest predators) by 33% in the soil also reduce the symbiotic efficiency
(reviewed in Sunderland and Samu 2000), whereas of nitrogen-fixing rhizobia and host plants.
management practices such as undersowing, More specifically, the insecticides DDT, methyl
mulching and reduced tillage were shown to parathion, and especially pentachlorophenol
enhance spider abundance by 80% (reviewed have been shown to interfere with legume–
in Sunderland and Samu 2000). Temporal and rhizobium chemical signalling. The environmental
spatial rotation of crops on fields is another consequences are an increased dependence on
important technique used to reduce the build-up synthetic nitrogenous fertilizers, reduced soil
of pathogens in soils and spread between plants fertility, and unsustainable long-term crop yields
(Abawi and Widmer 2000). (Fox et al. 2007).

Reduced pest activity not only increases potential 2. Because of their indiscriminate mode of action,
food production, but it may also reduce or herbicides have a direct negative effect on plants
eliminate the need for pesticides and reduce the that occur in and around agricultural production
presence of deleterious compounds associated systems. These include crop wild relatives and
with specific pests. plants used for integrated pest management
strategies, such as the push – pull system. A
3.3.1 ,he use of pesti;ides and number of pesticides have also been shown to have
fertiliRers in a?ri;ultural produ;tion some direct harmful effect on plants, including
poor root hair development, shoot yellowing and
The negative effects of pesticides on human health, reduced plant growth (Walley et al. 2006).
biodiversity and agricultural biodiversity have
been well documented. Pesticides affect almost 3. It has been estimated that farmers in the United
all living organisms and it has been estimated States (US) lose at least $200 million a year from
that more than 95% of herbicides and insecticides reduced crop pollination because pesticides applied
sprayed over agricultural fields reach a destination to fields eliminate about a fifth of honeybee
other than their target species (Tyler Miller colonies in the US and harm an additional 15%
1994). Pesticides can be carried away by runoff (Tyler Miller 2004). Henry et al. (2012) found
water, seepage and leaching into ground-water, that, even with very low levels of the pesticide
streams and aquatic environments, and through thiamethoxam, a neonicotinoid insecticide, in the
soil erosion. Through drift or evaporation, air bee’s diet a high proportion of bees (more than
can transport them for short and long distances, one third) suffered from orientation disorder and
contaminating other areas, including wildlife were unable to come back to the hive, putting the
(Cornell University 2001b; National Park Service colony at risk of collapse (colony collapse disorder)
2014; Papendick et al. 1986). The following (see also Whitehorn et al. 2012). The pesticide
examples illustrate the effect of pesticides on concentration was much smaller than the lethal
agricultural biodiversity: dose currently used, and its application, together
with clothianidin and imidacloprid, was restricted
1. As persistent soil contaminants, pesticides by the European Union in April 2013 (Wall Street
negatively affect soil biota leading to lower organic Journal 2013).
matter content and reduced water retention, the
latter reducing yields in drought years (Lotter et al. The repeated application of many of the chemicals
2003). The reduction in soil- dependent ecosystem used as pesticides increases pest resistance, while
services, such as carbon and nitrogen cycling, its effects on other species can facilitate the pest’s
leads to a situation of increased dependence on resurgence (Damalas and Eleftherohorinos 2011).
externally derived chemical inputs to support This is true not only of fungicides, insecticides and
production – in fact, a negative feedback loop. The bacteriocides but also of herbicides. The law of
overall long-term effect of pesticides is a reduction diminishing returns comes into force and requires
in soil biodiversity (Johnston 1986). Pesticides increasing use of such pesticides with decreasing

Connecting Global Priorities: Biodiversity and Human Health 83

 beneficial effects and increasing detrimental effects in the United States. Herbicides (including plant
on both the environment and human health. growth regulators) accounted for the largest
portion of total use, followed by other pesticides,
The pesticide production industry is dynamic insecticides and fungicides. Although the total
and able to develop, test and market an global consumption of pesticides increased in
increasing range of chemical compounds, which 2007 (US Environmental Protection Agency
have tended to become more specific and to 2011), there is evidence that countries can make
have fewer deleterious side-effects. However, a significant difference through their legislation
many pesticides remain generic with respect to and regulations to the amounts of pesticide used.
the class of organism affected. There are now For example, Indonesia reduced expenditure on
established international and national processes pesticides (an estimate of total amount used) from
aimed at limiting the use of pesticides that have a high of US$ 120–160 million in the period from
unacceptable negative effects on the environment 1980–1987 to US$ 30–40 million in the following
or humans. The “Stockholm Convention on the 5 years.
Protection of Human Health and the Environment
from Persistent Organic Pollutants (POPs)” came It has been estimated that as many as 25 million
into force in 2004. It restricts and ultimately agricultural workers in the developing world,
aims to eliminate the production and use of listed where programmes to control exposure are limited
chemicals. This Convention also promotes the use or non-existent (Alavanja 2009), experience
of both chemical and non-chemical alternatives to unintentional acute pesticide poisoning each
POPs. Twelve chemical compounds – “the dirty year (Jeyaratnam 1990). While the acute effects
dozen” – were on the Convention’s original list of of pesticides are well documented in the literature,
POPs. Nine of the 12 are pesticides (Gilden et al. especially with respect to organophosphate
2010; UNEP 2005), including DDT (which is still poisoning (Sanborn et al. 2004), it is much less
used to control malaria). To date, ten more POPs easy to assess the chronic effects of pesticide
have been added to this list and others are under exposure. Sanborn et al. (2004 and 2012)
review (UNEP 2013). Advances in agrochemistry conducted systematic reviews to establish whether
have generally allowed pesticides to become more chronic exposure to pesticides had adverse health
species-specific and to reduce their environmental effects. Many of the reviewed studies showed
impact. Moreover, the amount applied has declined positive statistically significant associations
in many cases, sometimes by 99% (Lamberth. et al between health problems and pesticide exposure.
2013). The global spread of pesticide use, however, The continuing presence of pesticides in food,
including the use of older or obsolete pesticides water and soil is also responsible for significant
that have been banned in some jurisdictions, risks to health (U.S. Environmental Protection
continues (Kohler and Triebskom 2013). Agency 2007).

It is likely that most farmers use pesticides of some Depending on their nature, properties and mode
kind or other at some stage in their production of use, exposure to pesticides can have a wide
(Alavanja 2009). Even many small- scale farmers range of negative health effects (Cornell University
in developing countries will use some pesticides 2001a). These include the following:
and this can create major health problems through
lack of appropriate equipment or knowledge, or • Reproductive effects: effects on the reproductive
through the use of outdated products. The US system or on the ability to produce healthy
Environmental Protection Agency’s (EPA) report offspring;
on Pesticides Industry Sales and Usage (2006 and
2007 Market Estimates) reports that the amount • Teratogenic effects: effects on unborn offspring,
of pesticide used worldwide was approximately such as birth defects;
2.36 billion kg on average in 2006 and 2007, of
which more than 0.5 billion kg (21%) was used
• Carcinogenic effects: produces cancer in living
animal tissues;

84 Connecting Global Priorities: Biodiversity and Human Health

 • Oncogenic effects: tumour-forming effects (not pyrethroids, the most frequently used insecticide
necessarily cancerous); in malaria vector control (WHO 2014).

• Mutagenic effects: permanent effects on genetic The development of resistance in disease-

material that can be inherited; producing organisms, or in vectors of human
disease, as a result of pesticide overuse is one
• Neurotoxicity: poisoning of the nervous example where health problems can be combined
system, including the brain; with ecological imbalance and the development
of large pest populations. The use of herbicides
• Immunosuppression: blocking of natural in rural areas can also have associated negative
responses of the immune system responsible for effects by reducing the availability of many
protecting the body. gathered foods and thus deprives communities
of important sources of dietary diversity. The
The direct negative effects of pesticides on
same is true of the negative effects of pesticides
biodiversity and human health are numerous but
on pollinators and the availability of honey in
it should be recalled that there have also been
rural areas. More generally, the use of pesticides
very tangible benefits to human health from
as a part of simplified agricultural systems, while
the use of pesticides and insecticides, such as in
increasing the production of major staples, can lead
malaria control programmes. However, insecticide
to production systems that are more vulnerable
resistance in malaria vectors was also reported in
to change and stress, resulting in much greater
53 of 65 reporting countries around the world since
fluctuations in yield, which renders farmers and
2010. The most commonly reported resistance is to
BIOVERSITY INTERNATIONAL

Connecting Global Priorities: Biodiversity and Human Health 85

 rural communities liable to complete losses in arable, grassland and horticultural soils can also
production and loss of food security. lead to the accumulation of nitrites and organic
nitrogen compounds such as amines, nitro and
Fertilizers nitroso compounds, including nitrosamines and
nitrosamides (Barabasz et al. 2002).
The overuse of synthetic fertilizers has major
negative effects on biodiversity, particularly Many studies have shown that mineral
freshwater and marine biodiversity and soil biota. fertilization strongly affects both the number of
It also has negative effects on human health, microorganisms in the soil and the make-up of
most obviously perhaps through pollution of communities of soil microorganisms (Barabasz et
groundwater and reduction in the availability al. 2002). Use of mineral fertilizers can also lead to
of unpolluted fresh water. As with pesticides, increased heavy metal accumulation in soils, and
there are points of interaction between loss of potential health problems have been identified
biodiversity and human health such as through in connection with increased levels of cadmium,
the damaging effect of algal blooms and the arsenic, lead and mercury. Eutrophication is also
increased frequency of toxic phytoplankton as a major problem caused by the excessive inputs
described in the chapter on freshwater in this of phosphorus and nitrogen in lakes, reservoirs,
volume. The increasing size of marine dead rivers and coastal oceans (Smith and Schindler
zones also has a significant negative effect on the 2009, see also the Box on eutrophication in the
availability of fish for human consumption. While chapter on freshwater).
the application of synthetic fertilizers makes a
significant contribution to improving overall food
3.4 Non-food crops
production and may be especially important in
parts of Africa, for example, overuse has created The demand for non-food crops has grown with
major environmental problems in Asia. Large-scale the population and increasing prosperity. This
synthetic fertilizer use is often associated with has resulted in the conversion of larger areas of
reduced adaptability and resilience in production land for the production of (what some consider)
systems and, in some stress situations, with “luxury” foods (e.g. coffee, tea, cacao), fibres (e.g.
reduced yield stability. Both synthetic fertilizers cotton), biofuels and oil (e.g. palm oil, rapeseed).
and pesticides can create negative feedback loops Many of these crops grow exclusively in tropical
in which the reduced agricultural biodiversity climates (e.g. coffee, tea, cacao, oil palm) with
associated with their use is accompanied by production areas occurring almost wholly within
production problems associated particularly with areas identified as biodiversity hotspots (Myers
loss of soil biota. et al. 2000), suggesting that production of
such crops may have an environmental impact
The negative effects of synthetic fertilizers on soil disproportional to its area (Donald 2004). The
biota, soil acidification and groundwater pollution expansion of production of these crops in the
can be significant (Osborne 2011). Nitrogen that is twentieth and twenty-first centuries has come at
not taken up by plants is transformed into nitrate, great expense to local biodiversity (reviewed in
which is easily washed off the soil into watercourses Donald et al. 2004).
or leached through soil into groundwater (Jackson
et al. 2008; Barabasz et al. 2002). Nitrate levels 3.5 Impacts of agricultural
above 10  mg/L in groundwater can cause LQWHQVLƩFDWLRQRQKXPDQKHDOWK
acquired methaemoglobinemia in infants (also
called “blue baby syndrome”), which leads to Agricultural intensification has involved the use of
an overall reduced ability of the red blood cell increasingly productive crop varieties and animal
to release oxygen to tissues, possibly leading to breeds, combined with the continually expanding
tissue hypoxia (Knobeloch et al. 2000; Self and use of chemical inputs, fossil fuel energy and
Waskom 2013). High N fertilizer rates applied to water in both plant and animal production
systems. The most important chemical inputs

86 Connecting Global Priorities: Biodiversity and Human Health

have been pesticides of many different types and systems. Food transport and processing have also
fertilizers. Fossil fuel energy inputs have included become increasingly important aspects of the
mechanization of cultivation and harvesting, overall food system with consequences both for
and the use of more intensive animal production human health and agricultural biodiversity.

Box 5. Case study: biofuels

Crops for industrial use, including biofuels, make up 9% of crops by mass, 9% by calorie content,
and 7% of total plant protein production, diverting a considerable quantity of food away from
human consumption (Cassidy et al. 2013). In 2000, biofuel production alone represented 3% of
crop production and is estimated to have increased more than 450% (in terms of litres produced)
between the year 2000 and 2010 (WWI 2009), suggesting that increasing areas of land are being
dedicated to the production of intensively managed corn, vegetable oils and sugarcane (Cassidy
et al. 2013). Based on biofuel statistics from 2010, ethanol production from maize in the United
States and from sugarcane in Brazil alone now represents 6% of global crop production by mass
and 4% of calorie production (FAPRI 2011). Although biofuels are meant to help reduce the
dependence on carbon-dense energy sources and reduce carbon emissions to mitigate climate
change, the production of food crops for biofuels can have additional negative impacts on human
health associated with (i) intense production techniques (i.e. air quality from forest burning, high
chemical use and contamination of waterways) and (ii) diversion of crop calories away from the food
production system. In addition to biofuels, signi cant portions of cultivated land are dedicated to the
production of bres, in particular cotton, as described in the chapter on freshwater.

Box 6. Case study: vegetable oils

Vegetable oils are among the most rapidly expanding agricultural sectors (Clay 2004), and more
palm oil is produced than any other vegetable oil (Carter et al. 2007). A native of West Africa, oil palm
(Elaeis guineensis) is grown across more than 13.5 million ha of tropical, high-rainfall, low-lying areas,
a zone naturally occupied by moist tropical forest, the most biologically diverse terrestrial ecosystem
on earth (Corley and Tinker 2003, MEA 2005). Palm oil has some of the world s largest plantations,
sometimes exceeding 20000 ha (Donald 2004), cut out of the tropical rainforests of Indonesia,
Malaysia and increasingly in Latin America. This has resulted in extensive clearing and burning
of carbon-rich forests and peat lands, contributing to biodiversity loss, poor air quality a ecting
respiratory health particularly in South-East Asia, and adding CO2 to the atmosphere (Clay 2004).
Examination of palm oil cultivation in contrast to shaded co ee, pasture and natural forest found
that palm plantations supported extremely low levels of birds, lizards, beetles and ant communities
(Power and Flecker 1998; Chung et al. 2000; Glor et al. 2001).

Per unit area, palm oil is the highest-yielding vegetable oil crop; the current global production of oil
palm fruit is estimated at 97.7 million tons, produced from 10.7 million ha; production is increasing
by 9% every year (Donald 2004). Palm oil now makes up about 21% of the world s production of
edible oils and fats, second only to soybean oil. The oil is used in the manufacture of cooking oil,
margarine, soap and cosmetics, and it has industrial uses. As a substitute for diesel, palm oil is less
suitable than other vegetable oils owing to its high viscosity, lower energy density and high ash
point (Agrawal 2007). However, oil palm gives high yields at low prices, and hence is likely to be
important in meeting biofuel demand (Carter et al. 2007; Koh 2007).

Connecting Global Priorities: Biodiversity and Human Health 87

 Specialization in one or a select number of and we will need genetic diversity to adapt to these
crop or animal species has reduced agricultural changing conditions.
biodiversity, affecting ecosystem services
and human health (Frison et al. 2011). The 3.6 Alternative production pathways
introduction of invasive alien species can also
have negative impacts on biodiversity, terrestrial The negative effects of modern intensive
and aquatic agriculture, and related provisioning agriculture on the environment and human health,
and regulating ecosystem services (Pejchar and together with concerns about the unsustainable
Mooney 2009). As discussed in the chapter on nature of many of the practices (e.g. with regard
freshwater, these impacts extend to human health. to water and phosphate use), the continuing
These trends can also affect the diversity of foods failure to deal with malnutrition and the need to
being produced for human consumption and alter confront the challenges of climate change, have led
agro-ecological processes (Kremen and Miles 2012 to the identification of an increasing number of
and references therein). Intercropping of species alternative approaches to agricultural production
and agroforestry practices (the maintenance of (e.g. Baulcombe et al. 2009; PAR/FAO 2011; FAO
perennials in fields) have been shown to enhance 2011; de Schutter 2010). The assessment that
above- and below-ground associated biodiversity, the food systems in place are no longer “fit for
soil quality, water-holding capacity, weed control, purpose” has been reflected in growing consumer
disease and pest control, pollination, carbon concerns and the growth of civil society groups
sequestration, and resilience to droughts and concerned about securing healthy and safe food
hurricanes (reviewed in Kremen and Siles 2012). production (Rosin et al. 2012).

There is also concern that industrialized farming Alternative approaches to ensuring sufficient
systems are vulnerable to the same disease risks as production to meet human needs in
crop monocultures. The level of genetic diversity environmentally safe ways are broadly based
in livestock breeds has fallen dramatically over the on enhancing the use of biological processes
past century as a result of intense selection. In in agriculture. There are many alternative
cattle, the Holstein breed dominates production approaches and concepts variously identified as
in the West and intensive sire selection is leading agroecology, ecological intensification or, more
to rapid inbreeding rates with a few sons of generally, as an ecological approach to agricultural
sires and grandsires dominating US populations production (Altieri et al. 1995; De Schutter
(Holstein Assoc. USA 1986). Over the past 100 2010; FAO/PAR 2011). Ecological approaches
years, approximately 28% of livestock breeds are characterized by minimal disturbance of the
have become rare, endangered or extinct globally ecosystem, plant nutrition from organic and
(Notter 1999). This is particularly worrisome non-organic sources, and the use of both natural
as genetic diversity is required to meet current and managed biodiversity to produce food, raw
production needs in various environments, to materials and other ecosystem services. This way,
allow sustained genetic improvement, and to crop production not only sustains the health of
facilitate rapid adaptation to changing breeding farmland already in use, but can also regenerate
objectives (Notter 1999). Modern agricultural land left in poor condition by past misuse (FAO
production systems decouple agriculture from 2011). This approach to agricultural production
the surrounding environment, controlling feed, emphasizes the importance of maintaining natural
water, temperature and disease in large industrial ecosystem services and function in agricultural
complexes, selecting for animals with very little production systems rather than replacing them
environmental tolerance. In the interim, we with external inputs.
will lose breeds with a range of environmental
There are a wide range of ecologically based options
tolerances (Tisdell 2003). As climate change
including conservation agriculture (Kassam et al.
progresses, the future will not look like the present
2009), organic agriculture (Badgley et al. 2007),

88 Connecting Global Priorities: Biodiversity and Human Health

integrated pest management (IPM), integrated between diet and local food sources, a situation
plant nutrition systems, ecoagriculture (Scherr that threatens the continued existence of valuable
and McNeely 2007), sustainable crop production agricultural biodiversity and the knowledge
intensification (FAO 2009) and agroecology associated with it.
(Wezel et al. 2009). Many of these have already
been deployed in large production areas although The development of widely adapted, highly
they are yet to be universally accepted or adopted, uniform crop and livestock varieties has
and each has its own community of advocates and played a major part in the homogenization
detractors. of agriculture. Such varieties or breeds can be
grown and produced over very wide areas (many
Ecological approaches to agricultural millions of hectares) owing partly to their broad
intensification make increased use of agricultural adaptation and partly to the homogenization
biodiversity and are expected to create conditions of agricultural production systems that can be
that will support the maintenance of biodiversity achieved through chemical inputs and irrigation.
as a whole and improve human health, either The use of genetic modification and production
directly or indirectly. Some of the features of of genetically modified organisms (GMOs) has
such approaches with respect to agricultural added a dimension that has been the subject of
biodiversity and to human health are illustrated substantial controversy (Letourneau and Burrows
in the section that follows. 2010; Costa-Font et al. 2010). The implications
for human health of the widespread adoption of
commercialized edible GMOs, including soy, maize
4. Food production, food security
and oilseed rape, is also disputed (summarized in
and human health De Vendômois et al. 2010 and references therein;
Dona and Arvanitoyannis 2009). Certainly some
4.1 Agricultural biodiversity and food
of the practices associated with their use may have
production undesirable side-effects such as the widescale use
Many barriers and challenges continue to of herbicides. However, others have suggested
hinder the optimum utilization and sustainable that GMO crop varieties reduce pesticide use and
management of agricultural biodiversity, which result in positive health benefits (Phipps and Park
have caused it to be relegated to a minor role 2002). There are also concerns with respect to the
in agriculture and health (Hunter and Fanzo unplanned spread of novel genes into wild crop
2013). This neglect of agricultural biodiversity relatives or to traditional varieties, especially in
continues to come at a great cost to national centres of crop diversity (Stewart et al. 2003).
health-care budgets, the global environment This unplanned spread could have significant
and society in general (see chapter on nutrition). negative consequences for existing patterns of
Globalization and the simplification of agriculture, within-species diversity, changing fitness levels
population increase and urbanization, along with of populations and varieties, and hence their
public policies that continue to provide perverse potential long-term survival and evolution.
incentives for unsustainable food production,
have changed patterns of food production and Shifts to monoculture or low diversity cropping
consumption in ways that profoundly affect systems in turn have led to the homogenization
ecosystems and human diets, and have led to of global food production and the loss of regional
increasingly dysfunctional food systems. High- and endemic crop types, while the adoption of
input industrial agriculture and long-distance global staple crops is changing people diet as
transport increase the availability and affordability many diets shift towards common starchy energy-
of refined carbohydrates and fats, leading to an dense foods crops in place of traditional crops or
overall simplification of diets and reliance on a varieties (Padulosi et al. 2002; Malaza and Howard
limited number of energy-rich foods (Figure 1). 2003; Adoukonou-Sagbadja et al. 2006; Smale et
This has also resulted in a considerable disconnect al. 2009). Such shifts have led to a global trend

Connecting Global Priorities: Biodiversity and Human Health 89

 ǡǤǢǰǭǠɻ The limited use of plant species diversity in agriculture

Source: FAO, 1995

of increased quantities of food calories, proteins et al. 2002) and Western Australia (Wellings et
and fat for human consumption, but they are al. 2003), as well as Central and northern Europe
increasingly sourced from a handful of energy- (Flath and Barthel 2002; Hovmoller and Justesen
dense foods (Khoury et al. 2014). Consequently, 2007). The vast and expansive spread of diseases
national food supplies worldwide became more affecting a small number of globally important
alike in composition, correlated with an increased crops can have important consequences for both
supply of several globally important cereal and local and global food supplies and human health
oil crops, and a decline of other cereal, oil and (Hovmoller et al. 2008).
starchy root species. The increase in homogeneity
worldwide portends the establishment of a global Such generalizations (Figure 1) mask the diversity
standard food supply, which is relatively species- of food crops, animal breeds, fish populations
rich with regard to measured crops at the national and genetic diversity that is still maintained
level, but species-poor globally (Khoury et al. and further developed by small-scale farmers,
2014). pastoralists and fisherfolk worldwide, and which is
available and produced in many of the world’s food
Agricultural homogenization not only affects production systems. Crop and livestock production
diets, but potentially the resilience of global food systems that are often the target of agricultural
systems. Such cropping patterns make both local development are in reality often elements of a
and global production landscapes vulnerable to larger landscape that comprises a broad range of
wide sweeping pest and disease outbreaks. As wild, weedy and feral species that not only play
landscapes become increasingly similar in the critical roles in securing food production and
crop composition, pests and pathogens, including ecosystem function but which may also contribute
those that are invasive, have increasingly large significantly to human diets, food security and
and connected cropland areas to infect and infest health, such as many of the wild edible species
– both through natural dispersal and through found in and around aquatic agricultural systems
increasingly integrated transportation and trade or forests. Wildlife is consumed as bushmeat,
pathways. This can be seen in the recent epidemics and wild leafy and fruit species, and other edible
of virulent yellow wheat rust, Puccinia striiformis species such as insects and mushrooms found in
f. sp. tritici that have appeared in new areas, e.g. and around agricultural fields play an important
eastern USA (Chen 2005), South Africa (Boshoff role in feeding populations in many parts of

90 Connecting Global Priorities: Biodiversity and Human Health

the world (PAR/FAO 2011). Despite potential Asia improve ecosystem function, nutrition
health benefits of bushmeat consumption, as and income in many different farming systems
the nutrition chapter also indicates, health risks (Halwart 1998; Pullin and White 2011; see
associated with its unsafe handling, storage also Box 2). Integrating trees into agricultural
and growing illegal trade must also be carefully environments helps to realize the full potential
considered (see also the chapter on nutrition of agroforestry ecosystem function and provides
in this volume). Agricultural intensification has marketable products (Garrity et al. 2010).
also often upset the balance maintained by rural
communities between sustainably managed All alternative approaches to agricultural
natural areas and farmed areas, leading not intensification based on increasing chemical
only to reductions in uncultivated areas but also inputs and uniformity of production systems
overexploitation of the resources that remain. involve increased use of agricultural biodiversity.
This increased use takes two forms: (1) the use of
different materials adapted to different agronomic
å.1.1 %ixed farEin? ;rop and Ísh
practices and reduced inputs, and (2) the use of
and a?roforestrQ x in;reasin? spe;ies
increased diversity at ecosystem, species and
diNersitQ
genetic levels (or at landscape, farm and field
Diverse production systems with a number of scales) (PAR/FAO, 2011), i.e. the use of more
different productive components themselves species, crop varieties, livestock breeds and wild
confer multiple benefits. The forms that these populations. As De Schutter (2010) noted in his
can take are many and varied. For example, home report to the UN Secretary General on the role of
gardens, which are characterized by high levels agroecology in food security, “These approaches
of species diversity in a relatively small space, involve the maintenance or introduction of
are highly productive with multiple livelihood, agricultural biodiversity (diversity of crops,
health and biodiversity maintenance benefits livestock, agroforestry, fish, pollinators, insects,
(Galuzzi et al. 2010; Box 7 on home gardens). soil biota and other components that occur in
Diversity in livestock production has been shown and around production systems) to achieve the
to confer benefits through improved provision of desired results in sustainability and productivity.”
nutrients, overall productivity, system resilience It has been estimated that traditional agricultural
and income (Morton, 2007). The aquatic rice- landscapes that are complex and rich in agricultural
based agroecosystems of South and South-East biodiversity still provide as much as 20% of the

Box 7: Home gardens

Home gardens are estimated to support nearly 1 billion people in the tropics and contain remarkable
diversity of food and other utilitarian species – up to a hundred or more species per garden – and
o er great potential for improving household food security and alleviating micronutrient de ciencies
(Heywood 2013). E orts to promote nutritious biodiversity through home gardens have been the
target of food security and nutrition interventions in many countries (Nielsen et al. 2013; Pudasaini
et al. 2013), and may also provide animal products such as chickens, eggs and livestock as in the
case of the homestead gardens promoted by Helen Keller International. Some studies have found
that a child s nutritional status is associated with the presence of a home garden and that the
garden s biodiversity, rather than its size, is the most important factor ( ones et al. 2005). In addition
to enhancing food security and nutrition, the presence of home gardens in highly populated areas
creates a pleasant and aesthetically pleasing environment, which may have broader health bene ts,
including mental health bene ts, as well (Pushpakumara et al. 2012).

Connecting Global Priorities: Biodiversity and Human Health 91

 world’s food supply (Heywood 2013). This may 2009). At the same time, according to recent
be a significant underestimate given that it has estimates, over 2 billion people worldwide are
also been estimated that small-scale producers overweight or obese (Ng et al. 2014).
produce most of the world’s food (Pretty and
Barucha 2014). We face a major global problem associated with
the replacement of foods derived from biodiversity
with high nutritional significance by globally
4.2 Global food security, biodiversity
marketed foods that are higher in energy but less
and human health
dense in nutrients and other functional factors
With the growing demand of an expected 9 billion that often confer some degree of protection
people by 2050, the world still faces tremendous against disease. The result is an emerging “double
challenges in securing adequate food that is burden”⁵ of malnutrition and “hidden hunger”⁶
healthy, safe and of high nutritional quality for all, in developing countries. Up to half a million
and doing so in an equitable and environmentally vitamin A-deficient children go blind every year,
sustainable manner (Pinstrup-Andersen 2009; half of them dying within a year of losing their
Godfray et al. 2010; Tilman et al. 2011; Foley sight; and iron deficiency is damaging the mental
et al. 2011). Climate change, ecosystems and development of 40–60% of children in developing
biodiversity under stress, increasing urbanization, countries. The estimated cost of undernutrition
social conflict and extreme poverty all make to potential economic development is between
attaining this challenge difficult. US$ 20 and 30 billion annually (Shetty 2010, see
also Chapter on nutrition within this volume).⁷
Despite progress in feeding a growing population,
we still live in a world with a highly dysfunctional, The Declaration of the World Summit on Food
and inequitable, food system, where there has Security (FAO 2009) addresses the issue of
been a failure to achieve global food security, in investments in agriculture highlighting that
which we have been unable to feed a significant efforts should focus more on sustainability by
part of humanity adequately, and which supporting sustainable agricultural production
continues to contribute to environmental and and practices aimed at conservation and improved
health problems, high species extinction rates, use of the natural resource base and protection of
loss of genetic diversity, and land and ecosystem the environment and enhanced use of ecosystem
degradation (Rosin et al. 2012). One major issue services. Some of the key aspects of improving
is the apparent continuing lack of political will and food security identified by the World Food
moral imperative (Horrigan et al. 2002). This is Summit where agricultural biodiversity is relevant
reflected in such continuing problems as the scale are listed in Box 8 (FAO/PAR, 2011).
of food waste. Of the total food produced, about
30% is lost through post-harvest losses on farms å.ã.1 liEate ;han?e food se;uritQ and
or in the process of marketing, distribution and huEan health
consumption (Lundqvist 2008). There is clearly
significant potential to improve the availability of FAO estimates that food production over the next
food and reduce hunger through reducing these 40 years will need to increase by about 70% in order
losses. In addition to the continued problems of to cope with increasing population and dietary
hunger, micronutrient deficiencies undermine the demands for more animal-sourced foods. Over
growth and development, health and productivity the same time frame, climate change is expected
of over 2 billion people (Micronutrient Initiative to cause significant reductions in not only crop

⁵ The Double burden of undernutrition and overnutrition.

⁶ Hidden hunger – a lack of essential vitamins and minerals often results in “hidden hunger” where the signs of malnutrition
and hunger are less visible in the immediate sense. See also chapter on nutrition in this volume.
⁷ Shetty P. (2010) The challenge of improving nutrition: fact and figures. SciDevNet. http://www.scidev.net/en/health/the-
challenge-of-improving-nutrition/features/the-challenge-of-improving-nutrition-facts-and-figures-1.html

92 Connecting Global Priorities: Biodiversity and Human Health

 %R[.H\DVSHFWVRILPSURYLQJIRRGVHFXULW\LGHQWLƩHGE\WKH:RUOG)RRG6XPPLW
Declaration which particularly involve agricultural biodiversity

• Increase production including through access to improved seed and inputs; reduce pre- and post-
harvest losses; pay special attention to smallholders.

• Implement sustainable practices, including responsible sheries, improved resource use,

protection of the environment, conservation of the natural resource base and enhanced use of
ecosystem services.

• Ensure better management of the biodiversity associated with food and agriculture; support the
conservation of and access to genetic resources, and fair and equitable sharing of the bene ts
arising from their use.

• Recognize that increasing agricultural productivity is the main way to meet the increasing
demand for food, given the constraints on expanding the amount of land and water used for food
production.

• Mobilize the resources needed to increase productivity, including research, and the review,
approval and adoption of biotechnology and other new technologies.

• Enable all farmers, particularly women and smallholder farmers from countries most vulnerable to
climate change, to adapt to, and mitigate the impact of, climate change.

• Support national, regional and international programmes that contribute to improved food safety
and animal and plant health.

• Encourage the consumption of foods, particularly those available locally, which contribute to
diversi ed and balanced diets.

• Address the challenges and opportunities posed by biofuels.

Reference: FAO/PAR 2011

production but also the nutritional content of in particular will be impacted, especially in arid
foods, particularly in respect of production of C3 and semi-arid regions, including effects on pasture
grains and legumes, which provide a large portion species composition and forage quality. Further,
of the global population with their primary source increasingly frequent and severe pest and disease
of iron and zinc. Increasing CO2 levels will lead attacks are expected. Bebber et al. (2013) highlight
to reductions ranging between 5% and 10% in poleward movements of pests and pathogens to
the iron and zinc content of the edible portion new areas from 1960 onwards. While soil-borne
of these crops, possibly increasing the burden of pathogens and diseases are likely to be more
disease for these deficiencies that already cause a of a problem under increasing temperatures
loss of 63 million life-years annually (Myers et al. (Jaggard et al. 2010), Tirado et al. (2010) and
2014). Climate change is also expected to impact Lake et al. (2012) also highlight the likelihood of
heavily on fish and livestock resources. Livestock climate change impacts on food contamination

Connecting Global Priorities: Biodiversity and Human Health 93

 and foodborne diseases through the increased Crop wild relatives represent one of our most
incidence of existing pathogens or the emergence precious resources in trying to deal with climate
of new pathogens. The Fifth Assessment Report of change, while at the same time improving the
the Intergovernmental Panel on Climate Change⁸ nutritional quality of crops and food (Hunter and
concluded that climate change is affecting all Heywood 2011). As well as containing genetic
aspects of food security and agriculture, and that traits for enhanced nutritional quality, they
impacts on crop yields are already evident across also have novel pest resistance and tolerance to
several regions of the world. heat, drought and salinity, among other traits
(Godfray et al. 2010; Hunter and Heywood 2011;
Agricultural biodiversity, including utilization, Hodgkin and Bordoni 2012). Crop wild relatives
and maintenance of plant genetic resources have already provided many useful genes for crop
for crop improvement and diversification, is improvement, which have been introduced to
an important strategy in dealing with ongoing improve varieties through conventional breeding
climate change and food security (FAO 2015). In techniques in crops as diverse as wheat, potato,
addition to their nutritional potential, Foley et tomato and lettuce (Hajjar and Hodgkin, 2007).
al. (2011) highlight important opportunities to However, crop wild relatives, as well as other
improve crop yield and resilience, by improving genetic diversity, cannot be taken for granted and
the myriad neglected and underutilized species they are currently under threat from changing
and conserving crop diversity as well as crop wild climate (Jarvis et al. 2008; Lira et al. 2008; Hunter
relatives. Bambara groundnut (Vigna subterranea) and Heywood, 2011).
is well known for its drought tolerance and ability
to grow in harsh and marginal environments, as Negative impacts on crop yields or when crops fail
are a number of minor millets commonly grown as a result of climate change may mean a greater
in South Asia. Ca˜nihua (Chenopodium pallidicaule), role for wild food species for food security and
an underutilized Andean grain, has significant nutrition in the future. Yet climate change is also
frost tolerance, while the perennial seabuckthorn likely to negatively impact on wild edible species
(Hippophaerhamnoides) has considerable tolerance themselves. A recent study (Carr et al. 2013) of
to abiotic stresses like frost and cold, assumed to wild plant and animal species of the Albertine
be associated with the high levels of ascorbic acid Rift region of East and Central Africa combined
and myo-inositol it contains (Padulosi et al. 2011; climate change vulnerability and use assessments
Yadav et al. 2015). to identify those species utilized by communities

Box 9. Agro-ecological resilience after Hurricane Mitch in Nicaragua

In October 1998, Hurricane Mitch hit Central America, causing damage worth at least US 6.7 billion.
Over 10000 people died and 3 million were displaced or left homeless. In Nicaragua, a comparative
study was carried out using participatory approaches, which involved farmers and local NGOs,
on the levels of resistance to the hurricane of “sustainable” farms using a variety of sustainable
land management practices, and neighbouring “conventional” farms that lacked those practices.
On average, agro-ecological plots on sustainable farms had more topsoil, higher eld moisture,
less erosion and lower economic losses after the hurricane than the plots on conventional farms.
The di erences in favour of agro-ecological plots tended to increase with increasing levels of
storm intensity, increasing slope and years under agro-ecological practices, though the patterns of
resistance suggested complex interactions and thresholds.

(Holt-Gimenez 2002. See also the Chapter on disaster risk reduction in this volume)

⁸ http://www.ipcc.ch/report/ar5/

94 Connecting Global Priorities: Biodiversity and Human Health

most likely to be negatively impacted by climate agricultural biodiversity to food security and
change. The study found that 14 amphibians (13% human health. These are listed below:
of those assessed), 17 birds (2%), 19 freshwater
fish (3%), 24 mammals (7%), 33 plants (36%) 1. There are still significant knowledge gaps in
and 25 reptiles (15%) of known importance for relation to the optimum use and deployment of
use, including food, were among those at greatest agricultural biodiversity in production systems.
vulnerability to climate change impacts. For The ways in which agricultural biodiversity can
these reasons, better knowledge of how wild food improve ecosystem-regulating and-supporting
species are likely to be impacted by climate change services is still poorly understood in terms of how
will be critical for both biodiversity conservation to achieve real benefits in different production
and developing sustainable use and livelihood systems. This will involve a substantial programme
strategies. of integrated transdisciplinary research, which
fully involves producers, and links the production
More biodiversity-friendly crop and food of improved crop and livestock materials to the
production mitigation strategies that might adoption of agronomic practices that support
contribute to reduced methane and nitrous biological functions in production systems.
oxide emissions could include improved soil
management practices, such as the enhanced 2. The importance of diversity-rich production
use of mulching, cover cropping, conservation systems and diversification is widely recognized
agriculture, more efficient N utilization, as in respect of their contribution to food security,
well as improved rice cultivation and manure sustainability, adaptation to change and human
management practices (Reynolds and Ortiz health. However, the ways in which such
2010; Cribb 2010). Among other things, such approaches can be adopted with direct benefits
strategies will require new crop varieties, including to producers who are committed to uniform
breeding of varieties with reduced carbon dioxide non-diverse approaches has not been clearly
and nitrous oxide emissions, different crop established. This will involve taking account
combinations, and modified management systems of biological, social, economic and political
and agronomic practices (Hodgkin and Bordoni dimensions, and of recognizing both producer and
2012; Reynolds and Ortiz 2010). consumer concerns.

3. Even when practices that provide food security,

5. Conclusions health and diversity benefits have been identified
The increase in food production achieved over (such as alternatives to the use of pesticides or of
the past decades has been accompanied by reducing the pollination deficit through improved
significant losses in agricultural biodiversity, pollinator diversity), there remain economic,
as production systems (crop and animal) have policy and other barriers to the adoption of such
become more uniform and dependent on practices, especially at the national level. These
externally derived chemical inputs. The loss of need to be identified and alternatives adopted. It
agricultural biodiversity has been associated with will be especially important to investigate ways
reductions in ecosystem service provision, often in which the full economic value of the use of
accompanied by negative impacts on human agricultural biodiversity can be measured and
health. It is clear that agricultural biodiversity rewarded.
can make significant contributions to improving
food security, nutrition and human health, and 4. A number of international policies and
will play an essential role in achieving sustainable instruments have been developed to take account
food production and improving the productivity of the importance of agricultural biodiversity.
needed to meet the challenges of climate change. However, there remain significant challenges in
The chapter points to a number of areas of work achieving full recognition of its importance in, for
that can help to improve the contribution of

Connecting Global Priorities: Biodiversity and Human Health 95

 example, climate change adaptation agendas⁹ and sustainable and resilient food production systems,
the global food security debates of the Committee and maintaining genetic diversity provide a
on World Food Security (CFS). A key objective of framework for developing a compelling agenda
international policy efforts should be to ensure the on the value of the improved use of agricultural
enhanced availability of agricultural biodiversity biodiversity.
to users.
6. The growing concerns of consumers about
5. Sustainable development goals and targets, and food production approaches and the demand for
the post-2015 Development Agenda provide an environmentally friendly approaches that provide
important global entry point to better recognition adequate rewards for rural communities and safe
of the ways in which agricultural biodiversity food provide important entry points for exploring
and health co-benefits can be maximized. The the contributions that agricultural biodiversity can
goals of ending hunger, malnutrition, increasing make to these wider social objectives.
agricultural productivity and incomes, ensuring

BIOVERSITY INTERNATIONAL

⁹ The recent adoption of guidelines on the integration of genetic diversity in climate change adaptation planning by the FAO
Commission on Genetic Resources for Food and Agriculture is a beneficial development.

96 Connecting Global Priorities: Biodiversity and Human Health

 6. Biodiversity and Nutrition
RAWPIXEL LTD

1. Introduction deficiencies alone can lead to several global health

and development challenges, impaired intellectual
Malnutrition remains one of the greatest global and psychomotor development, reduced physical
health challenges we face and women and children growth, and a range of other problems. It has also
are its most visible and vulnerable victims. been found to increase morbidity from infectious
Agricultural production is theoretically able to diseases in infants and young children (see
feed the world’s population in terms of calories Muthayya et al. 2013 and references therein).
(FAOSTAT, 2014), yet it is estimated that half
the world’s population still suffers from one or In recent years, the direct and indirect dependence
more forms of malnutrition. In all its forms, and impact of human nutrition on biodiversity
malnutrition is closely linked to disease – as both has been increasingly acknowledged by the
a cause and effect  – and it is the single largest health (WHO 2012b; UN SCN 2013 and ICN2),
contributor to the global burden of disease (WHO agriculture (FAO 2013a) and environment sectors
2012a). (UNEP 2012; CBD 2014). These activities have
included landmark research efforts, innovative
Countries are increasingly facing complex multiple development programmes and projects, policy
burdens of malnutrition, with undernutrition initiatives, and advocacy campaigns.
and micronutrient deficiencies coexisting with
overweight and obesity in many parts of the Biodiversity is a key source of food diversity
world, often even within the same population or and provides a natural richness of nutrients
family (Shrimpton 2013). Based on data released (macronutrients such as carbohydrates, proteins
in 2014, 161 million children under the age of five and fats, and micronutrients [vitamins and
are estimated to be stunted, almost 1.5 billion minerals] and bioactive non-nutrients for healthy
people are estimated to be overweight, over human diets (Blasbalg et al. 2011; Fanzo et al.
600 million to be obese (Ng et al. 2014) and two 2013). In addition, biodiversity also underpins
billion are estimated to be deficient in one or more critical supporting ecosystem services, such as
micronutrients, a phenomenon referred to by pollination and soil fertility, essential to food
some as “hidden hunger”. These conditions all have production, both in terms of quantity and quality.
severe consequences for survival, for morbidity,
and for the ability of individuals, the economy In the field of nutrition, food is seldom dealt with
and society to thrive (IFPRI 2014). Nutrient independently of the nutrients it contains, the

Connecting Global Priorities: Biodiversity and Human Health 97

 whole diet of which it is a part and the ecosystems Agricultural programmes and policies often focus
it is derived from. Taking a whole diet approach on increasing the production of a few staple crops,
enables the use of different combinations of diverse and their success is measured in terms of the food
foods, and their many interactions, to improve quantity or dietary energy supply. Ample quantity
dietary quality and meet nutritional needs. It also does not necessarily ensure appropriate nutritional
takes into account local knowledge – threatened quality, with staple crops unable to provide the
in many parts of the world (Sujarwo et al. 2014) – diversity and adequate amounts of nutrients to
and cultural acceptability and culinary traditions. meet human requirements, especially much-
needed micronutrients. This has led to numerous
Biodiversity for human nutrition therefore calls demanding new approaches to agriculture for
includes the diversity of plants, animals and improved nutrition outcomes, often referred to
other organisms used in food systems, covering as “nutrition-sensitive agriculture” (Ag2Nut CoP,
the genetic resources within and between species, 2013; Turner et al, 2103; McDermott et al. 2015).
and provided by ecosystems. In nutrition science,
however, the diversity of diets covers mostly the Notwithstanding the productivity successes
inter-species biodiversity, and the intra-species achieved in the agricultural sector in the past
biodiversity is a still underexplored dimension several decades, it is becoming increasingly
from a nutritional perspective. clear that current methods and levels of food
production and consumption are not sustainable,
Despite the increased recognition of the potential (FAO 2013b) and that finite natural resources and
of biodiversity for nutrition, national global food genetic diversity are being corroded or lost in the
supplies have become more homogeneous in process. A reduction in biodiversity is a prime
composition, being largely dependent on a few example (Toledo and Burlingame 2006; Wahlqvist
global crops (Khoury et al. 2014). and Specht 1998).

Global malnutrition
ǢǭǜǫǣɻGlobal malnutrition

At the time of going to press the global figure of the number of people undernourished globally was estimated at 795 million (SOFI 2015) http://www.fao.org/3/a-i4646e.pdf

98 Connecting Global Priorities: Biodiversity and Human Health

In view of these trends, monitoring and ensuring level, and strive for “year-round, nation-wide
biological diversity in global food systems for mean values”, with all compositional differences
nutrition and other outcomes is increasingly related to agro-ecological zone, seasonality and,
important and intimately tied to the underlying most significantly, biodiversity being obscured.
objectives of the post-2015 Development Agenda This has been the lamentable trend, despite
(see also Section 11 in this chapter as well as Part knowledge among food composition professionals
III chapters in this volume). that nutrient content differences among varieties
of the same species can be greater than the
This chapter provides an overview of our differences between species.
knowledge on food composition and the diversity
of food production systems. It also examines The scientific literature reports significant
the contribution of wild foods and traditional intraspecific differences in the nutrient content
food systems and cultures to dietary diversity of most plant-source foods (FAO/INFOODS,
and nutrition as well as the rising trend known 2013a). Significant nutrient content differences
as nutrition transition and Noncommunicable in meat and milk among different breeds of the
diseases (NCDs). The chapter will further discuss same animal species have also been documented
examples of initiatives for biodiversity and (Medhammar et al. 2012; Barnes et al. 2012;
nutrition, including in the context of urbanization. Hoffmann and Baumung 2013). The differences
Finally, relevant global policy initiatives and future are statistically significant, and more importantly,
directions relevant to the post-2015 Development nutritionally significant, with 1000 and more-
Agenda are explored. fold differences documented. For example,
consumption of 200 g of rice per day can
represent less than 25% or more than 65% of
2. Biodiversity and food
the recommended daily intake (RDI) of protein,
composition depending on the variety consumed (Kennedy
Food composition, i.e. the analysis of nutrients and Burlingame 2003). One apricot variety can
and other bioactive components in food, was provide less than 1% or more than 200% of the
traditionally the domain of the agriculture RDI for vitamin A. Variety-specific differences
sector, with FAO taking an early leadership role can represent the difference between nutrient
as early as the 1950s, and the US Department of deficiencies and nutrient adequacy in populations
Agriculture developing the single largest national and individuals (Lutaladio et al. 2010).
food composition database. In recent decades,
the health and nutrition sectors have become the Many countries, such as Bangladesh with its
main users of food composition data in studies diversity of inland water bodies and ecosystems,
exploring the relationship between nutrient or are rich in fish biodiversity (see Box 2 of the
dietary intake and diseases. agricultural biodiversity chapter). Freshwater
aquaculture is also rapidly growing with many
Given the inherent difficulties in collecting households now having access to a pond. Fish,
information about people’s diets, many national especially small indigenous species, are an
dietary surveys have recorded food intake at irreplaceable rich source of food in the diets of
a very aggregated level, sometimes using the millions. They contain essential, highly bioavailable
common name of the species (e.g. spinach) without nutrients, including high-quality protein, essential
specifying genetic variety, sometimes as a food fatty acids and micronutrients. Some, such as
type without specifying species (e.g. leafy greens), hilsa (Tenualosa ilisha), have a high fat content
and sometimes simply as a broad category with no and high levels of polyunsaturated fatty acids.
indication of the food itself (e.g. vegetable). Common small indigenous species such as mola
(Amblypharyngodon mola), chanda (Parambassis
The goal of food composition to date has been baculis), dhela (Rohtee cotio) and darkina (Esomus
to provide nutrient data at that same aggregate danricus) also have a high content of vitamin

Connecting Global Priorities: Biodiversity and Human Health 99

 A as the eyes and gut are consumed. Because al. 2003a, 2003b, 2003c, 2006, 2008, 2009;
many small indigenous species are eaten whole, Kuhnlein et al. 2009, 2013; Burlingame and
including bones and head, they can also represent Toledo 2006; Rubiang-Yalambing et al. 2014).
a very rich source of highly bioavailable calcium, As more and better data become available, food
along with high iron and zinc content. The edible biodiversity, covering thousands of varieties of
parts of larger cultured fish such as silver carp fruits, vegetables, grains and legumes, animal
(Hypophthalmichthys molitrix), tilapia (Oreochromis species and breeds, edible insects and fungi, is
niloticus) and panga (Pterogymnus laniarius) do not being recognized for its high nutritional value
contain vitamin A, iron or zinc, and as the bones and great potential for improving the nutritional
of large fish are discarded as plate waste, they do status of local communities. Furthermore, many
not contribute to calcium intake (Thilsted 2013). varieties of aibika (Abelmoschus manihot L.)
are consumed in the Pacific region as a common
Several studies illustrate well the importance leafy vegetable particularly in Papua New Guinea
of understanding the nutrient composition of (PNG) where a recent study (Rubiang-Yalumbing
biodiversity. For example, in the latter part of et al. 2014) has highlighted its high nutritional
the twentieth century, vitamin A deficiency was value and potential for improving the nutritional
identified as a serious public health problem status of local communities. This study has
among many Pacific Island nations, with over 50% also highlighted genotype and environment
of children manifesting stunting, night blindness, interactions that significantly influence the
Bitot spots, xerophthalmia causing blindness, micronutrient concentrations of even the same
and severe repeated respiratory infections (see accessions from year to year, even when planted
Box 6 ). Despite the fact that this was attributed in the same area.
to decreased consumption of traditional, local
vitamin A-rich foods, interventions promoted The selective specialization in a smaller number
since the 1980s were fortification of margarine and of crops and crop genotypes has made some crops
distribution of vitamin A capsules (Schaumberg et less resilient to diseases and has limited the range
al. 1995). Food composition research in the Pacific of available nutrients. Decades of research shows
later revealed that local varieties of familiar species that while yields of staple crops such as maize,
were often superior in their nutrient content to wheat and rice are increasing, their nutritional
the commonly consumed varieties that dominated contents tend to be decreasing (Jarrell and Beverly
the marketplace (Englberger and Johnson 2013, 1981; Simmonds, 1995). Moreover, as highlighted
Table 1). in the chapters on agricultural biodiversity and
climate change in this volume, climate change may
In a study by Huang and co-workers (1999), the significantly influence biodiversity resources, food
nutrient content of different variety of sweet production and food contamination, including the
potato was analysed, showing dramatic variety- incidence of aflatoxins, with implications for food
specific differences, with high-carotenoid varieties security, diets and nutrition (Cotty and Jaime-
containing 65 times more β-carotene than the low- Garcia 2007; Tirado et al. 2013). Climate change
carotenoid varieties. The pro-vitamin A carotenoid is also expected to cause significant reductions
content of some local banana varieties was more in the nutritional content of certain foods,
than 8000 μg per 100 g, compared to the common particularly C3 grains and legumes, which provide
Cavendish variety with about 25 micrograms per a large portion of the global population with their
100 grams (Englberger et al. 2003a, b). After primary source of iron and zinc. Increasing CO2
the publication of data on the nutrient richness concentrations may lead to reductions ranging
of local foods in Pacific Island countries (see between 5% and 10% in the iron and zinc content
Table 1), it was clear that agricultural biodiversity of the edible portion of these crops (Myers et al.
could provide more sustainable and culturally 2014).
acceptable solutions to several of the problems
of malnutrition in the region (Englberger et

100 Connecting Global Priorities: Biodiversity and Human Health

 Table 1: Carotenoid content of selected traditional staple food varieties compared to rice (μg/100 g edible portion) in Pohnpei, FSM

β-carotene Total
Variety Species Flesh colourƸ β-carotene α-carotene β-crypto-xanthin equivalentsƹ REƺ RAEƻ carotenoidsƼ
Banana
Utin Iap Musa spp Orange: 15 8508 na na 8508 1418 709 na
Karat Musa spp ellow/orange: 8 2230 455 30 2473 412 206 4320
Giant swamp taro
Mwahng Tekatek Cyrtosperma ellow: 1 4486 na na 4486 748 374 na
Weitahta merkusii
Mwahngin Wel Cyrtosperma ellow: 4 2930 2040 120 4010 668 334 5630
merkusii
Breadfruit
Mei Kole Artocarpus ellow 868 142 939 132 78 na
mariannensis
Pandanus
Luarmwe Pandanus tectorius ellow 310 50 20 345 58 29 5200
Imported food
Rice, white or Oryza sativa White na na na 0 0 0 0
brown

na- not analysed * below detection limits

Notes: Analyses were conducted at di erent laboratories, see published papers. All used state-of-the art techniques, including high performance liquid chromatography (HPLC). Samples were as eaten: raw
ripe (banana, pandanus); cooked ripe (breadfruit) and cooked as mature (taro). All samples were composite samples: 3–6 fruits or corms per sample, collected from Pohnpei State, Federated States of Micro-
nesia. Data are from: Englberger et al. 2009a (pandanus), Englberger et al. 2008 (giant swamp taro), Englberger et al. 2006 (banana), Englberger et al. 2003a (breadfruit). Imported food: rice: Dignan et al.
2004. Imported rice has now become a common staple food in Pohnpei.
Raw esh color was described visually and estimated using the DSM olk Color Fan, numbers ranging from 1 to 15 for increasing coloration of yellow and orange.
β-carotene equivalents: content of β-carotene plus half of α-carotene and β-cryptoxanthin.
Retinol equivalents (conversion factor 6:1 from β-carotene equivalents to RE).
The estimated recommended dietary intake (RDI) for a non-pregnant, non-lactating female is 500 μg RE/day and for a child 1–3 years old is 400 μg/day (FAO/WHO 2002).
Retinol activity equivalents (conversion factor 12:1 from β-carotene equivalents to RAE)
This includes estimates of identi ed and unidenti ed carotenoids level but is unrelated to vitamin A content.
Source: Englberger and ohnson, 2013

Connecting Global Priorities: Biodiversity and Human Health 101

 Food composition and food consumption 3. Systems diversity and human
indicators for biodiversity (see Box 1) can help nutrition
track the extent to which food biodiversity is being
documented for the purposes of human nutrition. A shared axiom of ecology and nutrition is that
While progress is being made in this area and diversity enhances the health and function of
more data on the nutrient composition of food complex biological systems (DeClerck et al. 2011;
biodiversity are required, enough evidence exists DeClerck 2013; Khoury 2014).
to warrant actions to provide biodiversity-based
solutions to solve some of the persistent problems A diverse diet should contain many different foods
of malnutrition (Burlingame et al. 2009). consumed in sufficient amounts. A healthy human
diet is composed of many hundreds of beneficial
bioactive components, a small subset of which have
been characterized and identified as nutrients. A
varied diet is the only way to ensure adequate

Box 1. Food composition and food consumption indicators for biodiversity

Speci c indicators for biodiversity are needed to understand, quantify, and monitor the role of
biodiversity in human diets, and the impact of biodiversity-related nutrition interventions and
initiatives. Among relevant activities under the Cross-cutting Initiative and within the framework of
the Biodiversity Indicator Partnership, FAO, INFOODS and Bioversity International convened a series of
meetings and expert consultations to propose, develop and monitor nutrition indicators for biodiversity.

During two technical meetings, two nutrition indicators were developed: Indicator 1 on food
composition (FAO, 2008) and Indicator 2 on food consumption (FAO 2010).

Indicator 1 relates to the availability of compositional data, i.e. nutrients, bioactive non-nutrients, and
contaminants, on foods meeting the criteria of biodiversity. The criteria include food items reported
at the taxonomic level below the species level, along with wild, neglected and underutilized species.
In 2008, the baseline report counted 5519 foods for Indicator 1. In subsequent years, between 835
and 5186 foods were added annually (FAO/INFOODS 2013). Researchers worldwide are submitting
their data to the FAO/INFOODS Food Composition Database for Biodiversity (FAO/INFOODS 2013a),
which serves as an international repository of analytical data on biodiversity of su cient quality.
These data are freely available, widely disseminated, and frequently cited.

Indicator 2 refers to a count of the number of biodiverse foods reported in food consumption or
similar surveys (FAO 2010). In 2009, the baseline report counted 3,119 foods. In the two reporting
periods that followed, 1,827 and 1,375 foods were added. A secondary survey indicator was
developed as a count of the number of food consumption and similar surveys taking biodiversity into
consideration in their design and/or reporting, with at least one reported food meeting the criteria for
Indicator 2 (FAO/INFOODS 2013).

These indicators have proven useful in stimulating the collection and dissemination of biodiversity
data for food composition and consumption. They are also advocacy tools to policy-makers and
programme managers for e ectively raising awareness of the importance of biodiversity for nutrition
and providing documentation of the ever-increasing knowledge of biodiversity and human nutrition.

Reference: http://www.fao.org/infoods/infoods/food-biodiversity/it/ (accessed 5 March 2015)

102 Connecting Global Priorities: Biodiversity and Human Health

intakes of these nutrients and related compounds. Though ecologists have focused increasingly on the
Researchers use different methods to determine relationship between biodiversity and ecosystem
the adequacy of diets of individuals, households functioning, there has been little but increasing
and communities, including the simple and easy focus on the capacity or role that ecosystems
to administer Diet Diversity Score (DDS), which is play in providing the essential elements and
defined as the number of food groups consumed nutrients of the human diet, as proposed through
by an individual or family over a certain time the concept of “eco-nutrition” (Deckelbaum
period, mostly 24-hours. Many studies carried out et al. 2006; DeClerck et al. 2011). While diet
among different age groups show that an increase diversity has long been recognized as important
in individual DDS is related to increased nutrient for adequate nutrient intake and human health,
adequacy, health and micronutrient density of the concept of nutritional diversity has yet to
diets of non-breastfed children, adolescents and be integrated into planning, assessments, and
adults (Hatloy et al. 1998; Ruel et al. 2004; Steyn policies and programmes of agricultural and food
et al. 2006; Kennedy et al. 2007; Mirmiran et al. systems.
2004; Foote et al. 2004; Lobstein et al. 2015 and
references therein; Arimond and Ruel 2004; Kant In the past, food-based interventions have been
et al. 1993; Slattery et al. 1997; Levi et al. 1998) mostly oriented toward single nutrients (Frison et
and food security (Ruel 2003). al. 2006). This may in part be attributed to a lack
of knowledge in earlier years of the interactions
Similarly, in ecology, species diversity has been among nutrients in human physiology and
shown to stimulate productivity, stability, metabolism. From various recommendations
ecosystem services, and resilience in natural for high-protein diets (Brock et al. 1955) and
(Cadotte et al. 2012; Gamfeldt et al. 2013; Hooper later for high-carbohydrate diets (McLaren 1966;
et al. 2005; Zhang et al. 2013; Hooper et al. 2012) McLaren 1974) to more recent efforts directed at
and agricultural ecosystems (Kremen and Miles the elimination of micronutrient deficiencies (UN
2012; Davis et al. 2012; Kirwan et al. 2007; Picasso committee on nutrition, 2000; Ruel and Levin
et al. 2008; Bonin and Tracy 2012; Mijatovic et al. 2002), the attention has generally concentrated
2013; Hajjar et al. 2008). on single nutrient approaches. The introduction
of crops focusing on single-nutrients serves as
Community ecology has demonstrated that an important means to address specific nutrients
increases in biodiversity can lead to increases (macro or micronutrients), but caution must be
in plant community productivity when species exercised as any single crop, including a fruit
complement each other, or use resources or vegetable crop, does not assure the complex
differently. Many studies of biodiversity and nutritional requirements needed to ensure good
ecosystem function have demonstrated that health (Graham et al. 2007, DeClerck et al. 2011).
there is much variance that cannot be explained
by species richness (DeClerck et al. 2011). For Deeper, less obvious, interactions and relationships
example, does it matter that an ecosystem has which affect nutritional outcomes and have long
five species, or would it be more important that a been important in traditional food cultures are
system has five different functional groups? Is a at play. The nutritional complementarity of the
field with maize, rice, wheat, sorghum, and millet traditional “American three-sisters” polycultural
the equivalent of a field with maize, beans, squash, system, which involves planting maize, beans and
sweet potato and guava? Both have five species, squash in the same hole, is a combination that is
but the latter contains five functional distinct almost nutritionally complete, with carbohydrates
species from a nutritional point of view in contrast and energy provided by maize, protein by beans
to the former where all of the species are from the and vitamin A by squash (DeClerck and Negreros-
grass family, high in carbohydrates, but poor in Castillo 2000; DeClerck 2013). Mayan farmers
essential nutrients. when eating meals comprising these plants do so
with condiments prepared with lime juice, which is

Connecting Global Priorities: Biodiversity and Human Health 103

 very important in making the niacin present in the and key nutrition health outcomes. Thereby these
beans bioavailable. So much so in fact, that when studies offer a potential intermediate indicator in
maize was introduced outside of Latin America the biodiversity–nutrition nexus that environment,
without the accompaniment of beans or lime, agriculture and nutrition strategies can consider
these dietary interactions were lost leading to and monitor towards using a systems approach,
negative nutritional outcomes including pellagra not replacing but complementing dietary diversity
(DeClerck 2013). Dietary interactions such as indicators and agrobiodiversity indicators.
these are often overlooked but play a major role
in improving the bioavailability of certain minerals Diversity in production and food systems can
(see Box 2). impact nutrition not only through the diversity of
nutrients made available for human consumption
A recent methodology applies ecological diversity but also through other aspects of the production
to nutritional traits, resulting in a metric coined and food system that influence nutrition-related
nutritional functional diversity or Nut FD outcomes more indirectly. Crop plants that
(Figure 1; DeClerck et al. 2011; Remans et al. depend on pollinators are key sources of vitamin
2011). Household, landscape and national-level A, C and folic acid, and on-going pollinator decline
assessments (DeClerck et al. 2011; Remans et may exacerbate current challenges of accessing
al. 2011; Jones et al. 2014; Remans et al. 2014) a nutritionally adequate diet (Box 3; see also
illustrate the importance of such diversity in local sub-section on pollination in the agricultural
and national food systems for dietary diversity biodiversity chapter). Species diversity has

%R[,QFUHDVLQJVPDOOƩVKLQWDNHLQSUHJQDQWDQGQXUVLQJZRPHQLQUXUDO%DQJODGHVK

In Bangladesh, a sh chutney was developed to increase the contribution of essential nutrients

from an animal-source food in the rst 1000 days of life, to supplement the diet of pregnant and
breastfeeding poor, rural women in Bangladesh, and promote growth and development in infants
and young children. The chutney is based on a traditional “achar” or pickle recipe which is commonly
served with boiled rice and curry vegetables. The chutney contains 37% dried small sh, 15% oil,
37% onion, 7% garlic and 4% chili. The recommended serving is one heaped tablespoon of sh
chutney (equal to 30 g containing 60 g of raw sh), to be eaten with the main meal. The sh chutney
is well-liked by women and is a good source of micronutrients such as iron, calcium, zinc and vitamin
B12, as well as animal protein and essential fatty acids. The particular relevance of the latter for
cognition in the rst 1000 days is especially important. In addition, the sh itself enhances the
bioavailability of minerals from the plant-source foods (rice and vegetables) in the meal.

The sh chutney, produced by a women s group, is presently being distributed to 150 pregnant and
lactating rural women in Sunamganj, north-eastern Bangladesh, through a project aimed at improving
the livelihoods of poor rural households. The small sh used is sourced from the wetlands and sun-
dried by local women. Assistance, training and supervision have been provided to ensure safe and
hygienic conditions for processing, storage and transportation. Women receiving the sh chutney
report producing “a lot of milk” and their children “getting more milk, being satis ed and growing
well”. Partners have shown interest in using the product in national food programmes, emergency
response food rations, school feeding programmes and for sale in local and urban outlets.

This project demonstrates that food processing is important for highly perishable products such as
sh, fruit or vegetables. They may increase food safety, market opportunities, the geographical and
temporal usage, as well as the livelihood of small-scale producers.

104 Connecting Global Priorities: Biodiversity and Human Health

been shown to stimulate productivity, stability, is about setting nutritional, environmental and
ecosystem services, and resilience in natural and agricultural targets together, and identifying
in agricultural ecosystems (Cadotte et al. 2012; mechanisms to achieve these using a systems
Gamfeldt et al. 2013; Zhang et al. 2012; Kremen approach. The overall objective is to create
and Miles 2012; Khoury et al. 2014). In general, synergies and minimize trade-offs between
increasing the number of species in a community reducing malnutrition of vulnerable populations
or system will enhance the number of functions and restoring and employing ecosystem services.
provided by that community, and will reinforce the NSL does not imply that the environment can
stability of provision of those functions (DeClerck produce all the nutrients required for adequate
et al. 2011). human nutrition; it does, however, mean a
focus on building biological diversity into the
By using diversity metrics in agriculture–nutrition landscape, diet, market and food system to provide
strategies, synergies as well as trade-offs with other multiple sources of nutrients, and contribute to
outcomes, e.g. environmental benefits, can be environmental and population resilience. NSL is
evaluated and taken into account. In view of global currently strongly embedded with the farming
national food supplies that have become more systems research of the CGIAR in a diversity
homogeneous in composition (Khoury et al. 2014), of settings, from aquatic agricultural systems,
monitoring and ensuring diversity for nutrition and to humid tropics and forest areas. Across these
other outcomes seems increasingly important. diverse settings, biodiversity and dietary diversity
sit at the nexus of environment, agriculture and
A CGIAR initiative, nutrition-sensitive landscapes nutrition, and serve as the entry point for this
(NSL), applies such systems approaches to landscape-based approach. 
concrete low-income settings. The NSL initiative

ǡǤǢǰǭǠɻSchematic presentation of the nutritional functional diversity metric, based on (1) species
composition in a given farm or landscape and (2) nutritional composition of these species. Thereby the
nutritional FD metric provides a way to assess complementarity between species for their nutritional
function. ǝNutritional functional diversity plotted against species richness for 170 farms in three
Millennium Villages project sites, Sauri in Kenya, Ruhiira in Uganda and Mwandama in Malawi.

ǜɰ ǝɰ

Source: Remans and Smukler 2013

Connecting Global Priorities: Biodiversity and Human Health 105

 “Landscape approaches” have gained prominence networks, and biophysical features such as
in the search for solutions to reconcile multiple watersheds. Households and farming systems in
objectives, particularly in the field of conservation rural areas, especially in low-income settings, are
and development trade-offs (Sayer 2009). often strongly dependent on resources available in
In general, “landscape approaches” seek to the landscape. In the social-institutional domain,
provide tools and concepts for allocating and households and communities continuously
managing land to achieve social, economic, interact with each other and with markets,
and environmental objectives in areas where political and social institutions. These interactions
agriculture, mining, and other productive land have a strong influence on household functioning
uses compete with environmental and biodiversity and food provisioning. Combining multi-objective
goals (Sayer et al. 2013). In NSL, “landscape” modelling and participatory research, NSL
refers, it is referred to the spatial extent that searches for and tests potential synergies between
influences both nutrition and the environment in improving availability, access and demand for
the study areas, including socioeconomic features a diversity of nutritious foods and managing
such as locations of markets and transportation ecosystem services.

Box 3. Pollinator declines, human nutrition and health

Declines in animal pollinators are a subset of biodiversity loss that have been well documented
around the globe (Vanbergen 2013; Burke et al. 2013; Potts et al. 2013). Over the past decade, the
human health implications of these declines have received increasing attention. Pollinators are
estimated to be responsible for roughly one third of human caloric intake (Kleine et al. 2007) as well
as up to 40% of the global nutrient supply (Eilers et al. 2011). Regions where pollinators contribute
most heavily to nutrient production may also be those where human populations are su ering
from the largest burdens of micronutrient de ciency diseases (Chaplin-Kramer et al. 2014). In the
rst published analysis of human vulnerability to pollinator declines based on an evaluation of
population-level dietary patterns, Ellis et al. (2015) found that as much as 56% of a population could
be placed at new risk of vitamin A de ciency as a result of the loss of animal pollinators.

Perhaps even more signi cant in terms of global health is the potential impact of pollinator declines
on the yields of food groups whose intakes, as a whole, have recently been shown to have very large
impacts on the global burden of disease. If pollinators work would need to be done manually by
mankind, additional economic costs would appear for a work less e ciently performed. The recent
assessment of the global burden of disease has emphasized a global pandemic of NCDs including
cardiovascular diseases, diabetes, and diet-related cancers (Lim et al. 2010). Because their intakes
reduce the risk of these diseases, low intakes of fruit, nuts and seeds, and vegetables have been
shown to rank fourth, twelfth, and seventeenth on the list of global risk factors for burden of disease.
ields of each of these food groups are highly pollinator dependent. A recent analysis involving a
member of our authorship group is currently in press at the Lancet and suggests very large global
burdens of disease would result from reduced intake of these food groups as a consequence of
animal pollinator declines. This analysis also emphasizes that large numbers of people around
the world would additionally be placed at risk for folate and vitamin A de ciency, and many who
are already de cient would become more de cient. Thus, animal pollinator declines could lead to
substantial new disease burdens from both micronutrient de ciencies and chronic diseases.

106 Connecting Global Priorities: Biodiversity and Human Health

4. Wild foods and human nutrition Pretty 2010). Xu et al. (2004) reported that 283
different species of edible vegetables were found
3.1 Wild foods and diet diversity in the markets of Xishuangbanna in southwest
China and the trade in wild vegetables contributed
Wild biodiversity has an important role in
between 15% and 84% of market income for
contributing to food production and security in
different groups. This represented between 4% and
many agroecosystems worldwide (Scoones et al.
13% of total household income. Notably, the mean
1992; Johns and Maundu 2006; Termote et al.
price of wild vegetables was 72% higher than that of
2011; Turner et al. 2011; Dogan 2012; Termote
cultivated vegetables. In South Africa, Shackleton
et al. 2012a; Mavengahama et al. 2013; Vinceti et
et al. (1998) found that 25% of households sampled
al. 2013; Powell et al. 2014; Achigan-Dako et al.
in nine villages sold wild vegetables.To investigate
2014; Vira et al. 2015). More than 10 millennia
the importance of wild foods in Europe, Schulp et
after the emergence of settled agriculture, millions
al. (2014) analysed the availability, utilization and
of rural smallholders in most geographical regions
benefits of wild game, wild plants and mushrooms
of the world are still reliant on wild products
in the European Union (EU). They recorded a wide
from foraging forests and wild lands for their
variety of game (38 species), vascular plants (81
subsistence and livelihoods (Wunder et al. 2014),
species) and mushrooms (27 species) collected and
although a recent study of wild product harvesting
consumed throughout the EU.
by 32 indigneous communities in the Ecuadorian
Amazon showed this was declining (Gray et al. Wild foods include varied forms of both plant
2015). Ickowitz et al. (2014) found a significant and animal products, ranging from fruits, leafy
positive relationship between tree cover and vegetables, woody foliage, bulbs and tubers,
dietary diversity, suggesting that children in Africa cereals and grains, nuts and kernels, saps and
who live in areas with more tree cover have more gums (which are eaten or used to make drinks),
diverse and nutritious diets. In a comparative mushrooms, to invertebrates such as insects and
analysis of environmental income data collected snails, honey, bird eggs, bushmeat from small and
from some 8000 households in 24 developing large vertebrates, reptiles, birds, fish and shellfish
countries, Angelsen et al. (2014) highlighted that (Bharucha and Pretty 2010; Shackleton et al.
environmental income accounts for 28% of total 2010). These various wild foods invariably add
household income, with 77% coming from natural diversity to the diets of people and communities
forests. Food products (wild fruit and vegetables, who make extensive use of them.¹ These examples
fish, bushmeat, mushrooms) were the second also reflect broad groups and not the dozens of
most important category (over 30%) and likely to species included within each wild food type.²
help meet the nutritional, medicinal, utilitarian Abu-Basutu (2013) reported that the species
and ritual needs of many households. “commonly” used across two villages in southeast
South Africa included 17 mammal, 14 bird, 6
A recent survey summarizing information from
fish, 10 leafy vegetables and 7 fruits species. In
36 studies in 22 countries highlights that wild
comparison, Ocho et al. (2012) reported that 120
biodiversity still plays an important role in local
wild plant species were listed as foods by residents
contexts with around 90–100 wild species per
of a single village in southern Ethiopia, with an
location and community group. Based on some
average of 20 species per household.
estimates, the use of wild food reached up to
300–800 species, although actual consumption
and dietary intakes were not studied (Bharucha and

¹ In another example, across a sample of 14 rural villages in South Africa, on average, 96% of households
consumed wild spinach, 88% ate wild fruits, 54% ate edible insects, 52% consumed bushmeat and 51% ate
honey (Shackleton and Shackleton 2004).
² For example, more than 100 different plant species are consumed as wild vegetables in South Africa overall
(Dweba and Mearns 2011). In northeast South Africa, 45 leafy vegetables and 54 fruits were recorded in a
household survey across nine villages (Shackleton et al. 1998, 2000).

Connecting Global Priorities: Biodiversity and Human Health 107

 However, caution is needed when analysing the supplied by wild foods relative to grown or bought
extent to which wild biodiversity is available foods remains largely unknown. It is likely to be
and that actually consumed and contributing to significant, however, as many wild food species
dietary diversity. In some instances, wild foods are much richer in vitamins, micronutrients or
can constitute a large portion of the diet while in proteins than many conventional domesticated
others, actual consumption is limited (Powell et species that dominate agricultural or home-garden
al. 2015). In Benin, for example, the contribution production (Yang and Keding 2009; Bharucha
of wild edible plants to total dietary intake was and Pretty 2010). Kobori and Rodriguez-Amaya
relatively low (Boedecker et al. 2014). More (2008) showed the higher carotenoid levels of wild
research is needed to determine the conditions native Brazilian leafy green vegatables compared
and factors that actually determine the utilization to commercially produced leafy vegetables.
and consumption of wild foods and the reasons Protein levels in edible insects such as mopane
for which consumption among communities in worms (Imbresia belina) are approximately double
some biodiverse regions may be low. The use of those in beef (Greyling and Potgieter 2004). The
wild foods is especially relevant where agricultural same applies to mushrooms, such as Psathyrella
production is primarily centred on one or two atroumbonata, which has 77% more protein than
cereals or tuber-based staples that contribute the beef (Barany et al. 2004). Vitamin C levels in
bulk of daily calorie requirements, but provide baobab fruits (Adansonia digitata) (see Box 4) are
limited micronutrient and dietary diversity. also six times higher than oranges (Fentahun and
Hager 2009); Amaranthus, a widely used green
Wild foods are an essential and preferred dietary leafy vegetable, has 200 times more vitamin A and
component in both rural and urban households ten times more iron than the same-sized portion
in many parts of the world.³ Aberoumand (2009) of cabbage (McGarry and Shackleton 2009b).
reports that approximately one billion people
around the world consume wild foods, but it is likely Importantly, higher values of vitamins and
to be much higher. It is not only rural communities minerals boost immunity against diseases
that make use of and may have preference for wild (Himmelgreen et al. 2009). Golden et al. (2011)
foods. There are many wild foods in large urban reported that bushmeat hunting by households
markets. Examples include wild vegetables in in northeastern Madagascar had a significant
West Africa (Mertz et al. 2001; Weinberg and impact (by approximately 30%) in lowering the
Pichop 2009), Croatia (Luczaj et al. 2013), Turkey incidence of childhood anaemia and this was more
(Dogan 2012), Brazil (Kobori and Rodriguez- pronounced in poorer households than wealthier
Amaya 2008), Lebanon (Batal and Hunter 2007), households. Most development agencies dealing
Morocco (Powell et al. 2014), Italy (Turner et al. with food security accept that there is a strong
2011), and China (Xu et al. 2004), bushmeat in relationship between dietary diversity generally
central Africa (Edderai and Dame 2006; van Vliet and health and nutrition status, founded on
et al. 2012), fish in the Democratic Republic of a number of studies globally (e.g. Ruel 2003;
Congo (de Merode et al. 2004), and mopane worms Arimond and Ruel 2004; Steyn et al. 2006). Thus,
in southern Africa (Greyling and Potgieter 2004). the inclusion of even small amounts of wild
These findings show that the consumption of wild foods add to the diversity of the standard diet in
foods is not driven solely by need or poverty, but many countries, with beneficial effects on health
also by culture, tradition and preference. outcomes.

While the above data and examples show a wide Dealing with the declining intake of grown food
diversity of wild species and food types in diets, the types by increasing the quantity and diversity of
actual proportion of daily nutrient requirements wild foods in the diet is a common strategy in

³ For example, the diets of the Turumbu people in the Democratic Republic of Congo are mainly composed of
cassava, which they grow, but are supplemented on a daily basis with wild foods such as wild leafy vegetables, bush
meat, wild fish, wild mushrooms, caterpillars, ants and honey, depending on the season (Termote et al. 2010).

108 Connecting Global Priorities: Biodiversity and Human Health

some parts of the world. For example, da Costa Wild species often contain essential nutrients, but
et al. (2013) describe how wild foods increase information on the composition and consumption
in prominence in the diet as stores of staple of these foods is limited and fragmented
carbohydrate crops decline (maize, rice and cassava) (Burlingame et al. 2009) or of poor quality
in Timor-Leste. This was regarded as one of the (McBurney et al. 2004). It is therefore difficult to
primary food coping strategies for approximately evaluate the contribution of underutilized wild
two months of the year. More detailed results are foods to dietary adequacy. Knowledge on the
reported by de Merode et al. (2004) for seasonal compositional data of these foods is essential in
uses of crops and wild foods in northeastern order to promote, market and expand the use of
Democratic Republic of the Congo. They found underutilized wild foods, for example, in nutrition-
that during the four-month hungry season the related projects, programmes and policies in the
consumption of own agricultural produce declined agricultural and environmental sectors. While
by 46%, while the use of wild foods increased forest foods cannot be a panacea for global issues
markedly, 475% for fish, 200% for wild plants related to food security and nutrition, in some
and 75% for bushmeat. The value of wild foods specific geographic contexts, they can play a
traded in the market also increased during the lean significant role as shown in Box 4.
season, a 365% increase in fish, 233% increase for
wild plants and 155% increase for bushmeat trade.
The storing of wild foods has been observed for
both plant-and animal-based foods.⁴

Box 4: Indigenous fruit trees: the African baobab

Forests and their non-timber forest products (NTFPs), either through direct or indirect provisioning for
human nutrition, can contribute to food security, particularly in developing countries. The potential
of indigenous food, is mostly derived from wild and underutilized cultivated species, has largely
remained untapped due to scant information on the nutritive and economic value of these foods.
For example, combining di erent indigenous fruit tree species in agroforestry systems based on the
seasonal calendar of fruit availability could result in a year-round supply of key nutrients (Vinceti
et al. 2013; amnadass et al. 2013; Kehlenbeck et al. 2013a, b; amnadass et al. 2011). A study by
Kehlenbeck et al. (2013a) in sub-Saharan Africa shows that consuming 40–100 g of berries from
Grewia tenax (Forrsk.) Fiori could supply almost 100% of the daily iron requirements for a child
under 8 years of age. In addition to micronutrients, the high sugar content of fruits such as tamarind
(Tamarindus indica L) and baobab (Adansonia digitata L) make them important sources of energy. The
fruits of Dacryodes edulis (G. Don) H. . Lam, and the seeds of Irvingia gabonensis (Aubrey-Lecomte ex
O Rorke) Baill., Sclerocarya caƱra Sond. and Ricinodendron rautanenii Schinz have a higher fat content
than peanuts (Vinceti et al. 2013; ohnson et al. 2013).

The occurrence and distribution of the African baobab (Adansonia digitata) in drier habitats of Africa,
commonly found in savanna, scrubland and semi-desert, has great potential to support communities
in more vulnerable dryland ecosystems and in the face of climate variability. The baobab is a
majestic tree in the landscape but it is not only its physical presence that exhibits diversity within

⁴ For example, Shackleton et al. (1998) reported that the majority of households in rural northeast South Africa
dried one or more wild vegetable species and between 20% and 50% dried wild fruits for use in the off season.
The role of traditional knowledge associated with wild foods is also important in helping communities cope
with lean periods as well as supporting the conservation of wild foods (Sujarwo et al. 2014; Pardo-de-Santayana
and Macia 2015).

Connecting Global Priorities: Biodiversity and Human Health 109

 and between its trees but also the high nutritional value of its fruits. The most important food from
baobab is the fruit pulp, which is rich in vitamins and minerals. It can provide far higher amounts of
vitamin C, calcium and iron than more common tropical fruits such as mango and orange (Kehlenbeck
et al. 2013a). However, there is a large variability in the levels of vitamin C in fruits of di erent
individual baobab trees – from 126 to 509 mg per 100 g edible portion (Stadlmayr et al. 2013) – but
even the lowest gure identi ed is far higher than in many other fruits. In addition to the fruit pulp,
baobab also produces leaves that are used as nutritious vegetables and edible seeds, from which oil
for consumption and cosmetic purposes are produced (Caluwe et al. 2010).

The potential of baobab for nutrition and income generation is a good example of a new product with
high potential in European market, given the acceptance of baobab as a novel food in 2008. Due to
its high nutrition potential and demand in consumer markets, research is ongoing in East Africa by the
World Agroforestry Centre (ICRAF) to identify populations of baobab, distribution across landscapes,
variation in genetic and morphological characteristics, and the diversity of nutritional content within
and between wild populations. Information on nutrient content may facilitate the selection of priority
fruit tree species for domestication programmes aiming at improving food and nutrition security and
for income generation.

While baobab is one example, there are hundreds of other wild food trees in Africa with similar
importance for food and nutrition security. Developing and disseminating nutrient-sensitive
processing techniques for indigenous fruits can further contribute to rural livelihoods through
diversi cation of income-generating activities and by extending the shelf-life and availability of tree-
based food products for consumption during o -seasons. Markets need to be developed for these
new products, and processors linked to domestic and international markets to further improve value
chain opportunities. However, the abundance of indigenous fruit trees is said to be decreasing in
many parts of sub-Saharan Africa due to changes in ecosystem equilibrium and loss of biodiversity
as a result of changes in land use, increasing urbanization and climatic shocks, among others. All of
these result in shifts in species distribution, altered pest and disease occurrences, and possibly a
lack of pollinators (see Box 3) for su cient fruit tree diversity and occurrence. Domestication and
increased cultivation of the most important indigenous fruit tree species may help to both conserve
biodiversity and provide rural communities with better livelihood options.

3.2 Sustainable harvest and (Vinceti et al. 2013). A study from Madagascar
consumption of wild foods estimated that the loss of bushmeat from the
diet of children, without substitution by other
Wildlife resources such as bushmeat or wild meat
sources, would result in a 29% increase in children
(here encompassing non-domesticated terrestrial
suffering from iron deficiency anaemia (Golden
mammals, birds, reptiles and amphibians
et al. 2011). It must nonetheless be noted that
harvested in the wild for food) constitute the main
various activities associated with the handling of
source of animal protein in many tropical forested
bushmeat, its consumption and (illegal) trade also
landscapes (Kothari et al. 2015), though the
involve varying levels of health risks for disease
availability of bushmeat resources around urban
emergence (Wolfe et al. 2005). In particular , these
centres may decline substantially, corresponding
include activities associated with unsafe hunting,
with a prevalence in child stunting (Fa et al.
butchering and transport of some species,
2015). Bushmeat also supplies many important
especially primates (see also chapter on infectious
micronutrients in much higher amounts or with
diseases). Moreover, the over exploitation of
higher bioavailability than plant source foods
certain wild animal populations is leading to the

110 Connecting Global Priorities: Biodiversity and Human Health

depletion of some species (Nasi et al. 2011) and food that was not normally, or rarely, part of the
constitutes a rising concern for conservation diet. For example, a household may normally
(Kothari et al. 2015). The resulting mass declines rarely eat bushmeat or wild caught fish, but in the
in wildlife, documented by Nasi et al. (2008), is aftermath of a shock may use it as their primary,
threatening the food security and livelihoods or only, source of meat until they have recovered.
of some forest communities (Heywood 2013), Thirdly, households may collect wild foods and sell
especially where home subsistence consumption them on local or nearby urban markets. The cash
is more common than the trade in bushmeat. earned is then used to help in relieving the impact
Interestingly, a study in Liberia, West Africa of the shock.
has found that regions with access to affordable
fish protein had higher chimpanzee population While many national or regional food security
densities (Junker et al. 2015) and highlights the indices or models focus on the net yields of key
importance of integrated approaches to better crops and average those across population demand
inform conservation actions. Wild foods such as or calorie needs, these overlook the potentially
edible insects also contribute nutritional value to high variability in the timing of food availability
the diet of people in certain regions (van Huis et from crops. The colloquially labelled “hungry
al. 2013). season” or the “lean season”, when food stores from
the previous cropping season begin to dwindle,
Over exploitation or over harvesting is also an and the new season’s crops have not matured is
area of concern for wild edible and medicinal plant typified by declining calorific intake and a low
species (see chapter on traditional medicine within diversity of grown foods in the diet. During the
this volume), and measures to avert this have been same period, food prices are high because stocks
integrated into tools such as FairWild Standard, from the previous cropping cycle have diminished.
most often used for medicinal plants, the This combination can result in clear patterns of
development of species management plans, plant seasonal nutritional status or malnutrition,
conservation areas, genetic reserves, community exemplified by Devereux and Longhurst (2010)
agreements, common property agreements, and for malnutrition in northern Ghana. This period
so forth (Kothari et al. 2015; Dulloo et al. 2014; may also be a time of peak labour demand for the
Hunter and Heywood 2011; Heywood and Dulloo preparation, planting, weeding and tending of the
2005). new crops. Tetens et al. (2003) recorded a 17%
drop in mean energy intake by adults between
3.3 Wild foods as a coping strategy the peak season and the lean season in rural
Bangladesh. Such seasonal patterns may also be
Use of wild edible plants and animals (wild foods) evident in urban populations because of food price
is a key coping strategy for many rural households, increases during the lean season (Becquey et al.
including in response to shocks, such as crop 2012). Seasonal nutritional or energy shortfalls
failure, drought (or other natural disasters), loss of can also exacerbate existing health issues such as
cash income, illness or death of the breadwinner. HIV/AIDS (Akrofi et al. 2012).
This coping strategy can be mobilized by one
or more of three strategies (Shackleton and There is ample evidence of wild foods being used
Shackleton 2004). The first is for households to as coping mechanisms in the face of a household
increase the direct consumption of wild foods that shock. Challe and Price (2009) showed how
are already part of their regular diet. For example, there was a major shift in primary livelihood
a household that normally consumes wild leafy strategies of HIV/AIDS-afflicted households
vegetables 2–3 times per week may increase their in southern Tanzania, from a largely agrarian
consumption to 5–6 times per week when faced livelihood (90% of non-affected households; 3%
with a shock that renders them unable to procure of afflicted households) to a gathering one (0% of
the usual purchased or grown foods. The second non-affected households; 68% of affected ones).
mechanism is to take up consumption of a wild This is typically interpreted as a result of the loss

Connecting Global Priorities: Biodiversity and Human Health 111

 of labour for agriculture to grow food (Drimie security until conditions improve (Mojeremane
2003; Yamano and Jayne 2004). The number and Tshwenyane 2004).
of weekly trips to collect wild edible orchids (to
supplement their diets or as cash income) also
5. Biodiversity and traditional
doubled in HIV/AIDS-affected households relative
to unaffected ones. McGarry and Shackleton food systems
(2009a, b) recorded the use of wild animal foods Indigenous peoples’ food systems and cultures are
by children in households with high HIV/AIDS good examples of the complexity and remarkable
proxy measures relative to households with low, diversity of food availability and utilization. They
or no, proxy measures. Hunting of wild animals, additionally represent important repositories
birds and insects was significantly higher in of knowledge from long-evolved cultures and
affected households. In a two-week monitoring patterns of living with local ecosystems (Kuhnlein
period, the consumption of wild mammals was et al. 2009). For centuries, communities of
three times higher, wild birds two times higher, Indigenous peoples have been the custodians
reptiles almost double and insects four times of the vast majority of the planet’s food and
higher. Species consumed over the two-week genetic resources, and stewards of the diverse
period include two red data species. Over 40% ecosystems and cultures that have shaped these
of households also sold some of the wild catch to resources. Indigenous peoples’ food systems and
supplement income. cultures have often provided for healthy and
resilient diets, which have had minimal impact
Hunter et al. (2007) provided qualitative evidence on the environment prior to colonization and
on how surviving members of a household, development, and for many generations have
following an HIV/AIDS death of an adult, turned ensured food security and nutrition. These food
to procuring a larger proportion of their diets systems have not developed in a vacuum and are
from wild foods. Surviving members stressed the strongly influenced by the forces of globalization
difficulties of food shortages, including reports and development (Kuhnlein et al. 2013). The
that “locusts are now our beef”. The findings also traditional foods they provide are also under
confirmed that food shortages increased as a threat from the impacts of climate change (Lynn
consequence of severe household shocks, and that et al. 2013).
household food security generally decreased after
the mortality of an adult, with increased reliance Indigenous peoples are often the most
on wild foods. Wild foods may also be a coping disenfranchised, marginalized and poorest
response to other types of household shocks. For members of wider society, and they are targeted
example, the ethnobotanical literature is replete by most governments for health improvement
with references to famine foods, namely, those and development. Such development often leads
wild foods that were traditionally used in times to dietary change, including increased reliance
of drought and crop failure. While dependence on “market foods”, which are more often than
on these may have declined to some extent with not highly processed and contribute to increased
modern national-scale responses, this reliance risk of chronic disease, including obesity and
persists in some cases. For example, Ocho et al. diabetes. This reduced reliance on traditional
(2012) list 120 different wild plant species used foods has also led to an erosion of traditional food
by people in Konso in southern Ethiopia, of resources and associated indigenous knowledge.
which 25 were generally used in times of food With obvious outcomes for food security, this has
shortages. Similarly, the Yanomani Indians in significantly affected the welfare, vulnerability and
Venezuela regularly use 20 wild plant species in marginalization of indigenous communities. This
their diets but consume an additional 20 species could be moderated with increased attention to
during food shortages (Fentahun and Hager the principles of diet and health already contained
2009). In Botswana, when there is crop failure within the culture, and with the recognition of the
due to drought, wild fruits also contribute to food nutrient properties of traditional food resources,

112 Connecting Global Priorities: Biodiversity and Human Health

and how these foods can be used to best advantage of the world’s top ten countries where obesity is
for health promotion (Egeland and Harrison now a problem are in the Pacific region (Ministry
2013). of Health 2012).

Indigenous and local communities have created A study led by the Centre for indigenous peoples’
an enduring relationship with the landscape and Nutrition and Environment covering 12 indigenous
its complement of flora and fauna (Turner et communities in different global regions confirmed
al. 2013).⁵ Regardless of geographical location, the diversity and complexity of indigenous
indigenous peoples suffer higher rates of health peoples’ food systems and diets (Kuhnlein et al.
disparities and lower life expectancy compared 2009).⁶ Strengthening and leveraging these food
with non-indigenous peoples (Egeland and systems is a strategy that should be considered to
Harrison 2013). Poor diet is a significant improve diets and reverse negative food-related
contributor to premature death among Indigenous health outcomes. This includes interventions that
Australians and is considered a significant risk aim to identify nutritionally rich traditional foods
factor for cardiovascular disease, type 2 diabetes, and to promote, mobilize and deliver these foods
renal disease and cancer. A study into the burden of to target populations. Not only do these food-
disease in Indigenous Australians (Vos et al. 2007) based approaches potentially improve nutrition
attributed 11.4% of the total burden of disease and health in a sustainable manner, they also help
in the indigenous population to high body mass revive traditional knowledge, biocultural heritage
and 3.5% to low fruit and vegetable consumption. and contribute to the conservation of biodiversity.
In 2012–13, 66% of indigenous Australians
over the age of 15 years were overweight or A corollary to this is the almost ubiquitous decline
obese, 42% were eating the recommended daily in intergenerational transmission of local cultural
intake of fruit (2 serves) and 5% were eating the values, beliefs, institutions, knowledge, practices
recommended daily intake of vegetables (5–6 and language regarding local biodiversity, and the
serves) (Australian Bureau of Statistics 2014). foods and food systems it underpins.
In New Zealand, statistics consistently show
Māori as being over-represented in key health Despite significant animal and plant biodiversity, it
areas such as cardiovascular disease, cancer and cannot always be assumed that a biodiversity-rich
diabetes, with much of this attributed to lifestyle environment or landscape necessarily contributes
and dietary choices. New Zealand’s latest nutrition to better diet or enhanced nutrition of individuals
survey (2011) highlights that the country’s obesity living in close proximity (Termote et al. 2012b).
epidemic has increased dramatically over the past Linking biodiversity assessments with quantitative
decade or so. This survey found that among Māori, dietary assessments in biodiverse environments
over 40% of men were obese while 48% of Māori should promote more ethnobiological studies to
women were obese. It also found that eight out better understand why some local communities do

⁵ For example, New Zealand, the southernmost landmass of the Pacific region, has a temperate but unpredictable
climate with extremes from sub-tropical in the north to sub-Antarctic in the south. Māori, the indigenous people
of Aotearoa-New Zealand, on settling in New Zealand from the more tropical Pacific islands to the north, had
to adapt their horticultural practices to this new environment and its many limitations. Much of their lifestyle
was based on a subsistence approach, including both cultivated and uncultivated plants, and the seasonal
harvesting of birds and fish. In light of the growing prevalence of obesity and NCD among the Māori, how to
recapture and retain traditional knowledge on traditional food systems is now a high priority for many Māori
communities (Roskruge 2014; McCarthy et al. 2014).
⁶ For example, in Pohnpei, there was major diversity and availability of local species and foods, with 381 food
items being documented including karat, an orange-fleshed local banana variety and pandanus varieties rich in
carotenoids. The Ingano diet revealed the utilization of over 160 types of food, ranging from roots to insects to
palm tree products with milpesos palm, yoco liana, bitter cane and cayamba mushroom found to be a priority
for maintaining local health. The Dalit food system revealed a diet highly reliant on wild plant foods with a
recorded total of 329 plant species or varieties providing food (Kuhnlein 2009).

Connecting Global Priorities: Biodiversity and Human Health 113

 not make more effective use of edible biodiversity be around US$ 30 trillion (Bloom et al. 2011).
(Penafiel et al. 2011). Possible barriers include The complex issues contributing to the alarming
negative perceptions of indigenous wild foods; rise in obesity and equally complex approaches
excessive women’s workloads and distances to reversing the obesity pandemic are dealt with
involved for collection; food preparation times; in detail in The Lancet Obesity 2015 Series (see,
and poor knowledge among local populations for example, Swinburn et al. 2015; Lobstein et al.
about the nutritional value of the indigenous wild 2015 in that issue).
foods in their immediate environment. If we are to
promote more effective biodiversity interventions The nutrition transition is particularly prevalent
it is important to address these barriers by among indigenous peoples, who tend to suffer
generating and maximizing use of quality data on higher rates of health disparities and lower
nutrient composition; increasing awareness of and life expectancy, regardless of geographical
nutritional education on the benefits of edible location (Egeland 2013) and across many other
biodiversity; domesticating priority species and populations in low-and middle-income countries.
facilitating their integration into home gardens; A recent study out of Australia (Australian Bureau
and developing guidelines for improved use of of Statistics 2014) found that compared with the
nutritionally rich foods from local biodiversity, non-indigenous population (and after adjusting
including recipes adapted to modern lifestyles. for age differences), aboriginal and Torres Strait
Islander people were:

6. Biodiversity and the nutrition • more than three times as likely to have diabetes
transition (rate ratio of 3.3);
Globalization, poverty, modern agricultural
practices and changes in dietary patterns have
• twice as likely to have signs of chronic kidney
disease (rate ratio of 2.1);
led to a “nutrition transition”. The nutrition
transition is the process by which development, • nearly twice as likely to have high triglycerides
globalization, poverty and subsequent changes (rate ratio 1.9), more likely to have more than one
in lifestyle have led to excessive dietary energy chronic condition, for example, both diabetes and
intakes, poor-quality diets and low physical kidney disease at the same time (53.1% compared
activity (e.g. Agyei-Mensah and Aikins 2010). with 32.5%).
A shift from traditional foods and healthy diets
towards consumption of poor-quality processed In many parts of the world, this nutrition
foods, often available at lower prices, has taken transition is accompanied by increased
place in many countries (see Box 5). Often this has consumption of meat, total fat and trans-fatty
resulted in the significant loss of biodiversity, and acids, sugar and sodium, components that
the agroecosystems and knowledge that nurture it, have contributed to the dramatic emergence of
much of it nutritionally superior to the energy-rich obesity and associated chronic diseases (Ho et
and nutrient-poor food products that comprise al. 2008; Eilat-Adar et al. 2008; Haddad et al.
the more simplified diets resulting from this 2014). Others also highlight that the links and
transformation (Dora et al. 2015). Such dietary interactions between diet and obesity may be
shifts are among the complex range of factors more complex than this, with diets excessively
that have contributed to the alarming levels of high in sugars and carbohydrates altering the gut
overweight and obesity observed in over 2 billion microflora to selectively favour bacterial groups
people globally (Ng et al. 2014), as well as the rise such as Firmicutes, which are better at processing
in diet-related chronic diseases such as diabetes these types of foods and converting them to
and hypertension, which have huge impacts on calories with the consequence that the obese gut
personal, social and economic development. It has microflora is much less diverse (DeClerck 2013;
been estimated that the costs of dealing with diet- Clark et al. 2012; Delzenne and Cani, 2011). As the
related NCDs globally between 2011 and 2030 will chapter on microbial diversity within this volume

114 Connecting Global Priorities: Biodiversity and Human Health

 %R['LHWVLPSOLƩFDWLRQLQWKH3KLOLSSLQHV

Results from the Philippine National Nutrition survey suggests that the nation s diet is consistent with
the world phenomenon of diet simpli cation, that is, less complex and high-energy diets (Frison et al.
2010). Food consumption data from 1978 to 2003 show the dietary pattern of Filipinos comprised
rice, sh and vegetables. Changes in proportions of these food items, however, led to energy-dense
density diets. Alongside this, there is a downward trend in the consumption of fruits and vegetables.
Intake of starchy roots and tubers was halved from 1978 to 2003 (Pedro et al. 2006). On the other
hand, there is increased consumption of meat, fats and oil, milk and sugars. This pattern, described as
the nutrition transition, is also seen in other developing countries (Popkin 2001; Popkin et al. 2012).
Recent diet diversity studies among Filipino children also re ect simpli ed diets as diet diversity
score results are found to be below cut-o points (Kennedy et al. 2007; Talavera et al. 2011). It
should be noted that low scores indicate unsatisfactory nutrient adequacy (Hoddinott and ohannes
2002; Ruel et al. 2004; Steyn et al. 2006). This lack of diet diversity is multi factorial (i.e. lack of
purchasing power, unavailability in the markets, unfamiliarity with certain food items, lack of know-
how on to prepare/consume them). The nutrition transition, together with intensive agriculture and
environmental pressures, is also attributed to reduction in dietary diversity and the accompanying
loss in agricultural biodiversity and associated traditional knowledge (Gold and McBurney 2012).

also indicates, further exposure to the microbial Box 6). In this region, it is estimated that NCDs
diversity in the environment may also contribute account for 75% of deaths, while there are signs
to the development of Firmicutes, particularly that life expectancy in some countries is slowing,
lactobacilli and the regulation of immune even declining, as a consequence of NCDs
responses (Lewis et al. 2012). More recently, (Snowdon and Thow 2014).
scientists have shown that the gut microbiome is
much more diverse in rural Papua New Guineans Key recommendations from The Lancet Obesity
compared to people living in the United States and 2015 Series include efforts to ensure healthy
attributed this to a western lifestyle, hygiene and food environments and food systems through
diet (Martinez et al. 2015). Similar observations approaches that protect healthy food preferences
regarding gut microbiota diversity have been made from market intrusion  – such as policies that
among pre-contact Yanomami Amerindians in the promote healthy food services in schools and early
Amazon (Clemente et al. 2015). As also noted in childhood settings – and approaches that allow
the chapter on agricultural biodiversity within people to satisfy their healthy food preferences
this volume, shifts to livestock intensification through food policies that place taxes on unhealthy
and diets dominated by meat consumption also foods or support good access to fresh nutritious
impact negatively on ecosystems and biodiversity, foods (Swinburn et al. 2015; Lobstein et al. 2015).
and are associated with an increased risk of NCDs, In Mexico – where the proportion of overweight
including cardiovascular disease and some types of women between the ages of 20 and 49 years
cancer (World Cancer Research Fund 2007). increased from 25% to 35.5%, and where almost
30% of children between the ages of 5 and 11 years
Some of the highest rates of obesity and growing are considered overweight – the government,
burden of NCDs can be observed in the Pacific under pressure to address the growing health
region (Snowdon and Thow 2014) where many crisis, passed a bill to apply taxes on high-
small island states have undergone major changes calorie packaged foods (including peanut butter,
in traditional diets, to the extent that they are sweetened breakfast cereals and soft drinks).
largely reliant on less healthy food imports (see More sustainable and complementary actions

Connecting Global Priorities: Biodiversity and Human Health 115

 %R['LHWDU\FKDQJHDQGWKHULVHRI1&'VLQWKH3DFLƩF

The Federated States of Micronesia (FSM) have witnessed signi cant dietary shifts from nutritious
and diverse local staples to an increased dependence on imported, often unhealthy, foods in the
past few decades, with up to 40% of all imports being food imports in 1986 (Englberger et al.
2003d; 2011). In 2007, it was the second most obese country in the world, with pockets of vitamin
A de ciency being among the highest worldwide, despite its abundance of local nutritionally rich
local foods, including 133 varieties of breadfruit, 55 of banana, 171 of yam, 24 of giant swamp taro,
nine varieties of tapioca and many varieties of pandanus in the state of Pohnpei alone (Englberger
and ohnson 2013). There was little evidence of malnutrition, diabetes or hypertension before the
1940s, with vitamin A de ciency not documented until 1998, indicating the likelihood that these
were not problems . Englberger et al. (2003d) argue that it was not until a number of US initiatives
started in the 1960s that issues of dependency on imported foods and dietary shifts began and, by
1985, the national school feeding programme provided meals to 30% of its population based largely
on food imports. While access to more diversi ed foods is not without its bene ts, an over reliance
on imported foods threatens food security, sometimes leading to foods with lower nutritional
quality, and can contribute to the chronic NCD burden (borne by an already overburdened national
economy), and undermine traditional coping mechanisms and contingency planning developed by
communities to deal with periods of food insecurity. Unfavourable food and trade policies often
exacerbate these problems. Imported chicken and turkey tails are commonly eaten in FSM. These
are fatty o -cuts, which are not marketed or consumed in their countries of origin because they are
considered “health damaging products” and the practice of selling in the Paci c is seen as a form
of “food inequality” considered by some as inappropriate “food dumping” (Hughes and Lawrence,
2005; ackson, 1997). Such practices in the Paci c have prompted a range of trade-related food
policy initiatives aimed at creating a healthier food environment (Thow et al. 2010; Snowdon and
Thow 2014).

to encourage healthy local food alternatives are farming families (Roberto et al. 2015). Swinburn et
needed (GRAIN 2015), despite the government’s al. (2015) also point out that the early momentum
efforts to put in place food regulations that aim to better link agriculture and nutrition⁷ must be
to improve the availability and accessibility of maintained in order to achieve the goal of healthy,
healthy foods in schools (Roberto et al. 2015). sustainable, equitable and economically viable
One example of an initiative to create healthy food food systems. Among other things, this should
environments in schools has been the Brazilian include efforts to concentrate on the preservation
government’s changed food procurement policies and strengthening of national food sovereignty
during President Luiz Inacio Lula da Silva’s term, and agro-food biodiversity, and the creation of
which favour and support the production and sustainable diets. They also emphasize the need
consumption of non-processed, fresh and locally to include global goals to reduce obesity and NCDs
produced foods and provide greater equity to in the UN’s Post-2015 Development Agenda.

⁷ See Key recommendations for improving nutrition through agriculture and food systems. http://www.fao.org/fileadmin/
user_upload/nutrition/docs/10Key_recommendations.pdf

116 Connecting Global Priorities: Biodiversity and Human Health

7. Nutrition, biodiversity and in open spaces (Gerster-Bentaya 2013). A case
agriculture in the context of study to determine the potential of rooftop
garden vegetable production in the city of Bologna
urbanization found that it could satisfy 77% of its residents’
By 2050, it is estimated that about 6.3 billion needs and that besides this contribution to food
people will inhabit the world’s towns and cities, security and nutrition of the city, the potential
marking a rise of 3.5 billion from 2010, and the benefits of rooftop gardens to urban biodiversity
total urban area is expected to triple between and ecosystem service provision could also
2000 and 2030 (CBD 2012). This will present be substantial by facilitating green corridors
great challenges for sustainable food production connecting biodiversity-rich areas across and close
and consumption, and food systems in general. to the city (Orsini et al. 2014).
A 2014 study using spatial overlay analysis,
integrating global data on croplands and urban There is a direct relationship between biodiversity
areas, estimates the global area of urban and peri- and food security in cities. Biodiversity and
urban irrigated and rainfed croplands to be about small-scale production in urban food systems
24 Mha (11% of all irrigated croplands) and 44 Mha play a critical role in the fight against hunger and
(4.7% of all rainfed croplands), respectively. This diet-related health problems, and is pivotal in
clearly demonstrates an important role for food developing resilient city-regional food systems.
production and security in urban areas (Thebo Yet the rapid growth of cities is challenging
et al. 2014). As urbanization continues to rise, the provisioning capabilities of agriculture and
both terrestrial and aquatic ecosystems may modifying food systems at local and global levels,
be increasingly threatened (Boelee 2011). This while at the same time, a shift in urban diets
urbanizing trend has corresponding implications to less diverse and more processed foods has
for food and nutrition security, as estimates increased the incidence of NCDs such as obesity
indicate that urban inhabitants are likely to and diabetes. The expansion of urban populations
shift to diets that are more energy, calorie and will dramatically increase global demand for food
protein intensive, further exacerbating the risks of a non-subsistence nature while continuing
of obesity, including in low-and middle-income urbanization will put pressure on existing food
countries (Popkin et al. 2012). Despite these production, potentially increasing land-cover
risks, urban spaces also present considerable change and threatening biodiversity unless
opportunities to promote greater conservation carefully managed. Increasing biodiversity in our
and use of biodiversity, including mainstreaming existing food systems is critical to maintaining
of biodiversity into city landscapes and city food healthy global food systems and the ecosystem
systems, as exemplified by recent discussions for services they depend on, and to improving global
an urban food policy pact (UFPP); an emerging food security (CBD 2012).
global initiative to “feed cities” in a more just,
healthy and sustainable way.⁸ Peri-urban locations With increasing urbanization and rural-to-urban
may already be important areas where crop migration, the provision of a healthy and
diversity survives (Elyse Messer 2015). balanced diet will require an increase in urban
agriculture. In the Kibera slums of Nairobi,
It is estimated that around 15% of the world’s Kenya, households have recently begun a new
food is currently grown in urban and peri-urban form of urban agriculture called “sack gardening”
areas, including backyards, roof-tops, balconies, in which neglected and underutilized but highly
community gardening in vacant lots and parks, nutritious indigenous vegetables can be planted
urban fringe agriculture and livestock grazing into large sacks filled with topsoil, which can

⁸ At the time of writing, discussions were under way on the implementation of the UFPP, which will be implemented by Milan’s
city government over the next five years. It was being drafted through a broad participatory process, beginning with an
assessment of the strengths and weaknesses of the city’s food system. See for example: http://www.ipsnews.net/2015/04/
expo-2015-host-city-promotes-urban-food-policy-pact/

Connecting Global Priorities: Biodiversity and Human Health 117

 contribute to household food security, increase the urban poor (Patel et al. 2014). Roberto et
dietary diversity and reduce the need to resort al. (2015) also highlight that local governments
to other coping mechanisms used during food are increasingly using urban planning processes
shortages (Gallaher et al. 2013). One of the to ensure that new residential and commercial
remarkable success stories of linking agricultural developments have adequate access to healthy
biodiversity to urban markets have been African food markets such as farmers’ markets and mobile
leafy vegetables (ALVs). A project to promote ALVs vendors of healthy foods.
in urban markets in Kenya in 2003 resulted in
significant impacts and outcomes. Growers around In developed countries such as Australia and the
Nairobi who were trained to produce high-quality UK, approaches to urban agriculture have focused
ALVs for city supermarkets saw their incomes on biodiversity, localization, farmer’s markets,
increase twenty fold while sales of ALVs in Nairobi community gardens and the viability of farms
increased by a staggering 1100% (Cherfas 2006). that occupy or surround cities. In 2008, the City
The IndigenoVeg network, targeting urban and of Melbourne endorsed the Future Melbourne
peri-urban areas, was also successful in promoting Plan which links production, biodiversity and
African indigenous vegetables (Shackleton et al. sustainable consumption by setting out an
2009). ambitious target of 30% of food to be either
grown within the city or sourced from within 50
The urban street food sector can also play an km of the city by 2020. There are now over fifty
important role in urban food security and accredited farmers, markets in the larger Victoria
nutrition. For example, the urban vendors in area supplied by some 2000 farmers. Twelve
Madurai who sell ready-to-eat, healthy millet- of these farmers markets are located within
based porridges have improved access to nutritious Melbourne’s suburbs, eight within 125 km of the
foods and created livelihood opportunities for city, and the rest in rural and regional areas. Rare

BIOVERSITY INTERNATIONAL

118 Connecting Global Priorities: Biodiversity and Human Health

breeds sold at farmer’s markets around Melbourne field-to-plate lunch, and seed swaps. Regular
include critical, endangered or vulnerable pig newsletters, an active website, presentations
breeds such as the Wessex Saddleback, Large beyond the local district, and veggie tourism also
Black and Tamworth as well as “at risk cattle serve to maintain the momentum of the initiative
breeds such as the Belted Galloway. Melbourne (Paull 2013).
farmers” markets contain far greater diversity
of plant varieties and animal breeds than can be
8. Food cultures: local strategies
found in mainstream supply chains. A network
of community gardens further adds to initiatives with global policy implications
that make available additional nutritious fruit and There is ample evidence of how monocrop, low-
vegetable biodiversity to low-income households diversity agriculture, the shift toward urbanization
(Donati et al. 2013). and the depletion of natural resources, including
our marine resources, has led not only to the
In the UK, the Incredible Edible Todmorden erosion of our terrestrial, freshwater and marine
initiative encourages the novel concept of open- ecosystems but also of traditional food cultures
source food, through “permission gardens” and in many parts of the world (Anderson 2010;
“guerilla gardens”, which consist of picking and Petrini 2013). This has dramatically changed our
eating foods others have planted and nurtured. relationship with food and challenged many of the
Under this initative, forty public fruit and cultural norms, customs and traditions which have
vegetable gardens that promote awareness about governed how we grow and consume food. This
the benefits of food biodiversity, dietary diversity has led to significant changes in our food choices,
and nutrition were created. It also held a variety the amount of different foods we eat, the order
of communication and awareness-raising events, in which we eat, when and with whom (Pollan
including street cook-offs, “Tod Talks”, targeted 2008). In some parts of the world this has led to
campaigns such as “Every Egg Matters”, which a growing Slow Food movement as described in
maps local egg production, cooking courses, the Box 7.

Box 7. Slow Food and Torre Guaceto, Italy Marine Protected Area: a model to
promote food cultures, health and sustainable use

Slow Food, a grassroots organization now spanning over 150 countries, is aimed at preventing
the disappearance of local food cultures and traditions, counteracting the rise of “the fast life”,
homogenizing food production, intensive industrial agricultural crops based on monoculture,
and promoting interest in food s origins and cultural traditions at all levels of production and
consumption (Petrini 2013; Schneider 2008; Kinley 2012). The selection of Slow Food products
is based on an established set of criteria and a continuous exchange of information with local
stakeholders to ensure social–cultural, environmental and economic sustainability.

Several approaches have been used to evaluate the sustainability and nutritional impact of these
products. Recently, Pezzana et al. (2014) combined nutritional and multi-criteria sustainability to
de ne the Life Cycle Assessment of Slow Food Presidia products. The study found “high levels of
sustainability” and additional nutritional value of Slow Food products, and the value of multifactorial
approaches in the analysis of the food–health–sustainability relationship (Pezzana et al. 2014).

Presidia products focus on key issues of interest for small-scale agriculture and farming, including
the protection of mountain pastures and pastoral farming, defence of traditional landscapes
and propagation of traditional seeds by communities, protection of small-scale onshore shing,

Connecting Global Priorities: Biodiversity and Human Health 119

 transparent labelling, ecologically sustainable packaging and the preservation of traditional artisanal
knowledge linked to processing methods.

Examples include small-scale artisanal shing, which uses low-impact shing gear and regulates
exploitation; it is part of the Mediterranean identity, employing half-a-million people in the region,
promoting sustainable shing practices and allowing sh stocks to recover. Sustainable shing also
implies the need to consider the conservation of marine species, production chains, ecological
communities, and the human communities that support and rely on them for food, nutrition
and income.

The 22 km2 marine protected area (MPA) of Torre Guaceto is a successful example of the bene ts of
Slow Food for local communities. Initially established as a no shing MPA in 1991, its enforcement
became e ective only in 2000 when the MPA authority and local shermen struck an agreement
to implement a ve-year shing ban, allowing sh to repopulate and habitats to recover (Guidetti
2010). Fishing gear and practices that caused the least damage to marine species and habitats
were enforced. By the end of 2005, striped red mullet (Mullus surmuletus), large-scaled scorpion sh
(Scorpaena scrofa) and other taxa also rebounded (Guidetti 2010). Once the reserve partially
reopened, local shermen began to haul in catches more than twice the size of those outside the
reserve (PISCO 2011).

Local MPA management authorities can also help shing communities to increase income
opportunities where these are limited by seasonal variations or local preferences. For example, the
Torre Guaceto MPA Municipality of Carovigno is far from large markets, some catch, including mullets
(family Mugilidae), are not a local favourite year-round, making market value and income highly
variable. Collaboration between the MPA Authority, the Slow Food Association and the Fishermen
Cooperative of Carovigno in 2014 led to the production of mullet llets in extra virgin olive oil in
glass jars, to stimulate quality and sustainable production of mullet processing for a broader market.

This o ers a good example of how local communities bene t from MPAs, which are critical for
their protection, and how co-management schemes within protected areas may in turn deliver
co-bene ts to ecosystems and local communities. These may reduce competition for shared shing
resources, promote foods high in nutritional value, and support livelihoods and the conservation of
food cultures. These initiatives are important to jointly increase awareness, sustainability and social
acceptance of MPAs, and maximize bene ts for local populations.

Pockets of traditional food culture remain strong plant, animal and fungal origin have been reported,
in many parts of the world despite economic, which are used and prepared in many different
social and cultural change. Where people still ways (Maundu et al. 2013a; 2013b;2013c; 2013d,
retain a close connection with the landscape. see also chapter on traditional medicines). Another
Where biocultural refugia continue to exist, example of retained traditional food culture can
which safeguard the diversity of food-related be found in the harsh geography of the Pamir
practices for food and nutrition (Barthel et al. Mountains of Afghanistan and Tajikistan, where
2013). The East Pokot and Isukha communities biodiversity plays a very large role in sustaining life
in Kenya constitute examples for rich traditional and the environment has shaped a system that is
food cultures with manifold associated traditions, uniquely suited to this region and which, in turn,
beliefs, taboos and practices based on living in a has fostered the development of a rich source of
biodiverse environment. More than 130 foods of skills and resilience in its people (van Oudenhoven

120 Connecting Global Priorities: Biodiversity and Human Health

& Haider 2015). In Indonesia, the Centre for Food 2001). In fact, vegetable consumption is among
and Nutrition Studies of the University of Gadjah the highest in Asia. There is hardly any Korean
Mada (UGM) is documenting food diversity and dish without vegetables and over 300 types of
traditional knowledge among communities in vegetables are eaten in rural areas, including wild
Yogyakarta. Closely linked to cultural and religious greens like Chinese bellflower and bracken, field-
festivals, food culture is very much alive in rural grown greens like shepherd’s purse and wild garlic,
communities where ten local root crops are still and cultivated vegetables like squash, eggplant
widely consumed by the young and old. Efforts and cucumber (Lee et al. 2002). The inherent
are being made to establish links between these biodiversity of this traditional diet has beneficial
foods and healthier diets and to promote these health effects resulting, for example, in low adult
local alternatives to imported convenience foods⁹. obesity levels (Lee et al. 2002) as well as a 33%
and 21% decreased risk of having elevated blood
There are examples where traditional foods and glucose and elevated blood pressure, respectively,
the food cultures which have embraced them have compared to a westernized “meat and alcohol”-
contributed to sustainable and healthy diets as based diet (Song & Joung 2012). Okinawa, the
well as healthy lifestyles – in fact, the term diet most southern prefecture of Japan, is widely
originates from the Greek diaita meaning way of life known for its population that is characterized
or lifestyle (UNESCO 2010). The Mediterranean by long average life expectancy, large number
diet has recently been recognized by UNESCO of persons reaching the age of 100 years, and
as an intangible heritage of humanity in Spain, low prevalence of age-associated diseases. These
Greece, Italy, Cyprus, Croatia, Portugal and positive characteristics are mainly associated
Morocco in order to preserve the Mediterranean with the traditional Okinawa diet and its deeply
food culture (UNESCO 2013). The nutritional embedded biodiversity, which is nutritionally
and cultural model of the Mediterranean diet is dense and low in calories due to high consumption
characterized by skills, knowledge, practices and of phytonutrient-and antioxidant-rich fruits and
traditions that concern obtaining food from the vegetables (Willcox et al. 2009). The Okinawa
landscape to the table, and that have remained food culture comprises many traditional foods,
constant over time and space (UNESCO 2013; herbs or spices derived from local ecosystems
Petrillo 2012). Besides the nutrition and health and consumed on a regular basis (such as white-
benefits of the Mediterranean diet, Tilman skinned or purple sweet potatoes, local bitter
and Clark (2014) highlight its environmental melons or green seaweed) which are classified as
benefits by showing, among others, that diet- “functional foods” (“food is medicine” is intrinsic
related greenhouse gas emissions per kilocalorie of Okinawan culture) due to their, among
from “cradle to farm gate” are nearly 25% lower others, anticancer, antidiabetic, antiviral, anti-
compared to a western omnivorous diet. South inflammatory and immune-enhancing properties
Korea is another example of a country that has (Willcox et al. 2009; Sho 2001).
retained much of its food culture and traditional
dietary habits despite change (Lee et al. 2002). It The New Nordic Diet (NND)¹⁰ was recently
is estimated that more than half of the population developed in Nordic countries in collaboration
still follows the traditional dietary patterns, with a world-leading Copenhagen gourmet
making the nutrition transition in South Korea restaurant to promote a food-based dietary
unique (Song & Joung 2012; Lee et al. 2002). The concept that emphasizes gastronomy, health and
traditional diet is characterized by high intake of the environment (Poulsen et al. 2014). Based
fruits and vegetables (especially fermented kimchi on traditional food culture and dietary habits,
rich in antioxidants, vitamins and minerals) and the NND strongly relies on diverse, regional
low intake of total fat (Lee et al. 2002; Lee et al. foods in season such as berries, cabbages, pears,

⁹ See Traditional Root Crops in Indonesia (http://www.b4fn.org/case-studies/traditional-root-crops-in-indonesia/) and many

other related case studies of food cultures.
¹⁰ http://newnordicfood.org/about-nnf-ii/new-nordic-kitchen-manifesto/

Connecting Global Priorities: Biodiversity and Human Health 121

 UNDP
apples, root vegetables, oats, rye, and fish – all 9. Mainstreaming biodiversity
of them traditional Nordic foods that have been for food and nutrition into public
found to have beneficial nutrition and health
effects (Poulsen et al. 2014; Olsen et al. 2011).
policies
Preliminary evidence shows that compliance Policy support is essential for making changes
with NND and its traditional healthy foods is sustainable. Nutrition and biodiversity offer
related to decreased mortality among Danes aged better opportunities to mainstream biodiversity
50–64 years (Olsen et al. 2011), increased weight into policies, programmes and projects. They
loss and improved blood pressure reduction in include the commitments made at ICN2 of
centrally obese individuals (Poulsen et al. 2014), countries to improve nutrition, e.g. by fostering
and significantly higher micronutrient intake (e.g. the relation between nutrition and agriculture
iodine 11%, vitamin D 42%) among schoolchildren through “nutrition-sensitive agriculture” where
aged 8–11 years compared to control groups biodiversity has an important role to play. Another
(Andersen et al. 2014). Furthermore, estimates major achievement in the agriculture sector is
from Denmark indicate that shifting from the the endorsement of the Voluntary Guidelines
average Danish diet to NND leads to overall for Mainstreaming Biodiversity into Policies,
socioeconomic savings of €42–266/person per Programmes and National and Regional Plans of
year due to reduced environmental impacts and Action on Nutrition (Guidelines) in 2015 by the
their associated costs (Saxe 2014). The example Commission on Genetic Resources for Food and
of NND shows that culturally appropriate dietary Agriculture (CGRFA)¹¹.
patterns based on local and traditional biodiverse
foods can successfully be developed in order to The Food Acquisition Programme (PAA) and
reach societal nutritional goals as well as decrease the National School Meals Programme (PNAE)
environmental impacts (Saxe 2014; Bere & Brug in Brazil are two public policy instruments that
2009). support family farming by acquiring family farm

¹¹ http://www.fao.org/3/a-mm464e.pdf

122 Connecting Global Priorities: Biodiversity and Human Health

products and directing them to public programmes The Ministry of Education through the National
and social organizations. Both instruments also Fund for Education Development (FNDE) is
provide incentives for greater integration of responsible for the PNAE, which aims to meet
biodiversity and have demonstrated that public the nutritional needs of schoolchildren, and
policy can be used to address food security while is considered one of the largest school feeding
supporting family farming, improving nutrition programmes in the world. By 2012, it is estimated
and encouraging biodiversity conservation. that the programme assisted over 43 million
schoolchildren. In 2009, the PNAE decreed that
By 2014, more than US$ 3.3 billion had been spent at least 30% of the food purchased through
on the purchase of over 3 million tonnes of food its programme must be bought directly from
under the PAA, with an average of 80,000 farming family farmers, which may encourage the use of
families/year involved in the programme. The PAA native species, and promote local and regional
is currently being implemented in approximately biodiversity. The FNDE also supports efforts
48% of Brazilian municipalities. through the promotion of school gardens to
improve awareness about food production and
In 2014, 619 of Brazilian municipalities (11%) were healthy eating habits.
assisted, reaching more than 3,900 governmental
and non-governmental organizations, including In Brazil, other relevant instruments to
schools, child care organizations, nursing homes mainstream biodiversity for food and nutrition
and community kitchens.¹² An estimated 15 also include the Food and Nutrition National
million people/year benefit from food distribution Policy (PNAN), National Plan for the Promotion
under the programme. The PAA has contributed of Socio-biodiversity Product Chains (PNPSB)
to promoting dietary diversification (including and Development of Organic Agriculture (Pro-
fruits and vegetables), sustainable management of Organic). A key component of this effort is to
biodiversity for food and nutrition on family farms, carry out nutritional composition analysis of
and the recovery and promotion of neglected and prioritized native edible species, both wild and
underutilized regional and local biodiversity foods. cultivated, to demonstrate that these species
In schools, the PAA ensures that fresh, locally are rich in nutrients and to use this knowledge
produced, often organic food, more compatible base to bring biodiversity conservation and its
with local food cultures, is also made available in sustainable use into these different public policies,
canteens. The programme has also contributed to and provide added incentives for procurement and
the validation and documentation of threatened use in school feeding. Brazil, with the assistance
traditional knowledge, food customs and local of the Biodiversity for Food and Nutrition
cultures associated with these foods, and foods (BFN) Initiative¹³, will establish the nutritional
such as babassu palm (Attalea speciosa) flour, baru composition data of over 70 native species
nut (Dipteryx alata) flour, cupuaçu (Theobroma prioritized by the Plants for the Future initiative,
grandiflorum), palm hearts, umbu (Spondias and those included in the PNPSB. This includes,
tuberosa), maxixe (Cucumis anguria) and jambú baru (Dipteryx alata), buriti (Mauritia flexuosa),
(Syzygium sp.) are being served more frequently cagaita (Eugenia dysenterica), mangaba (Hancornia
in schools and social care organizations (Grisa and speciosa) and pequi (Caryocar brasiliense). It
Schmitt 2013). While the nutritional impacts have also includes Umbu (Spondias tuberosa) from
yet to be fully assessed, preliminary PAA survey the Caatinga biome, and cupuaçu (Theobroma
results indicate improvements in dietary diversity grandiflorum) and pupunha (Bactris gasipaes)
and health status of target families. among others. This initiative is also working in
partnership with university-based Collaboration
Centers on School Food and Nutrition (CECANEs),

¹² http://www.conab.gov.br/OlalaCMS/uploads/arquivos/14_09_15_16_03_05_artigo_evolucao_do_paa_2.pdf, http://www.
conab.gov.br/OlalaCMS/uploads/arquivos/15_03_23_15_42_09_sumario_executivo_2014_revisado.pdf
¹³ http://www.b4fn.org/

Connecting Global Priorities: Biodiversity and Human Health 123

 which are linked to the PNAE. To this end, Brazil is Sustainability was featured as an important issue
building national capacity to facilitate the setting in many sectors, but in nutrition it was not clear
up of “Regional Centres for food composition how to proceed. As the health sector’s individual
data” within federal universities to strengthen nutrient approach and the agriculture sector’s food
integration and mainstreaming of biodiversity production approach were not leading to improved
into relevant policies, programmes, and initiatives nutritional outcomes, the focus had to turn to
focused on food and nutritional security, and “diets” as the fundamental unit of nutrition.
on the promotion of a healthy, diversified and
sustainable diet. Collaboration is also under way Biodiversity was the theme of the First
with the FNDE School Garden programme to International Conference on Sustainable Diets
promote awareness and appreciation of native motivated by the growing awareness of the
biodiversity for food and nutrition. alarming pace of biodiversity loss, ecosystem
degradation and their negative impacts on health
The BFN Project in all participating countries has and development. The Conference provided a
been active in drawing attention to the importance forum for consolidating the state of knowledge and
of biodiversity for food and nutrition in another advancing the thinking with a multidisciplinary
important national policy instrument aimed at the focus. In addition to the scientific sessions, two
sustainable use and conservation of biodiversity: working groups were convened: one to work on
National Biodiversity Strategies and Action Plans the draft definition of sustainable diets and the
(NBSAPs). other to develop a code of conduct (or code of
practice). A consensus definition of sustainable
diets, adopted at the First International
10. Global policy initiatives
Conference on Sustainable Diets, acknowledged
The decades of unsustainable nutrition-related the interdependencies of food production and
interventions, not to mention outright failures, consumption with food requirements and nutrient
from both the agriculture and health sectors recommendations, and reaffirmed the notion that
has prompted new thinking in many relevant the health of humans cannot be isolated from the
areas (McDermott et al. 2015). Nevertheless, health of ecosystems. Biodiversity was included
mainstream nutrition has largely continued to as an important component of the definition (see
focus on malnutrition solutions that take little or Box Definition of sustainable diets).
no heed of long-term sustainability or biodiversity,
and have relied principally on supplements,
Definition: Sustainable Diets are those diets
therapeutic formulations, nutrient fortificants for
with low environmental impacts, which
staple or convenience foods, and biofortification
contribute to food and nutrition security
through conventional plant breeding or genetic
and to a healthy life for present and future
modification (Lancet series 2008, 2013). At the
generations. Sustainable diets are protective
same time, refreshingly new perspectives on these
and respectful of biodiversity and ecosystems;
problems and challenges have been emerging
culturally acceptable; accessible; economically
from ecologists, among other fields, on the need
fair and affordable; nutritionally adequate,
to better integrate the disciplines of nutrition,
safe and healthy; while optimizing natural and
agronomy, ecology, economics with nutrition and
human resources.
human health, agriculture and food production,
environmental health and economic development
to address the multiple goals of reducing At the same time, Working Group 2 prepared
malnutrition, promoting sustainable agricultural a preamble and an outline for what might one
and food production and environmental day be developed and adopted as a code of
protection, often called eco-nutrition (Wahlqvist conduct or practice. It was modelled on the WHO
& Specht 1998; Deckelbaum 2011; Deckelbaum et International Code of Marketing of Breast-milk
al. 2006) or nutrition-sensitive agriculture (ICN2).

124 Connecting Global Priorities: Biodiversity and Human Health

Substitutes (WHO 1981). Text from that preamble livestock and the biodiversity of pasture and
included the following statements: grazing lands. Features included new data on
the nutrient content of milk and meat from the
• Conscious that food is an unequalled way of native horse breed of Mongolia, with its high n-3
providing ideal nutrition for all ages and life stages; fatty acid content; and similarly new data on the
n-3 fatty acid content of the pasture plants upon
• Recognizing that the conservation and which the horse feeds. Together, the genetic trait
sustainable use of food biodiversity is an of the mare and the grassland species provide
important part of human well-being; the essential fatty acids commonly thought to
be found almost exclusively in marine species to
• Considering that when ecosystems are not the population of this landlocked country (FAO
able to support healthy diets, there is a legitimate
2013b; Minjigdorj et al. 2012).
use of supplements and fortificants; but when
ecosystems are able to support healthy diets, The Mediterranean diet is being used in some of
nutrition programmes, policies and interventions these studies as a model for sustainable diets, with
supporting the use of supplements and fortificants “biodiversity” featuring in the most recent version
are inappropriate and can create or exacerbate of the Mediterranean diet pyramid (Bach-Faig et
malnutrition, and that the marketing of these food al. 2011), and as a key component in developing
substitutes and related products can contribute to methods and indicators (Dernini et al. 2013). In
major public health problems. their analysis using 50 years of global-level data
for over 100 countries to quantify the relationship
A platform for action was also conceived at the
between diet, NCDs and environmental
Conference, with the aim to improving the
sustainability, Tilman and Clark (2014) found
evidence base for biodiversity and nutrition.
that dietary changes have considerable potential
This has led to research partnerships involving
to reduce both the incidence of NCDs and
FAO, the Centre International de Hautes Études
environmental impacts. Their review illustrates
Agronomiques Méditerranéennes (CIHEAM),
a significant reduction in some selected negative
Biodiversity International, INRA (Institut
health outcomes, including type II diabetes, cancer
National de la Recherche Agronomique) and
incidence and mortality due to heart disease,
others, to develop methods and indicators for
for three alternative diets: a pescetarian diet; a
the characterization of different agro-ecological
vegetarian diet; and Mediterranean diet when
zones for sustainable diets (Dernini et al. 2013).
compared to a reference diet including all food
These studies are fostering new ideas for building
groups. Other studies confirm these conclusions
consensus on research and actions needed to link
(e.g. Katz and Meller 2014; Maillot and colleagues
human nutrition with biodiversity, ecosystems and
2011). Such findings have important implications
environmental impacts. Some examples include
for both the health and conservation sectors.
new metrics for nutritional diversity of cropping
Further integration of these considerations is
systems, nutrient diversity within species in
needed for the development of robust strategies
major food crops, sustainability of the food chain
and policies targeting a reduction in the global
from field to plate, traditional food system and
burden of NCDs.
nutrition security (Ignatius 2012), underutilized
fruit for human nutrition and sustainable diets, The sustainability of a diet is heavily determined
and conservation systems for plant biodiversity by interrelated factors categorized as agricultural,
for sustainable diets (FAO, 2012). health, sociocultural, environmental and
socioeconomic; so changes to one affect the others.
The Second International Scientific Symposium
This complex relationship makes understanding
on Sustainable Diets featured livestock as its
how sustainable diets can contribute to food
theme (FAO 2013b). The biodiversity of food
security and sustainable development agendas
animal species and breeds was presented, along
difficult (Johnston et al. 2014). Metrics and
with the synergies and interdependencies between

Connecting Global Priorities: Biodiversity and Human Health 125

 guidelines that form the basis for wider application identified (FAO 2005). In 2006, the COP adopted
are needed to aid decision-making processes the Framework for a Cross-Cutting Initiative
at regional and national scales (Prosperi et al. on Biodiversity for Food and Nutrition (CBD
2014), and to better understand the synergies and 2006). The Initiative gave a useful profile to some
trade-offs between dietary diversity, agricultural on-going research and development activities,
biodiversity and associated ecosystem functions and motivated renewed efforts in establishing
(Allen et al. 2014; Remans et al. 2014). and documenting the linkage among agriculture,
health and the environment sectors in addressing
A clear consensus has been reached in the nexus food and nutrition security with biodiversity as
between agriculture, health and environment, that a central feature. For the nutrition, community
the sustainable diets rationale, with biodiversity this represented a major thrust to mainstream
at its core, along with education and policies, is biodiversity in nutrition research, projects,
fundamental to the achievement of the broader programmes and initiatives.
goals of sustainable development, connecting
nutritional well-being of the individual and of The CGRFA, at its 14th session in 2013 (FAO
the community to the sustainability of feeding 2013a), formally recognized nutrients and diets,
the planet (UN 2012). The UN Secretary General’s as well as food, as ecosystem services, in order to
Zero Hunger Challenge, which links sustainable further increase the awareness of human nutrition
food systems and hunger reduction, is critical, as a concern for the environment sector, and the
as the world moves from the largely unmet awareness among human nutritionists of the
Millennium Development Goals to the post-2015 importance of biodiversity; and requested the
Development Agenda. And in his final report to preparation of guidelines for mainstreaming
the United Nations, the Special Rapporteur on biodiversity into all aspects of nutrition, including
the Right to Food issued a key recommendation, nutrition education, nutrition interventions,
“To reshape food systems for the promotion of nutrition policies and programmes. These
sustainable diets and effectively combat the mainstreaming guidelines were adopted at the
different faces of malnutrition” (Human Rights 15th Session of the CGRFA in 2015 (FAO 2015)¹⁴
Council 2014). to assist countries in mainstreaming biodiversity
into different sectors at country and regional levels,
In 2004, the CBD’s Conference of the Parties and into policies, programmes and plans of action,
(COP) formally recognized the linkages between all with the aim of improving nutrition. Prior to
biodiversity, food and nutrition, and the need to this formalized recognition, similarly important
enhance sustainable use of biodiversity to combat declarations were made, based on collection and
hunger and malnutrition. The COP requested analysis of research and traditional knowledge, in
the CBD’s Executive Secretary, in collaboration order to bring biodiversity and its attendant issues
with FAO and the former International Plant to the forefront of mainstream nutrition thinking.
Genetic Resources Institute, now Bioversity One of these was the AFROFOODS Call for Action
International, to undertake a cross-cutting (2009). This declaration was motivated in part by
initiative on biodiversity for food and nutrition the Lancet series (2008), and in part by a prevailing
(CBD 2004). Later that same year, the Commission dogma that Africa did not have the affluence or
on Genetic Resources for Food and Agriculture ability to be concerned about biodiversity, or
(CGRFA) also requested that FAO evaluate the indeed environmental sustainability, as other
relationship between biodiversity and nutrition. competing issues took priority (FAO 2009).
In 2005, via the Intergovernmental Technical
Working Group on Plant Genetic Resources for The Second International Conference on Nutrition
Food and Agriculture, eight high-priority actions (ICN2), jointly convened by FAO and WHO in
and another six lower-priority actions were 2014, focused on policies aimed at eradicating

¹⁴ http://www.fao.org/3/a-mm464e.pdf

126 Connecting Global Priorities: Biodiversity and Human Health

malnutrition in all its forms and transforming collaboration have been largely absent, with each
food systems to make nutritious diets available sector promoting solutions that unleash actual and
to all. Participants at ICN2 endorsed the Rome potential damage to other sectors (McEwan et al.
Declaration on Nutrition¹⁵ and the Framework 2013). Examples include agricultural production
for Action¹⁶. While the ICN2 outcomes do not intensification that causes biodiversity loss (IUCN
explicitly mention the potential use of biodiversity 2008), food and nutrition interventions that
or genetic resources for food and agriculture to undermine traditional/local agriculture (Frison
address malnutrition, some recommendations are et al. 2006; Wahlqvist and Specht 1998), and
highly relevant to promoting the use of biodiversity environmental conservation programmes that
to address certain nutritional problems. Examples lead to undernutrition (Kaimowitz and Sheil
include the following: 2007). While there has been some convergence
among the agriculture, environment, health and
• Recommendation 8 on the need to “review nutrition communities toward understanding the
national policies and investments and integrate interdependence between human and ecosystem
nutrition objectives into food and agriculture health, and how agricultural biodiversity and
policy, programme design and implementation, to healthy food systems plays a role in maintaining
enhance nutrition sensitive agriculture¹⁷, ensure both, more collaboration is needed to
food security and enable healthy diets”. simultaneously address the issues and minimize
the damage that can arise when sectors work alone
• Recommendation 10 on the need to “promote (McEwan et al. 2013; Burlingame 2014).
the diversification of crops including underutilized
traditional crops, more production of fruits and Policy dialogue is also key. Many voices from
vegetables, and appropriate production of animal- UN agencies, civil society, academia and the
source products as needed, applying sustainable private sector have expressed the need to
food production and natural resource management include biodiversity for food and nutrition in
practices”. the negotiations for the post-2015 Development
Agenda. Calls for Action, Declarations,
• Recommendation 42 on the need to “improve Recommendations, Codes and Compacts have
intake of micronutrients through consumption been put forward to assist the research and
of nutrient-dense foods, especially foods rich in development communities in their efforts to
iron, where necessary, through fortification and address biodiversity for food and nutrition.
supplementation strategies, and promote healthy The draft proposal of the Open Working Group
and diversified diets”. for Sustainable Development Goals presents
nutrition together with sustainable agriculture
11. Ways forward: toward a post- as one goal, and halting biodiversity loss together
with protection and sustainable use of ecosystems
2015 development agenda
as another goal (UN 2014). While negotiations on
Food and nutrition insecurity presents a this process are still ongoing, the points raised here
serious and growing global challenge, as does are key to informing the critical policy dialogue
environmental sustainability, and unsustainable that is taking place and indeed to the subsequent
and unhealthy food systems. They affect citizens implementation of the SDGs.
in all countries, everywhere. They are multifaceted
and complex issues, with no single way, or Biodiversity sits at the nexus of improving
single sector, to effectively solve such problems. nutrition and environmental sustainability, and
Interdisciplinary analysis and cross-sectoral offers unique opportunities to create synergies

¹⁵ http://www.fao.org/3/a-ml542e.pdf
¹⁶ http://www.fao.org/3/a-mm215e.pdf
¹⁷ http://www.fao.org/nutrition/policies-programmes/en/

Connecting Global Priorities: Biodiversity and Human Health 127

 between human and environmental health. This programming, and metrics that help us
chapter has reviewed many of the issues pertinent characterize food systems’ and ecosystems’
to this and points to a number of areas of concern, ability to provide sustainable diets; we need
which if improved and strengthened can help more information on tested and proven good
to improve the contribution of biodiversity to practices and interventions that can be scaled
nutrition and human health. These include the up to better mobilize biodiversity to improve
following: nutrition. Addressing these gaps would go
a long way in creating a more solid scientific
1. The current agricultural focus on food quantity base of reliable evidence that acknowledges
requires a paradigm shift to look at ways in food biodiversity’s actual and potential role in
which we can maximize food quality and safety. reducing malnutrition.
Biodiversity has an important role to play in this.
This has many aspects to it, including improving 3. To benefit from a more improved scientific
relevant agricultural, trade and food policies. evidence base of this nature, truly
Topical initiatives such as the current interest interdisciplinary analysis and cross-sectoral
in nutrition-sensitive agriculture and value collaboration at the highest level will be
chains provide opportunities for biodiversity essential to ensure the effective mainstreaming
to contribute to the quality and diversity of of biodiversity into relevant policies,
agricultural production. Regardless of the many programmes and national and regional plans
successes of agriculture during the past several of action on food and nutrition security.
decades, it is clear that current methods and This will require transformative political will,
levels of food production and consumption are leadership and vision. It will also require
not sustainable, and the finite natural resources considerable resources and budgets. While
of the planet are being exhausted or lost in there has been some convergence between
the process. While agricultural production is the agriculture, environment, health and
theoretically able to feed the world’s population, nutrition communities toward understanding
serious malnutrition still persists with an ever the interdependence between human and
increasing diet-related NCD burden, which ecosystem health, and how biodiversity plays
is going to have major public health cost a role in maintaining both, much more is
implications for many countries. needed to yield the necessary interdisciplinary
analysis and cross-sectoral approaches required
2. If we are to effect such a paradigm shift, moving to better understand and address nutrition and
from a focus on quantity to quality, significant environmental sustainability. In addition, much
knowledge gaps in our understanding of food more is needed to translate recent policy gains
biodiversity and its role in improving nutrition, and achievements at the global level to action
which still remain, will need to be addressed. and implementation at country level.
Among these gaps are: the need for enhanced
generation, compilation and dissemination of 4. All these changes, shifts and transformations
more food composition data – we still know so will require major attention to improving
little about the nutrient composition of the vast awareness and understanding among many
majority of the world’s edible biodiversity; the actors and stakeholders. It will also require
need for whole diets and landscape approaches significant attention to capacity building at
rather than approaches that focus on specific the global, national and local levels. It will
nutrients or single food approaches; the need require working with universities to encourage
for better and more informative research and the necessary interdisciplinary approaches to
studies to understand the complex pathways teaching and research. Realizing the creation of
that link biodiversity to human nutrition a scientific evidence base as elaborated above
and health as well as the development of will require major changes in approaches to
better tools, such as cost of diets and linear how we undertake research. It will require

128 Connecting Global Priorities: Biodiversity and Human Health

RAWPIXEL LTD / ISTOCKPHOTO

novel, innovative ways for individuals, century are increasingly interconnected. The
disciplines and organizations to work challenge of achieving good nutrition status
together. It will also require efforts aimed at in a way that is environmentally sustainable is
increasing the awareness of the general public, only now beginning to receive serious attention.
policy-makers, decision-makers and of the A change at scale in how people interact with
different stakeholders across all sectors on the their environment to fulfil the goals of food
importance of foods from different varieties and nutrition security is required. As we move
and breeds of plants and animals, as well as forward into the post-2015 Development
wild, neglected and underutilized species, in Agenda, it is increasingly recognized that
addressing malnutrition. human nutrition and environmental
sustainability should be considered intrinsically
5. All of this presents a big agenda; however, linked. But a major question now is “how to
the post-2015 Development Agenda presents practically do so?’. This chapter has gone some
a big opportunity. As we move forward into way in addressing this question. Innovative
the post-2015 Development Agenda we find scientific methods, pilot studies, metrics and
ourselves on the threshold of an opportunity good practices are emerging to help us rise to
where humanity can decide to alter course and the challenge. The opportunity is now to ensure
move beyond business-as-usual, which is really that nutrition security and environment are
no longer viable, to scenarios that facilitate closely linked through biodiversity in the post-
real substantial transformative change. As we 2015 Agenda.
have seen, the challenges of the twenty-first

Connecting Global Priorities: Biodiversity and Human Health 129

JAMES L. OCCI/AFPMB

7. Infectious diseases
1. Introduction and background 1.2 Socioecological relevance and
impacts of infectious diseases
1.1 Introduction Endemic infectious diseases (those that have
Infectious diseases have important implications been stably established in a given region) are
for both human health and biodiversity. Pathogens, responsible for over one billion human cases
the infectious diseases they cause, and the per year, leading to millions of deaths annually
organisms that carry them are often recognized (Grace et al. 2006). Two-thirds of known human
for their detrimental effects, but also serve vital infectious pathogens have emerged from animals,
roles for some species, ecosystem functioning and with the majority of recently emerging pathogens
supporting biodiversity. The same microbe may be originating in wildlife (Taylor et al. 2001; Jones et
pathogenic to some hosts and beneficial to others, al. 2008). This transmission from other species to
and the diversity and interactions of microbes are humans fits with pathogen ecology and evolution
important. For example, commensal organisms (e.g. opportunistic microbial adaptation and niche
(normal microbial flora) serve an important role exploitation), but our increasing interactions with
in fighting pathogens. This essential complexity is the environment are enabling opportunities for
often best understood in the plant kingdom, with pathogen spill-over into humans and altering
well-documented interdependencies among plant the systems around pathogen evolution and
species and microbes. In some cases, public health survival (Karesh et al. 2012). The human–human
and biodiversity needs do not align and must be transmission potential varies among pathogens.
balanced. However, human-caused global changes, For example, some infections are established in
such as deforestation, extractive industries animals (enzootic) and can be transmitted to
including logging and mining, introduction of people, but typically do not transmit between
invasive species, and urban development, are people (e.g. rabies), whereas others may be
driving infectious disease emergence and spread, maintained in human populations primarily by
as well as biodiversity loss. There are opportunities human–human transmission following initial
for preventing infectious diseases and reducing infection (e.g. HIV and Ebola virus disease).
biodiversity loss by addressing their common
drivers through a synergistic approach. With global change, ecological determinants are
interfacing more and more with socioeconomic
dynamics, affecting disease risks. As the global

130 Connecting Global Priorities: Biodiversity and Human Health

population increases, over five billion people ecosystem with impacts visible over a century
are projected to be living in urban areas by later (Holdo et al. 2007). At a micro-level, the
2030, and land allocated to urban landscapes is shared evolutionary fate of humans and their
expected to triple from 2000 levels (Seto et al. symbiotic bacteria has selected for mutual
2012), posing growing resource demands. Urban interactions that are essential for human health,
demography presents variable socioeconomic and ecological or genetic changes that uncouple
trends, with a significant population globally this shared fate can result in disease (Dethlefsen
(≥800 million people) residing in urban slums, et al. 2007). Geneticists have added a further
with limited access to sustaining resources and layer of understanding on the role disease plays
sanitation (Hacker et al. 2013). While the risks in maintaining the genetic diversity or variation
and impacts of infectious diseases are not limited within populations (Acevedo-Whitehouse et al.
to urban settings, urban conditions may present 2005; Acevedo-Whitehouse et al. 2006). Humans
heightened potential for spread and maintenance have generally worked to disrupt or deny this
in population-dense settings. process in both our own species by disease control
efforts, and in animals through both selective
In addition to the burden of human morbidity breeding and disease control (see also chapter on
and mortality, there are high financial costs microbial communities within this volume).
associated with infectious diseases. For example,
the 2003 SARS outbreak was estimated to cost the Despite our disease control efforts, there is
global economy over US $30 billion. Regionally increasing evidence that susceptibility to disease
endemic, often “neglected” diseases also inflict has genetic determinants, as shown in bovines
economic damages, e.g. control and treatment (Richards et al. 2010; Driscoll et al. 2011). The
for the canine tapeworm-transmitted Echinoccocus assumption from these results is that disease
– for which ungulates serve as an intermediate (through parasitic and/or pathogenic mechanisms)
host – totals over US $4 billion annually. Whereas contributes to maintaining genetic health, through
emerging diseases may pose acute health and “selecting” and “removing” the more homozygous,
financial impacts, they may potentially become disease-susceptible individuals and their genes
endemic, posing long-term impacts. Vector-borne (Acevedo-Whitehouse et al. 2003; Luquet et al.
and parasitic diseases, for which the predicted 2012; Paterson et al. 1998; Amos et al. 2009).
disease burden is driven by biodiversity changes Disease may also play a role in selection of animals
(increasing as biodiversity declines), have been for predation through reducing their fitness
shown to amplify the poverty cycle in some areas and this in turn may determine evolutionary
(Bonds et al. 2012). polymorphism and strain diversity of the infective
agents and/or pathogens adapted to these hosts
1.3 Ecological background (Morozov 2012). Disease ecology of natural
populations is complex and there is probably
Ecologists have observed that animal populations considerable fine tuning at the level of the host,
may contain significant numbers of infected pathogen and the environment, also considering
animals with few ecological consequences, e.g. co-infection (Ezenwa and Jolles 2011; Cleaveland
healthy pinniped and grouse population dynamics et al. 2008) and predation effects (Hethcotea et al
are influenced by the frequency and severity of 2004). With some pathogens, e.g. trypanosomes
epidemics without necessarily causing long- and avian influenza viruses, the regular challenge
term decline (Harwood & Hall 1990; Hudson they present to the immune system in a wide
et al. 1998). On the other hand, the ecology of range of hosts induces rapid evolution of new
an ecosystem (for example, factors including its antigenic profiles in parasite populations, as well
function and structure) can be fundamentally as a strong selection pressure for heterozygosity
changed by disease alone. The introduction of and/or variability in the parasite population. The
the rinderpest virus has dramatically altered host community responds with adaptive immunity
the animal and plant ecology of the Serengeti and latent infection, and with sub-clinical disease

Connecting Global Priorities: Biodiversity and Human Health 131

 at worst when stressed (Huchzmeyer 2001; van Ebola virus, but anthropogenic land use change,
Gils et al. 2007). These findings suggest that beginning with logging roads, bushmeat hunting,
an ecological approach to disease, rather than a development of villages and transformation for
simplistic “one germ, one disease” approach will agriculture, likely brings human populations into
provide a richer understanding of disease-related closer contact with the reservoir hosts (Walsh et
outcomes. al. 2003).

Natural landscapes also harbour vectors of

2. Infectious disease ecology and human pathogens, some of which have thwarted
drivers the colonization and persistence of human
settlements in some regions. In particular,
2.1 The complex relationship between malaria, carried and transmitted by the Anopheles
habitat, biodiversity and disease sp. mosquito, has plagued human populations
Anthropogenic disturbance and biodiversity loss globally for centuries. The drainage of large areas
have been strongly linked to increased prevalence of wetland and swamps, the breeding habitat
and elevated risk of zoonotic disease for a variety for Anopheles sp., for agriculture and land use
of pathogens. For instance, hantavirus prevalence change has helped to dramatically reduce the
is thought to increase when mammal diversity incidence of malaria in some parts of the world
decreases; the rise of West Nile virus is correlated (e.g. Lower Great Lakes Basin, Rapport et al 2009).
with decreases in non-passerine bird richness; Meanwhile, deforestation has coincided with
landscape prevalence of Bartonella increases an upsurge of malaria and its vectors in Africa
when large wildlife are removed; and habitat (Coluzzi 1984; Coluzzi 1994; Coluzzi et al. 1979),
fragmentation increases risk of Lyme disease in Asia (Bunnag et al. 1979) and in Latin America
(Allan et al. 2003; Ezenwa et al. 2006; Suzán et al. (Tadei et al. 1998) as converted lands often include
2009; Young et al. 2014). Given that more than more areas of still water necessary for breeding of
60% of described human infectious diseases are malaria-transmitting mosquitos than intact forest
zoonotic (Taylor et al. 2001), including many of (Charlwood and Alecrim 1989; Marquez 1987).
humanity’s most pervasive diseases (e.g. influenza, This is especially true with expansion of paddy-
schistosomiasis), the relationships between field rice cultivation in previously forested areas,
biodiversity loss, disturbance and disease will have creating substantial habitat areas for the mosquito
enormous consequences for human well-being. (Singh et al. 1989). In Africa, the extensive current
deforestation and expansion of human activities
Changing landscape patterns can both positively into previously untouched regions is increasing
and negatively affect the transmission of zoonotic direct or indirect contact between humans and the
disease depending on the habitat change, shifts natural reservoirs of diseases, linked to increases
in species composition and the resulting extent in Yellow Fever (Brown 1977), and leishmaniasis
of human–disease contact (Rapport et al. 2009). (Sutherst 1993).
In many areas, human-induced land use changes
are primary drivers of range of infectious disease The mechanisms by which these relationships
outbreaks and emergence events and modifiers occur vary by systems, and include changes in host
of transmission of endemic infections (Patz et al. density, host behaviour, and mean competence of
2000). Indeed, land use change, food production all the hosts in an ecosystem at maintaining and
and agricultural change are reported to collectively transmitting a pathogen (Keesing et al. 2006).
account for almost half of all global zoonotic However, much of the focus on the diversity–
emergent infectious diseases (Keesing et al. disease relationship to date has focused on one
2010). At this scale, the most important factors particular mechanism – the so called “dilution
may be the contact among people and wildlife that effect.” The dilution effect suggests that non-
harbour zoonotic pathogens. For example, pristine random patterns of biodiversity loss following
forests in West Africa harbour bats that carry human disturbance will cause systematic losses

132 Connecting Global Priorities: Biodiversity and Human Health

of low competence (“diluting”) hosts, thereby species richness per se, but rather with changes in
increasing mean competence of hosts, and causing community composition (Dornelas et al. 2014).
an overall increased prevalence of pathogens in Changing species and population dynamics may
a landscape (Ostfeld and Keesing 2012; Myers also cause the amplification of a disease, enabling
et al. 2013). This pattern is hypothesized to more efficient transmission and spread.
occur because of a correlation between “pace of
life”, competence and vulnerability to human There is a strong and pressing need for more
disturbance. Consistent with this, there are now research on both the mechanisms and context
several studies that have found that fast life dependence of disturbance–biodiversity–disease
history traits also favour high host competence relationships – recognizing that diversity–disease
(Johnson et al. 2012; Johnson et al. 2013a; relationships are likely to vary with both space
Joseph et al. 2013), likely mediated by variation and time. While negative disturbance–disease
in immunological tolerance (Previtali et al. relationships certainly occur, we do not yet have
2012). Direct links between susceptibility to strong predictive power to suggest when and
human disturbance and mean competence for where they will occur for most human pathogens.
a particular pathogen have also been found in Environmental characteristics are also strongly
a few disease systems (Johnson et al. 2013b). likely to impact the likelihood of feedback between
While the dilution theory has been proposed as disturbance and disease prevalence (Estrada-Peña
the mechanism for some specific circumstances et al. 2014), but the nature of these relationships
(e.g. tick-borne disease), the effect appears to are still poorly understood.  
be more dependent on community composition
rather than biodiversity itself, and has been the 2.2 Biodiversity and hotspots of
subject of significant debate in the literature (e.g. diseases
Randolph and Dobson 2012).
Disease and biodiversity links can also be viewed
Thus, the impacts of biodiversity loss and habitat on a more global scale. In a 2008 study, Jones et al.
disturbance are far from straightforward, linear analysed the distribution of emerging infectious
or consistent (Ostfeld and Keesing 2012; Wood et disease (EID) events, defined as “the first temporal
al. 2014). Even for a single disease, such as Lyme emergence of a pathogen in a human population...
disease or malaria, the magnitude and direction related to the increase in distribution, increase in
of impact can vary across environmental contexts incidence or increase in virulence or other factor
and scales (Swei et al. 2011; Valle and Clark which led to that pathogen being classed as an
2013; Wood and Lafferty 2013), and quantitative emerging disease” (Jones et al. 2008). Jones et
reviews across pathogens and systems have also al. found that, after correcting for reporting bias,
shown even more mixed effects (Salkeld et al. EID events for different classes of diseases had
2013; Young et al. 2013). Most of the theoretical different global distributions (thus allowing us to
and experimental work to date on the dilution see so-called “hotspots” of disease emergence).
effect focuses on a small subset of vector-borne Jones et al. also examined the association of
diseases that meet a series of strict criteria; careful EID events with different socioeconomic and
review of major human pathogens suggests that environmental drivers of disease emergence,
only a subset appear likely to meet all criteria that including mammal species richness. They found
would make such a relationship likely (Wood et al. that mammalian biodiversity was a significant
2014). Parasite biodiversity and human pathogen predictor of the origin of zoonoses from wildlife.
richness also covary with diversity of larger
animals (Dunn et al. 2010), driving an increased These findings suggest that biodiversity
risk of emergence of novel infectious disease from contributes to disease emergence risk. One
biodiversity hotspots (Jones et al. 2008). Moreover, potential mechanism for this is that areas with
anthropogenic disturbance is not always, or even high biodiversity may play host to a larger pool
typically, associated with changes in diversity or of pathogens with the potential to infect humans

Connecting Global Priorities: Biodiversity and Human Health 133

 (Murray & Daszak 2013). If we assume that each in developing, tropical forest countries (Lambin
animal species is host to an average number of and Meyfroidt 2011). It is estimated that annual
pathogen species, we would expect regions with forest loss has averaged 2101km²/year across the
more animal species to also contain more species tropics between 2000 and 2012, and is increasing
of pathogens. If a relatively fixed proportion of globally (Hansen et al. 2013). Much of this forest
pathogens were able to infect humans, then we loss can be attributed to growing global demand
would expect to see more emerging zoonoses for food and natural resources (Cohen 2003;
in those regions. However, evidence supporting DeFries et al. 2010). In extent, the most significant
this assumption is scant; pathogen diversity form of land-use change is the expansion of
and the ability of a pathogen to infect humans crop and pastoral lands, which continue to have
seem to differ between taxa (Murray & Daszak serious negative long-term consequences for
2013; Ostfeld & Keesing 2013). Further study conservation of global biodiversity (Phalan et al.
of the ecology of host and pathogen biodiversity 2013), as agricultural expansion has largely come
would deepen our understanding of the role that at the expense of intact forests (Gibbs et al. 2010;
biodiversity plays in the risk of disease emergence. Lambin and Meyfroidt 2011).
This is especially warranted given the rapidly
changing ecological dynamics that are driving Under land-use change, human activities have
infectious disease emergence. the potential to impact disease dynamics by
directly and indirectly changing the behaviour,
distribution, abundance and contact between
2.3 Implications of ecosystem and
host species and vectors, as well as altering host
land use change: drivers of infectious
community composition. Land-use change has
diseases
been identified as a leading driver of recently-
During the last half century, anthropogenic emerging infectious diseases in humans (Figure 1).
conversion of much of the Earth’s natural Common land-use changes related to disease
ecosystems has greatly increased. Significant transmission include agricultural development,
changes in land use are occurring currently, mainly urbanization, deforestation, and forest and habitat

ǡǤǢǰǭǠɻ Drivers of emerging infectious diseases from wildlife (Loh et al., Vector Borne and Zoonotic
Diseases. In press)

Land-use changes

Human susceptibility to infection

Agricultural industry changes

International travel and commerce

War and famine

Medical industry changes

Climate and weather

Other

Demography and behavior

Bushmeat

Breakdown of public health

Food industry changes

0 10 20 30 40
Number of EID events

134 Connecting Global Priorities: Biodiversity and Human Health

fragmentation. A recent review investigating disease risk; or 2) via a “dilution effect” in which
how specific types of land-use change influence one would expect biodiversity to negatively
infectious disease risk found that more than half correlate with disease risk (Dunn 2010; Keesing et
of the studies (56.9%) documented increased al. 2010). Yet, examination of the theoretical and
pathogen transmission, 10.4% of studies observed empirical evidence has produced mixed support
decreased pathogen transmission, 30.4% had as to which of these hypotheses is generally more
variable and complex pathogen responses, and likely to occur under a land-use change scenario
2.4% showed no detectable changes (Gottdenker (Brearley et al. 2012; Murray and Daszak 2013;
et al. 2014). Randolph and Dobson 2012; Vourc’h et al. 2012).

Despite numerous and increasing attempts to

2.3.1 Extractive industries
detect a general relationship between land-use
change, biodiversity and disease risk, studies to Disease impacts may be magnified in tropical
date suggest few generalizations. As noted in the regions where primary forest is opened up to
sections above, a growing number of studies have mining, logging, plantation development, or oil
shown that biodiversity can influence disease risk and gas extraction (Karesh et al. 2012). These
through: 1) an “amplification effect” that predicts factors have been associated with outbreaks of
a positive correlation between biodiversity and Marburg virus, Chagas disease, yellow fever,
leishmaniasis and others.

Box 1: Case study: Changing human–animal–environment dynamics and the

emergence of Nipah virus

Increasingly intensi ed human-caused landscape and behaviour changes have had signi cant
consequences for human health over past decades. The emergence of Nipah virus provides a useful
example of anthropogenic drivers of EIDs. In 1998, the Nipah virus outbreak emerged in humans
in Malaysia. Flying fox bats (Pteropus spp.), the natural reservoir for Nipah virus, had rst infected
domestic pigs. The vehicle for the bat–pig spillover is thought to be fruit contaminated with bat saliva
from a fruit tree on the pig farm (Daszak et al. 2013). The dense pig housing conditions, respiratory
shedding and high birth rate enabled “ampli cation” of viral transmission, allowing ease of
transmission between pigs and to humans, leading to encephalitis and respiratory disease and over
100 human deaths. The disease was also seen in Singapore and was estimated to cost US 550–650
million in South East Asia, including costs incurred for control measures, the nancial impact to swine
industry, and loss of employment (Newcomb et al. 2011). Nipah virus has also since emerged in
Bangladesh and caused upwards of ten human outbreaks since 2001 (Luby et al. 2009a). The primary
mode of the initial transmission to humans in these outbreaks is thought to be infection directly
via ingestion of date palm sap that has been contaminated with bat saliva, urine or faeces (human–
human transmission following initial infection has also been reported in Bangladesh s Nipah virus
outbreaks) (Luby et al 2009a; Luby et al. 2009b). Domestic animals may also consume the date palm
sap contaminated by bats, thus potentially becoming infected and serving as an intermediate host
for infection to humans or other species (Hughes et al. 2009). As a preventive solution, some date
palm sap harvesters and researchers have tried placing bamboo skirts over sap collection buckets to
protect the harvest from contamination (Luby et al. 2009a; Khan et al. 2012). This approach promotes
both human livelihoods and the continued ecosystem services provided by bats such as seed
dispersion and pollination (Luby et al. 2009b).

Connecting Global Priorities: Biodiversity and Human Health 135

 The situations by which Nipah virus has emerged and re-emerged demonstrate two key factors: 1)
Human activity has driven Nipah virus emergence events. In Malaysia, deforestation and intensi ed
agriculture enabled the movement and mixing of species and the resulting opportunity for pathogen
transmission. In Bangladesh, human demand for natural resources through tapping into trees for sap
enabled a new food source for bats, similarly providing pathogen mixing opportunities that can be
detrimental to people and domestic animals (and potentially wildlife through con ict with humans
given health and livelihood risks, though this has not been documented speci cally for Nipah virus).
2) Ecosystem dynamics and disease ecology are complex. Land-use change and other changing
ecological scenarios in one region may have unanticipated e ects in another region through species
range adaptations and other factors. Climate change scenario models have suggested that increasing
temperature may enable spread of the bat species that harbour Nipah virus (Daszak et al. 2013).
Valuable information on risk factors for transmission from bats has been gained from bat ecology
studies, such as considerations around seroprevalence for Nipah virus, bat mobility and colony
connectivity, and temporal/seasonal aspects (Rahman et al. 2013). An ecosystem health perspective
is needed to better understand and mitigate both health and biodiversity risks of potential changes
to the environment.

NEIL PALMER PHOTOGRAPHY

Box 2: Ecological dynamics of infectious Disease: examples from South America

Changes in species biodiversity and composition a ect infectious disease transmission dynamics
(Terborgh et al. 2001; Osteld & Holt; 2004, Rocha et al.; 2014). In the Brazilian Amazon, the
transmission cycle for the human Chagas disease-causing parasite, Trypanosona cruzi, is related to
changes in small mammal composition. Species competent in transmission have been favoured
by transformation of native forest for homogeneous açaí plantations. The vector (Hemiptera sp.) is
sheltered naturally in palm trees and is attracted to açaí plantations. As major wild mammals have

136 Connecting Global Priorities: Biodiversity and Human Health

been removed from these areas, the vector is attracted to human habitations and begins to feed
on people and domestic animals living or working at açaí plantations, thus transposing the sylvatic
cycle to human dwellings (Araújo et al. 2009; Varella et al. 2009; Xavier et al. 2012). Handling,
extraction and preparation of coconut açaí pulp can allow for oral transmission (via contaminated
food) of T. cruzi, as the vector can be crushed in açaí processing and remains in cold conditions until
consumption, resulting in more than 100 new registered cases annually (Ministério da Saúde 2005;
Roque et al. 2008; Nobrega et al. 2009). The costs of Chagas disease are high: 30% of infected
people develop serious heart and digestive diseases. From 1975 to 1995 the Brazil Government
invested US 420 million in control of Chagas disease, with a return of US 3 billion, or US 7.16 for
each dollar invested (Akhavan 2000). Similar ecological dynamics have been observed for spotted
fever, an acute infection caused by the bacterium Rickettsia rickettsii, and transmitted by the bite of
an infected tick. Incidence in Brazil has been increasing since 1996, although most cases are not
diagnosed. Human mortality rate is 20%, and the most common vector is the star tick, Amblyomma
cajennense, that typically infests chickens, horses, cattle, dogs and pigs, as well as wild animals such
as capybaras, opossums, armadillos, snakes and wild canids. Changing species composition in small
fragments and conservation units remaining around the Atlantic Forest have resulted in growing
cases in south eastern Brazil, as also seen with Lyme disease in the United States (Meira et al. 2013).

Some disease relationships involve predator and prey, as predators can feed on prey that were
already ill or disabled, removing them from a population and thus controlling disease. Other
dynamics may also play important roles, as seen with the increase in rodent populations that are
controlled by a combination of factors besides predator control (Mills 2006; Armién et al. 2009),
as seems to be the scenario for hantavirus in the southern cone of South America. Several rodent
species and viral genotypes build a parasite–host puzzle in which hantavirus infection is density-
dependent of rodent populations. Rodent populations are promoted by food supply, absence of
predators, and even adaptability to synanthropic surroundings (Palma et al. 2012). In this region,
habitat characteristics determine infection prevalence. In Paraguay and Uruguay, the highest
prevalence of infected rodents are in disturbed areas such as planted elds, highway boundaries,
planted forests, shrub-woods and near houses. In these cases, predators no longer exist and even
with depleted populations of rodents, some population densities are high, increasing transmission
risk. In Argentina, areas with highest prevalence are the preserved ones, demonstrating complexities
and showing that knowledge of species and habitat characteristics are fundamental to the study of
disease (Palma et al. 2012).

In the Amazon region the number of cases of human bat bites increased by nine times in areas of
greatest deforestation between the years 2003 (852 cases) and 2004 (8,258 cases) (Ministério da
Saúde 2006). In Pará, the Brazilian state with the highest deforestation rate, the number of cases
jumped from 383 in 2003, to 7,640 in 2004, and more than 15,000 cases in 2005. These and other
increases have been related to the loss of the wild native species that are the natural food sources
for blood-sucking bats; humans, especially in mining areas, may serve as a substitute. Despite an
increase in the number of bites, a decrease in the number of rabies cases was observed, likely
indicating development of immunity in human populations through repeated exposure (Schneider et
al. 2001).

Ecological studies in the Amazon correlate deforestation, hydroelectric industry, human occupations,
and the presence of the mosquito vector Anopheles darlingi with increased malaria risk (Vasconcelos
et al. 2006; Vittor et al. 2009). In regions with large hydropower plants, the rate of malaria is 278

Connecting Global Priorities: Biodiversity and Human Health 137

 times higher than in forested areas (Afrane et al. 2006). In Brazil, according to 2011 data from the
Ministry of Health, 99.5% of cases of disease transmission were in the Amazon region. In Amazonia, a
complex set of factors relate disease transmission with environmental transformation. High mosquito
density caused by deforestation, construction of power plants, roads, irrigation, dams and the large
in ux of susceptible people (often living in houses without walls) inside or in forest edges helps
increase circulation of aetiological agents linked to geographical and climatic factors such as high
rates of rainfall, watershed amplitude and vegetation cover (Oliveira-Ferreira et al. 2010).

Genetic erosion may occur with loss of species, resulting in selection of receptive individuals for
new pathogens or ones without ability to adapt to growing resistance to pathogens already present.
This creates patches of high prevalence of infection and risk of spill-over to neighbouring regions,
signifying the need to align conservation and health goals to maintain connectivity between natural
areas to reduce anthropogenic driving forces for the emergence of diseases and biodiversity loss.

Disease dynamics are not limited to terrestrial settings. In marine environments, parasites tend to
be generalists that seemingly use an adaptive strategy of dispersion in uid environments. Infective
forms of parasites are more common on juvenile shes that are transmitted to others through the
food chain by predation (Marcogliese 2002). In some cases, humans can replace natural de nitive
hosts (e.g. cetaceans and pinnipeds) by eating raw sh. Thus, the reduction of sh stocks and the size
of sh caught (Shin et al. 2005) may be risk factors for helminth transmission (Ferreira et al 1984).
Oceans are typically a nal destination for e uent of domestic and industrial activities, and high
concentrations of microbes in coastal waters indicate probable water and seafood contamination.
Many bacteria and viruses are autochthonous to marine ecosystems (e.g. Aeromonadaceae and
Vibrionaceae), so the use of enteric microbes as indicators of microbiological water quality is strongly
limited, although many of them are clinically important to human health and biodiversity (Moura et
al. 2012). Early eutrophication of aquatic systems bene ts parasites with gastropod and crustacean
secondary hosts; additionally, release of waste into rivers and seas from human sewage and animal
farms also increases black y populations, resulting in increased risk of transmission of onchocerciasis
and economic losses to the cattle industry in areas of the Atlantic forest (Strieder et al. 2009).

Taken together, these examples of di erent infectious disease scenarios observed in South America
highlight the complexity of disease ecology, and the impacts of rapidly changing environmental
pressures. Ultimately, they demonstrate the importance of employing science-based proactive
disease risk analyses and risk prevention and mitigation strategies.

The mechanisms vary among sites and extractive cross-species transmission of pathogens, which
activity, but road building, establishment of can result in zoonotic disease. Additionally, new
settlements, and increased mobility of people into human inhabitants (recent immigrants) might not
remote regions, coupled with a lack of domestic have immunity to zoonotic diseases endemic to
animal food supply likely lead to an increase the area, making them particularly susceptible to
in hunting, wildlife consumption, and wildlife infection.
trade in areas where these changes are occurring.
Further, if sites are poorly managed, increased 2.3.2 Food production
populations can strain existing infrastructure,
leading to overcrowding, poor sanitary conditions, Changing food production methods, particularly
improper disposal of waste, and a lack of potable in livestock production, to meet the protein needs
water. All of these changes increase the risk of of a growing global population have also increased

138 Connecting Global Priorities: Biodiversity and Human Health

contact and pathogen transmission opportunities livestock or humans (Messenger et al. 2014).
between domestic animals, wildlife and humans. Epizootics of rinderpest, a cattle disease, have
Livestock grazing and livestock-associated feed caused large wildlife die-offs (Domenech et al.
crops account for an estimated 30% of land 2009). Smallholder farming, primarily in low-
area use, commonly involving deforestation for to middle-income, often biodiversity-rich areas
cattle farming (Pinto et al. 2008). The resulting in the southern hemisphere presents ongoing
infectious disease dynamics have ecological risks opportunities for contact between wildlife and
relevant to biodiversity, especially as areas may domestic animals. As seen in southern Africa,
be located on the perimeter of forest, wetlands the co-evolution in wildlife and livestock for
and other natural areas where wildlife–livestock several pathogens presents complex disease risks
animal contact opportunities are heightened. The (Cleaveland et al. 2005; Thomson et al. 2013).
intensification of livestock production in many Biosecurity strategies may not be available, or are
parts of the world, typically involving high animal ineffective. In some cases, disease containment
density, confined living quarters, and antimicrobial measures in food production may pose direct
use, have created conditions that may enable rapid threats to biodiversity; for example, fencing used
pathogen spread and evolution, especially among to enclose livestock production sites may cause
genetically similar breeds or immune-suppressed detrimental fragmentation of wildlife population,
animals (Liverani et al. 2013). The introduction affecting genetic diversity and increasing risk of
of disease can occur through many pathways, population crashes (Thomson et al. 2013).
including from wildlife (e.g. via direct contact,
via a vector carrying a pathogen acquired from Non-therapeutic use of antimicrobials in
wildlife, etc.). Wildlife may serve as reservoirs or food production systems (both agriculture
hosts for diseases of high importance for livestock and aquaculture) for prophylaxis and growth
production, including the majority of those listed promotion may also pose implications for
by the World Organisation for Animal Health biodiversity and potentially human medicine.
(OIE), such as the causal agents for foot and mouth While development of antimicrobial resistance
disease and bovine tuberculosis (Cleaveland et al.
2005; Miller et al. 2013). Non-zoonotic diseases,
while not posing infection risks to humans or
wildlife, can have detrimental impacts on food
security and thus access to nutrition for human
populations.

In addition to threats to livelihoods and food

security from livestock die-offs, human health may
be impacted. Livestock may serve as intermediate
hosts for zoonotic disease transmission from
wildlife to humans, in some cases serving an
amplifying role. For example, Nipah virus, for
which fruit bats are a natural reservoir, emerged
in humans in Malaysia following conversion of
forest to an intensive swine facility that enabled
bat–swine contact, and subsequently transmission
from pigs to humans (Karesh et al. 2012).

Most directly related to biodiversity, although

less well established given limited wildlife
disease surveillance, are known and novel
pathogen transmission events to wildlife from
FAO

Connecting Global Priorities: Biodiversity and Human Health 139

 is a natural phenomenon, the widespread of use The hefty economic value of the global trade in
of antimicrobials can create genetic selection wildlife is rarely countered in the literature by
pressures for resistant strains. Dispersion of its costs to governments and the public for the
antimicrobial drugs as well as genetic exchange introduction of invasive species, as discussed
through ecological processes may also present further in the following section. Likewise, several
non-target environmental exposure in humans significant zoonotic infectious diseases have
and wildlife (Allen et al. 2010). emerged in part due to the substantial human–
animal contact that occurs along the wildlife trade
2.3.3 Wildlife trade and disease chain, from harvest to end point. These diseases
have included SARS coronavirus (wet markets
Trade in wildlife involves the geographic in China), HIV (primate bushmeat hunting),
movement of hundreds of millions plants and monkeypox virus (exotic pet trade), and H5N1 and
animals worldwide comprising an estimated H7N9 avian influenza viruses (Karesh et al. 2005;
economic value of over US$ 300 billion per annum Gilbert et al. 2014). The global trade in wildlife
(including both legal and illegal trade estimates) provides disease transmission mechanisms that
(Ahlenius 2008). This trade is driven by consumer not only result in human and animal health
demand for a multitude of products ranging from threats but also damages to international trade,
traditional medicines, bushmeat, trophies, live agricultural livelihoods, and global food security.
exotic pets, and foods. Within each of these broad
categories exists a wide range of specialty market There is minimal overall health regulation of
value chains that vary greatly in their motivating the wildlife trade in comparison to agricultural
economics, sociocultural origins, geographical trade, and such work falls between regulatory
source and destination, transportation type authorities of national ministries (e.g. agricultural,
and route, trader and consumer profiles, species environmental and public health) and international
composition and condition, and local and regulatory organizations. Wildlife trade is complex
international legality. and multimodal and does not present equal
risk to environmental, agricultural and human
Trade in wildlife is illegal if it is contrary to the health. Thus the threat of disease emergence
laws of the participating nations or the limitations from the wildlife trade and the socioeconomic
on trade presented by the Convention on and behavioural factors that contribute to it
International Trade of Endangered Species of Flora cannot be defined with one overarching risk
and Fauna (CITES). Despite such protections, it assessment. Rather, specific market value chain
is estimated that illegal wildlife trade results in types require targeted evaluation and tailored
a mean source population decline of 60–70% in intervention policies that would put measures
targeted species (Karesh et al. 2012). This failure in place to facilitate relatively benign commerce
to protect vulnerable populations is a testament to while establishing the necessary measures to
the evasiveness of the wildlife trafficking industry minimize practices that are damaging to the global
from poacher to the black market, seemingly environment and health.
impossible to monitor, let alone control. Further,
challenges in curbing illegal international wildlife
2.3.4 Implications of biotic exchange
trade described by Conrad (2012) include high
demand and profit, cultural and societal traditions,
(invasive alien species)
ambiguity of property rights, negative economic The term invasive alien species (IAS) refers to a
incentives for bans, and inadequate enforcement. species, sub-species or other taxon of organism,
Of additional concern is the fact that only CITES- introduced by human action outside its natural
listed species garner much attempt at regulation past or present distribution, and whose introduc-
at all, while the ecological impact of harvest and tion, establishment and spread threatens biological
international trade of billions of non-CITES-listed diversity or ecosystem integrity. Introductions can
animals goes largely unassessed. occur either intentionally or accidentally, and the

140 Connecting Global Priorities: Biodiversity and Human Health

number of cases has dramatically increased with the accumulation of microcystins, hepatotoxins
globalized trade and travel (Butchart et al. 2010). and probable tumour promoters in the edible
Though many introductions have proven benefi- tissues of fish and their transfer and magnification
cial, the overall impact of IAS on biodiversity as along the food chain to final consumers” (Mazza
well as on human livelihood is negative, because 2013); some reports attribute the rise of Type E
they threaten health, infrastructures, economic botulism in Lake Erie to the ecological impact of
activities, food supplies, and ascetic/cultural eco- the zebra mussel (Perkins et al. 2010). Both the
system services (Pejchar and Mooney 2009; Vilà zebra mussel and cholera have been spread by
et al. 2010; Stoett 2010). IAS are also implicated the introduction of discharged ballast water from
in the spread of infectious diseases; and both inva- ships. Cholera killed more than 10 000 people in
sive species and infectious diseases are known Peru in 1991, and has been found in ballast tanks
drivers of ecosystem change (Crowl et al. 2008). from South America in North American ports
(Takahashi et al. 2008). Efforts to regulate ballast
A recent review (Mazza 2013) suggested that water have improved vastly in recent years, but it
the links between IAS, human health, and remains a primary vector of IAS worldwide with
infectious disease are manifold. Some pathogens immediate consequences for human health (see
and parasites, such as waterborne cholera or also chapter on freshwater within this volume).
mosquito-borne West Nile virus, can themselves
be categorized as IAS. Thus we can view modern These vector linkages can be quite complex. For
pandemics, such as HIV and the SARS crises, as example, the water hyacinth, a South American
instances of invasion at the microbial level. This freshwater ornamental plant now introduced
application of the IAS category is more usually worldwide and especially troublesome in sub-
investigated by epidemiologists than invasion Saharan Africa, can host mosquitoes and snail
biologists, but the two sciences will continue to species such as Biomphalaria sudanica and B.
learn from each other. choanomphala, which are in turn vectors of malaria
and schistosomiasis (Mack et al. 2000).
Other IAS act as vectors or reservoirs for
pathogens or parasites. For example, the Asian Human consumption of plants can also be linked
tiger mosquito has been linked to more than 20 to the spread of disease, since plants themselves
diseases, including yellow fever, dengue fever, and are highly susceptible. An analysis of emerging
chikungunya fever, and climate change projections infectious diseases (EIDs) in plants showed that the
show that the mosquito will likely extend its most significant cause of emergence is pathogen
range further north in coming years, exposing introduction via the international trade in plants
more people to bites. Raccoon dogs and red foxes and plant materials, as seen with introductions of
are becoming a new reservoir for rabies as they potato blight in several regions and Moko disease
spread into new Eastern European habitats from in bananas in Australia (Anderson et al. 2004).
the accidental release of animals utilized in the Furthermore, the majority of plant EIDs globally
fur trade (Mazza 2013; Chomel et al. 2007). The over past decades have stemmed from previously
invasion of East Africa by the neotropical shrub unknown pathogens (Santini 2013; see also
Lantana camara has increased the incidence of Bandyopadhyay & Frederiksen 1999; Anderson
sleeping sickness, since this species provides et al. 2004).
shelter to the tsetse fly (Mack et al. 2000).
The ecological, health and associated financial
Thirdly, IAS can also influence local conditions, costs from invasive alien species introductions
disturbing ecosystems to make them favourable to are significant. For example, the United States
pathogen or parasitic invasions. The invasion of the loses an estimated US$ 120 billion per year to the
North American Great Lakes by the infamous zebra over 50 000 invasive species that have already
mussel “favours the blooms of toxic cyanobacteria entered its borders (Pimentel et al. 2005). In most
such as Microcystis aeruginosa [which] can lead to nations these damages go unexamined. Beyond

Connecting Global Priorities: Biodiversity and Human Health 141

 the direct environmental impacts of non-native 2.3.5 Plant diseases
invasive species lies the less recognized pathogen
All biological entities on earth require energy for
pollution spread by these hosts. Under-recognized
the construction of their physical structure from
examples abound, ranging from the Varroa mite
molecular components, as well as for movement,
of pollinating honey bees to crayfish plague
behaviour, reproduction and other life activities.
(Alderman et al. 1996; Smith et al. 2013).
The ultimate source of new and replenishing
As climate change proceeds, most projections energy is sunlight, but because only green plants
suggest that there will be a further upsurge in and a few algae can capture solar energy and
infectious diseases related to IAS (Capinha et al. convert it to the “bio-currency” of chemical bonds
2013; Foxcroft et al. 2013; Hatcher et al. 2012) they are the primary producers in most natural
Perkins et al. assert that “[t]he introduction ecosystems, and the rest of us rely upon them,
of parasites with invading hosts is the most directly or indirectly, for our very lives.
important driver of disease emergence worldwide”
Consideration of biodiversity with respect to
(2010). It is imperative that invasion biology and
plant diseases must include both plants and their
policy be given adequate resources to recognize
pathogens, and in many cases insects that serve as
and respond to this direct threat to human
vectors for dissemination of some plant pathogens.
health. Effective biosecurity policies, focused on
Some of the drivers and threats to biodiversity
prevention of arrival of unwanted IAS, and on
affect all three. For example, ecosystem and land-
properly planned control of the most harmful
use changes (such as farming, mining, human
species, including those potentially impacting
habitation, trade and transportation) can change
human health, can help protect our environments,
the geographical ranges of plants, microbes and
and also prevent severe impacts on human
arthropods, creating new community structures
livelihood. Risk analysis tools, such as stated
and zones of intersection, and increase the risk
in the OIE Guidelines for Assessing the Risk of
of the emergence or spread of infectious plant
Non-Native Animals Becoming Invasive, can
diseases, just as they do in humans and animals.
be employed to better manage risks proactively
Even programmes designed to manage diseases
(World Organisation for Animal Health 2012).
may threaten biodiversity (Karesh et al. 2012).

Humans depend upon plants for more than just

food for ourselves and our livestock; we require
their fibre for clothing and shelter, and we are
exploring their potential to provide us with
renewable sources of biofuels. Over the centuries,
humans have utilized well over 7000 plant
species, some gathered from nature, but most
domesticated and modified via plant breeding
for convenient and cost-effective production,
harvest and processing. In nations where crops are
generally planted as high-yielding monocultures to
support modern production technologies, genetic
diversity is critical to sustainability in the face
of myriad threats (pathogens, insects, weather
extremes and climate change, habitat disturbance
or loss, escape of genes introduced into crop
species, etc.) that could affect a subset of species
at any given time. Humans rely currently on only
ECOHEALTH ALLIANCE

four species, rice, wheat, maize and potatoes, for

nearly two-thirds of our food energy requirements.

142 Connecting Global Priorities: Biodiversity and Human Health

Genetic diversity within such cultivated species, Each individual plant supports approximately
including progenitors and near-neighbours, is 30 other species, mostly microbes and insects
essential for long-term food and fibre security, (Ingram 2014). Many are pathogens, but others
not only for direct consumption but also as are synergists and commensals that fix nitrogen,
sources of germplasm for cultivar improvement acquire and share minerals and water from the
and adaptation in a changing world (FAO 2014; environment, produce plant growth-promoting
Ingram 2014) (see nutrition chapter). substances and antimicrobials, and out-compete
harmful organisms. Microbial biodiversity, there-
How does plant diversity influence disease fore, is a key factor in plant sustainability, in both
susceptibility and incidence? The answer is: “it natural and managed ecosystems. We know rel-
depends.” There is a non-linear, intricately complex atively little about microbes that inhabit native
relationship between habitat, biodiversity and plants and how they interact with their hosts, but
diseases, and evidence supports two contrasting investigators who look for them rarely fail to find
hypotheses (Keesing et al. 2006; Pagan et al. microbes in wild plants; for example, a range of
2012). The dilution effect asserts that plant viruses and fungi were detected in asymptomatic
diversity increases the space between individual grass species in the Tallgrass Prairie of north-cen-
members of a species, thereby reducing disease tral Oklahoma (Dutta et al. 2014; Cox et al. 2013).
risk. Monocultures, being highly artificial Can microbes residing in native plants jump to crop
environments, drastically alter microclimate species planted nearby? Alternatively, will agricul-
habitat and are more susceptible to high losses tural pathogens associated with cultivated species
because if one plant is susceptible, all are escape to wild relatives? Populations of pathogens
susceptible (Pagan et al. 2012; Garrett et al. 2013; having multi-species host ranges generally have
Mundt et al. 2002; Zhu et al. 2005). Disease greater connectedness, and plant community
and insect infestations may be less damaging dynamics can change; plant species having greater
in areas where cropping mixtures (such maize– disease resistance can serve as reservoirs for more
bean intercropping systems in Latin America, susceptible species (Cox et al. 2013).
or mixed-cultivar rice crops in China) are still
practiced (Castro et al. 1992; Zhu et al. 2005). In Aside from its key role in natural settings,
the amplification effect, diversity increases disease microbial biodiversity is also essential for
risk either because it leads to increased abundance successful agricultural enterprise. “Good”
of inoculum sources for a focal host (Pagan et al. microbes are deployed intentionally into crops
2012) or because it considers cases of non-optimal for disease biocontrol, nitrogen fixation, plant
insect vector populations (Keesing et al. 2006). growth promotion activity, and other benefits.
These two hypotheses are not mutually exclusive; Furthermore, crop improvement efforts, whether
rather, they can be considered as the ends of a by traditional or marker-assisted breeding, or
continuum (Pagan et al. 2012). genetic modification, are dependent upon the
availability of diverse and relevant pathogen

Box 3: One Health

The growing One Health philosophy provides a new and overarching perspective for understanding
the intersections of medicine, veterinary science and the environment (Karesh et al. 2012). Although
plant health and pathogen interactions are clearly central to sustainable life on earth, their critical
roles in the health of people, animals, and other elements of the environment should be more
systematically addressed as science seeks a holistic strategy that enfolds the multisectoral, policy-
level approaches that promote a One Health perspective (Fletcher et al. 2009).

Connecting Global Priorities: Biodiversity and Human Health 143

 strains for cultivar screening and evaluation of and viruses in aquacultured species; reviewed in
disease resistance. Stentiford et al. 2012).

Managing disease is an important goal to maintain

2.3.6 Marine infectious disease
ecosystem function and biodiversity in the ocean
Infectious diseases are important drivers within and to limit the exposure to disease in both
ecosystems, including marine ecosystems. Marine humans and marine organisms. Many of the
infectious disease is a complex interaction between land-based management techniques used in the
the host, pathogen and the environment (reviewed terrestrial environment are not practical and/or
by Burge et al. 2014), and each host–pathogen successful in the ocean, including quarantine,
interaction should be considered in a case-by-case culling and vaccination. The reduction of
manner. The ocean is a complex human-coupled exposure to and impacts of marine disease may
environment where transmission and severity be achieved through reducing stressors such as
of disease can be impacted by terrestrial run-off coastal pollution, habitat loss, translocation of
and pollution, direct and indirect impacts of pathogens, and harvest practices. However, some
climate change, transfers of animals (culture, stressors, such as those associated with climate
aquarium trade and private citizens), fishing and change – that is changes to physical (e.g. changes
aquaculture. Although disease is a notable driver in temperature, pH, and salinity) and biological
of community change in marine ecosystems, (e.g. range shifts of organisms) characteristics of
we still lack baseline data and understanding of the ocean – will be difficult to reduce. Strategies to
transmission dynamics in many systems. The manage disease need to include long-term climate
presence of disease is often first noted by dramatic and organismal monitoring, experimental work
large-scale die-offs of organisms. In case studies to test effects of ocean change on host–pathogen
spanning the globe, including both temperate and interactions, and forecasting and decision-support
tropical systems, diseases have been found to be tools to inform management. Factoring drivers of
important drivers of marine biodiversity change. disease such as climate into management will be
Key examples of large-scale impacts caused by key to ensuring the long-term sustainability of
marine infectious disease include eelgrass (e.g. diverse ocean ecosystems, and the benefits these
eelgrass wasting disease; reviewed by Burge et al. ecosystems provide to people.
2013), reef-building corals (multiple syndromes;
reviewed by Sutherland et al. 2004; Harvell et al.
2007; Bourne et al 2009; Burge et al 2014), oysters
3. Challenges and approaches
(e.g. Dermo and MSX diseases, Ford & Trip 1996),
3.1 Growing pressures and climate
abalone (e.g. withering syndrome; Friedman et al.
change
2000) and sea urchins (e.g. large scale of losses
of Diadema; Lessios et al. 1984). Understanding Increasing human populations, and their growing
the impacts of disease on biodiversity of large resource demands, are exacerbating the drivers
interconnected systems of highly mobile of infectious disease emergence detailed above.
organisms (i.e. crustaceans, marine fishes and Adding to these pressures are the impacts of
mammals) is more difficult. Additionally, diseases climate change and associated shifts in species
have had large impacts on both cultured and wild range, as well as the pathogens for which they
harvests of commercially important species, such may serve as a host or reservoir. For example,
as salmon [e.g. Ichthyophonus infection in marine ecological niche models incorporating climate
and anadromous fish (reviewed in McVicar change scenarios for 2050 have suggested that
2011; Burge et al. 2014) and viral infections in the habitat range and distribution of the bat
Atlantic and Pacific salmon (reviewed in Kurath & reservoir species for henipaviruses will expand,
Winton 2011)], abalone (e.g. withering syndrome; increasing human disease risk (Daszak et al. 2013).
Friedman et al. 2000), and crustaceans (e.g. These risks may be compounded by increasing
protozoan infections of natural populations movement of species through trade and travel

144 Connecting Global Priorities: Biodiversity and Human Health

and the evolution of a more suitable habitat for Similarly, many neglected infectious diseases
invasive alien species. have an animal link. For example, echinococcosis,
a zoonotic pathogen transmitted from a dog
/ei?ht of the eNiden;e and further tapeworm, causes 200 000 human cases each year,
resear;h needs costs an estimated US$ 2 billion in losses annually
to the global livestock industry, and infects a range
• Research to date has shown strong evidence of wild species (Cardona et al. 2013; Karesh et al.
for the overlapping drivers of disease emergence 2012). These examples highlight the importance
and biodiversity loss. Anthropogenic activities of disease surveillance across the species spectrum
are rapidly altering ecological and evolutionary to enable early detection or early warning systems.
systems under which hosts and pathogens While in some cases disease control measures may
operate, creating new dynamics and opportunities be harmful to biodiversity, they can also yield
for disease transmission and spread. benefits for wildlife. Mass vaccination of cattle
for rinderpest boosted wildebeest population
• Further investigation is needed around the numbers after large drops attributed to rinderpest
ecological factors (e.g. community composition, infection. Surveillance in wildlife has subsequently
abundance, etc.) affecting disease risks for humans been used to monitor rinderpest circulation
and other species in ecosystems. Disease ecology (Couacy-Hymann et al. 2005). Surveillance and
studies can provide insight on both host and reporting employing a One Health approach
pathogen dynamics. Understanding of disease may provide sentinel benefits to enable early
in an ecosystem can be best served through detection of pathogens potentially transmissible
One Health approaches that consider the links between humans, wild species, and livestock.
between humans, animals and the environment, This is especially important given chronic under-
thus providing a more integrated and broader reporting of disease in animals, including in food
understanding of disease risks as well as production, as well as changing ecological factors
prevention and control strategies. from climate change (de Balogh et al. 2013; Pinto
et al. 2008).
• Environmental impact assessments (EIAs)
provide useful tools to guide risk prevention and In order to move from the currently reactive
mitigation. Incorporating health risks into EIA response to infectious disease emergence and
processes can provide a more robust evaluation of spread, we must also go a step further to address
risks, including the high financial cost of potential the underlying drivers of disease emergence, many
disease emergence and outbreaks. Disease may which also overlap with drivers of biodiversity loss
also have significant impacts on ecosystems (e.g. (FAO 2013; Karesh et al. 2012; CBD 2012). This
to wild species and their provision of ecosystem requires an integrated effort around ecosystems,
services) in addition to human health. human, and animal health, rather than a siloed
one-species or one-discipline perspective. A One
3.2 One Health approach to drivers of Health or ecohealth approach that considers
infectious diseases the links between humans, animals (domestic
and wild), and the environment can improve
The integral infectious disease connections
understanding of infectious disease drivers and
between domestic animals, humans and
dynamics and move from response to prevention
ecosystems are exemplified by the highly
measures (FAO 2013; Karesh et al. 2012). Given
pathogenic avian influenza (HPAI) H5N1
the high costs of disease emergence events (for
panzootic. Evolving from a low-pathogenic
example, the 2003 outbreak of SARS cost the
strain, intensive poultry production, paired with
global economy an estimated US$ 30 billion) and
inadequate biosecurity, enabled the emergence
significant public health impacts (over one billion
and spread of H5N1 among poultry flocks,
cases of infectious diseases annually), both the
geographies, and species, including infection
economic and health arguments for tackling root
of wild birds and humans (Karesh et al. 2012)

Connecting Global Priorities: Biodiversity and Human Health 145

 causes of disease emergence drivers may directly pathogens of major human health relevance. By
and indirectly serve to protect biodiversity (Karesh closing these gaps we will improve our ability
et al. 2012). to identify synergies between biodiversity
and net human infectious disease risk burden
Moreover, given that health and land management where they exist, and move to a predictive,
decisions are rarely made on the basis of a single impact-based framework. While EIAs may be
pathogen, we need to move towards a multiple commonly employed for potential environment-
pathogen approach and increase our focus on modifying projects, also applying health impact

Box 3: Sentinel surveillance opportunities for the prevention of Ebola outbreaks

The long-running and highly disruptive human Ebola outbreak in West Africa (responsible for >25
000 reported human cases between December 2013 and early April 2015) demonstrates the
public health challenge posed by the Ebola virus. Despite global attention and response, over
fteen months into the outbreak the initial source of the outbreak had still not been de nitively
identi ed (WHO 2015). While the number of new cases had shown signs of decline as of early
April 2015, intense transmission was continuing in parts of Guinea and Sierra Leone. Prior Ebola
outbreaks in humans, and a concurrent outbreak in the Democratic Republic of Congo beginning
in August 2014, have been linked to the hunting or handling of wild animals, with subsequent
human–human transmission (Rouquet et al. 2005; Feldmann and Geisbert 2011). Some bat species
are the suspected natural reservoir for the virus and are thought to harbour it without symptoms.
Investigations of wild animal carcasses have detected infection and mortality in chimpanzees, gorillas
and duikers, suggesting that they may serve as intermediate hosts for potential human spill-over
(Rouquet et al. 2005). Ebola virus has also been recognized as causing severe declines in great ape
populations, especially critically endangered wild lowland gorilla troops (Leroy et al. 2004; Olson et
al. 2012).

Ebola virus outbreaks in humans are typically sporadic, presenting a challenge for ongoing detection
and monitoring (Leroy et al. 2004). Data generated from the Animal Mortality Monitoring Network
in Gabon and Republic of Congo and subsequently the United States Agency for International
Development (USAID) Emerging Pandemic Threats PREDICT programme suggest that surveillance for
Ebola virus circulating in wildlife may enable early detection or prevention of Ebola virus outbreaks
in humans (Rouquet et al. 2004; Olson et al. 2012). Finding fresh wild animal carcasses had been
viewed as a food resource and a sign of good fortune for some hunting communities, but poses risks
for human transmission (Karesh and Cook 2005). To manage and reduce risks from Ebola virus spill-
over, reporting of deceased or sick animal sightings by hunters and foresters can provide important
sentinel bene ts for public health and conservation monitoring, informing opportunistic sampling
by trained eld teams who can respond to reported morbidities and mortalities in wildlife with
sampling and testing e orts (Rouquet et al. 2005; Olson et al. 2012). Additionally, non-invasive
great ape faecal sampling may provide a cost-e ective surveillance method and provide data on
Ebola virus exposures and survival to bene t conservation strategies (Reed et al. 2014). This One
Health approach, paired with sharing of information on Ebola virus detection across health and
wildlife authorities and local hunting communities, allows for targeted early detection e orts and
implementation of preventive measures.

146 Connecting Global Priorities: Biodiversity and Human Health

assessments – including wildlife disease risk highlights, public health infrastructure globally is
analyses – can provide a more full understanding largely reactive, with preventive efforts frequently
of potential disease risks to people, animals and hampered by limited knowledge about the source
the environment (Karesh et al. 2012). of disease (as also exemplified by the unknown
animal–human transmission pathway for the
3.3 Economic impacts Middle East Respiratory Syndrome (MERS-CoV)
and the pathogens harboured in our environment
The high economic burden of disease – which that could be detrimental to humans. However,
has the potential to grow as anthropogenic recent studies suggest that approximately three
activities increase risks of disease emergence and quarters of recently emerging diseases in humans
globalization enables rapid spread – may hinder have come from wildlife, with most of them caused
development progress. Reactive disease control by viruses, and thus provides a starting point
efforts have proven vastly expensive, as seen with for predicting and preventing future emergence
SARS in 2003 (US$ 30–50 billion), Nipah virus efforts (Jones et al. 2008; Taylor et al. 2001). The
in 1998 (over US$ 500 million) and many other cost of detecting 85% of viral diversity in mammals
recent disease outbreaks, and pandemics have has been estimated at US$ 1.4 billion, or US$140
been identified as having potentially catastrophic million per year over ten years (Anthony et al.
impacts that are global in scale (World Bank 2013). While this represents a significant sum, it
2012). Over the past two decades, the cost of is only a small fraction of the cost of an emerging
emerging diseases alone (in humans) has reached diseases event and its early detection may enable
the hundreds of billions of dollars, and regionally actions to prevent spill-over of some pathogens
endemic diseases have persistent financial from animals to humans. Furthermore, routine
implications, often to low- or middle-income disease surveillance of animals may provide
populations (Karesh et al. 2012). While emerging sentinel benefits for humans for early detection
diseases may have acute costs from short-term of both infectious and non-infectious (e.g. heavy
outbreaks, they also have the potential to become metals in ecosystems) health risks.
established in human populations and yield long-
term costs. While pathogens causing disease The efficiency gains of a One Health approach
in humans are primarily the focus of human to zoonotic disease were recently highlighted in
infectious disease efforts, even non-zoonotic a report by the World Bank (2012) which also
diseases in livestock can severely threaten health highlighted the limited investments in One Health
and livelihoods of smallholder farmers through at present. Specifically, it noted very low actual
loss of income and food security, and/or control investments for wildlife health surveillance are
costs. being made, and estimated that between US$ 1.9
and 3.4 billion per year were needed (over ten
Costs of disease may be borne by both the years) to bring low- and middle-income countries
international community and local communities up to WHO and OIE standards to support more
affected by disease-related disruptions. For integrated and prepared national human and
example, based on UN estimates over US$ 600 animal health systems. Many low-income nations
million are needed to end the Ebola outbreak in are also biodiversity-rich although public health
West Africa, which began in December of 2013 infrastructure is poor, creating “hotspots” for
but was not detected by health authorities until disease emergence (see infectious disease chapter
March of 2014 (Baize et al. 2014). In addition in this volume and Jones et al. 2008). As we move
to the direct costs of response and control, the toward the SDGs, these should be considered
outbreak has the potential to yield extremely necessary investments for the reduction of the
high indirect costs, with travel, trade, and other health burden. In addition to human health
productivity also gravely affected and resources benefits, biodiversity conservation efforts can also
directed to fighting Ebola, potentially at the cost benefit from a more integrated disease surveillance
of treating other health threats. As the Ebola crisis approach. For example, rabies is a neglected

Connecting Global Priorities: Biodiversity and Human Health 147

 disease concern for humans as well a mammalian prevention of new cases, but dedicating a small
domestic animals and wildlife, killing over 50 000 portion of funds to preventing future disease
people annually worldwide, necessitating ongoing emergence could yield downstream cost savings.
vaccination and/or population control methods
in domestic animals, and causing major declines To tackle the issues described above requires a
in some wild canid populations (e.g. African highly collaborative and interdisciplinary, systems
Wild Dog and Ethiopian Bale Wolf populations). approach. But, the big question is, where to start?
Moreover, disease spill-over is not one-directional; There is currently no reliable toolkit to accurately
wild and domestic animal populations may acquire determine which of the candidate infectious agents
disease directly from human contact. Integrated will emerge as pathogens. Given limited resources
surveillance and control campaigns may be cost- and millions of potential species and billions of
effective means for the early identification of potential strains of micro-organisms, starting
threats before they harm humans, domestic efforts might be targeted to detecting pathogen
animals, or wild species (Machalaba and Karesh families that are known to be highly pathogenic to
2012). humans and other species and taking preventive
measures, and refining risk analyses for wider
pathogen pools as more knowledge is generated.
3.4 Systems approach and collaboration
While most emerging diseases originate in In light of this evidence, measures and policies to
wildlife, sustained infections are commonly reduce risk of spill-over should include:
transmitted among humans or through a domestic
animal connection (Kock 2014). For example, • On a precautionary principle, avoidance of
HIV originated in non-human primates, but high-density monoculture agriculture and human
its principal ongoing transmission source for activity/settlement adjacent to highly biodiverse
new infections is human–human. However, ecosystems (especially urban centres, mining,
given the population impacts of HIV and other industrial and intensive livestock systems).
diseases that have emerged from wildlife, there
are opportunities to move upstream toward • Utilization of an ecological or “One Health”
more preventive efforts for future disease while approach to disease, rather than a simplistic “one
still focusing on mitigating impacts of current germ, one disease” approach to provide a richer
ones. Vector-borne disease will always be a understanding of human, animal and environment
challenge for control from ongoing movement health links.
across boundaries (but it is the vector, and not
wild host, which matters here) and attempts to
• High biosecurity of all industrial and intensive
animal and plant agriculture, and more judicious
eliminate vectors are frequently ineffective or
or prudent use of antimicrobial agents in both
lead to unintended and detrimental ecological
human and animal medicine and food production
consequences. Despite this, the main concern
systems to reduce selection pressure for evolution
related to biodiversity and emerging disease
of resistant strains.
remains the spill-over of microorganisms from
wildlife into human-modified landscapes where
the organisms occasionally evolve into pathogens
• More resilient diverse agriculture and
sustainable harvesting systems. In the case of the
(e.g. corona and influenza viruses). Importantly,
latter some species are high risk for pathogens
the evolution of these pathogens is largely driven
and should not be included in the human diet,
by the human system itself (landscape, domestic
e.g. non-human primates given their high
animals, artificial habitats, behaviour) and through
genetic relatedness to humans (additionally, they
peri-domestic wild species that have adapted to
constitute an unsustainable protein source). For
the modified landscape (Kock 2013; Jones et al.
example, the origin of the 2014 human Ebola
2013). Infectious disease funding streams are
outbreak in the Democratic Republic of Congo
currently heavily directed toward human–human
was linked to the butchering of an infected

148 Connecting Global Priorities: Biodiversity and Human Health

monkey. If non-human primates are hunted and – Surveillance and risk prediction systems
consumed, these activities should be accompanied can also support risk analysis. For example,
by intensive surveillance efforts for early detection in Brazil, the Information System of Wildlife
and response to disease spill-over events. of Oswaldo Cruz Foundation is designed
to use mathematical models to build alerts
• Advances in the identification and modelling of of the occurrence of pathogens in wildlife
synthetic biological, ecological and anthropogenic with potential human involvement, with the
parameters that drive the emergence of wildlife participation of society and experts in mobile
diseases, and analysis of risk mitigation strategies. technology. Additionally, the USAID Emerging
Pandemic Threats PREDICT programme has
• Prevention of harvesting for wildlife trade and/ conducted pathogen surveillance in wildlife
or regulation for disease control in addition to in 20 countries that are “hotspots” for disease
source population sustainability. emergence and worked closely with health,
agriculture and environment ministries to
• Increased systems research to better characterize risks and interpret findings
understand the mechanism of pathogen jumping
through a One Health approach (see case study
and evolution and the effects of community
in Part III of this volume).
composition, abundance, and other ecosystem
dynamics. These measures and policies are largely outside
the competence levels of most human and
• Careful management of tourism in biodiverse
animal health systems, which in any case are
areas, in order to reduce risk of infection especially
largely reactive. Policy and implementation
where anthropophilic vectors occur (there
should involve a One Health approach to ensure
should also be measures in place to reduce the
a politically, socially and economically acceptable
possibility of introduction of pathogens into these
solution to the whole of society, and not to the
environments from people and domestic animals).
detriment of the environment.
• Development and support for the inclusion
of monitoring wildlife pathogens in national
programmes of surveillance in health, agriculture
and conservation.

• More proactive and integrated risk assessment

and analysis, to be informed and refined by
integrated infectious disease surveillance and
response measures. Analysis, monitoring and
management of infectious disease risks are
warranted for both potential conversion of natural
areas, as well as changing ecologies in urban areas
(e.g. proposed “greening” of cities, which may
change interactions between humans and other
species). Some approaches that can be leveraged
include:

– Risk analysis tools, such as the approaches

set forth in the OIE Guidelines on assessing risk
of non-native animals becoming invasive and the
OIE-IUCN Guidelines to disease risk analysis, can
ECOHEALTH ALLIANCE

provide qualitative and quantitative measures

of risk.

Connecting Global Priorities: Biodiversity and Human Health 149

MARIANA CERATTI / WORLD BANK PHOTO

8. Environmental microbial diversity

and noncommunicable diseases
1. Introduction The purpose of this section is to explore the
relationship between these worrying disease
Many countries worldwide, particularly in their trends, and defective immunoregulation
urban centres, have undergone large increases attributable to diminishing microbial biodiversity.
in the incidences of chronic inflammatory
disorders such as allergies, autoimmune diseases
and inflammatory bowel diseases (Bach 2002), 2. The ‘hygiene hypothesis’: the
all of which are at least partly disorders of updated concept
immunoregulation, where the immune system
The expression ‘hygiene hypothesis’ emerged
is attacking inappropriate targets (harmless
in 1989 and since then has had wide, often
allergens, self and gut contents respectively).
misleading, media appeal (Strachan 1989). The
Similar increases in these noncommunicable
problem has been that although based on a crucial
diseases (NCDs) are now occurring in emerging
underlying insight (that microbial experience
and urbanising economies.
modulates our immune systems) it was initially
There is also an increase in diseases associated interpreted narrowly in the context of allergic
with another consequence of disturbed disorders, and there was a tendency to assume that
immunoregulation: long-term background the relevant microbes were the common infections
inflammation manifested as persistently raised of childhood (Dunder et al. 2007; Strachan 1989).
C-reactive protein (CRP) in the absence of However, the concept has broadened so that it is
detectable medical cause. This is common in now a fundamental component of Darwinian (or
high-income countries, and is associated with evolutionary) medicine, with implications for
cardiovascular disease, metabolic syndrome, essentially all aspects of human health (Rook et
insulin resistance, obesity (Goldberg 2009; al. 2014b). The allergic disorders are only a part
Shoelson et al. 2007) and depression (Rook et of the story, and neither hygiene nor the common
al. 2014b; Valkanova et al. 2013). Finally, some childhood infections necessarily play an important
cancers that are increasing in prevalence are also role. For this reason, more recent terminology
associated with poorly controlled inflammation now employs terms such as the biodiversity
(e.g. cancer of the colorectum, breast, prostate, hypothesis (von Hertzen et al. 2011a) or the Old
classical Hodgkin’s lymphoma and acute lymphatic Friends mechanism (Rook et al. 2014b) to refer to
leukaemia of childhood) (Rook and Dalgleish situations where changing patterns of microbial
2011; von Hertzen et al. 2011b). exposure, in concert with changing diets, are

150 Connecting Global Priorities: Biodiversity and Human Health

contributing to diminished immunoregulation, Some soil spore-formers germinate and replicate
and to increased incidences of immunoregulatory in the human gut (Hong et al. 2009). Horizonal
disorders. gene transfer from environmental microbiota
to symbiotic microbiota has been documented,
Earlier controversy surrounding this topic may be although transfer between microbiota where
considerably reduced when the differing roles of donor and recipient both inhabit the gut is more
major functional and evolutionary categories of common (Smillie et al. 2011).
organism are taken into account.
å ,he z;roOd{ infe;tions parti;ularlQ
2.1 Categories of organisms ;oEEon Nirus infe;tions of ;hildhood

1 ,he z'ld{ infe;tions Recently acquired (after Neolithic revolution)

because they either kill or immunize, and so could
Co-evolved with humans (Comas et al. 2013; not evolve or persist in small hunter-gatherer
Linz et al. 2007; Wolfe et al. 2007). Modulate groups because a large enough population is
the immune system so they can persist for life in required for susceptible individuals to persist
small hunter-gatherer groups without killing the (Wolfe et al. 2007). Therefore humans did not
host, or being eliminated by the immune system. co-evolve with them as down-regulators of the
Progressively eliminated by modern medicine immune system, and epidemiological studies have
(Helicobacter pylori, blood and gut helminths etc.). confirmed that the crowd infections do not protect
Known to regulate the immune system and to act children from allergic disorders (Benn et al. 2004;
as ‘Treg adjuvants’: they encourage development Bremner et al. 2008; Dunder et al. 2007) and in
of the regulatory T lymphocytes (Treg) that fact often trigger them (Yoo et al. 2007).
regulate the immune system (Babu et al. 2006;
Correale and Farez 2013). Therefore, using this simple functional
classification it is possible to make a number of
ã +QEbioti; Ei;robiotas well-documented statements.

Co-evolved with humans. Loss of diversity in i) The Old infections and the commensal
modern urban settings, due to caesarean delivery, microbiotas (as well as their supplements, as yet
lack of breast feeding, antibiotics (Rook et al. poorly defined, from animals and the environment)
2014b), and increasing uniformity of diet (Khoury have potent immunoregulatory effects with well-
et al. 2014; Thorburn et al. 2014). Known to studied and documented molecular pathways,
drive development and regulation of the immune summarized in the next section (reviewed in Rook
system (Round and Mazmanian 2010). et al. 2014b).

3 +uppleEents to the sQEbioti; ii) The Old infections are rapidly and progressively
Ei;robiotas froE the natural eliminated by modern medicine and lifestyles.
enNironEent
iii) The biodiversity of the microbiotas is restricted
Major differences exist between hunter-gatherer, by the modern lifestyle.
traditional rural and urban gut microbiotas (De
Filippo et al. 2010; Yatsunenko et al. 2012). In iv) Exposure to the Crowd infections should be
an experimental model, exposure to the outdoor avoided rather than promoted.
environment increased firmicutes, particularly
lactobacilli (which produce short-chain fatty acids Therefore, depletion of categories 1), 2) and 3) is
that have anti-inflammatory effects), whereas relevant to changes in regulation of the human
rearing in the indoor environment led to increased immune system, whereas depletion of category
expression of inflammatory molecules in the gut 4) has not occurred in urban populations (except
epithelium (Lewis et al. 2012; Mulder et al. 2009). where an efficient vaccine has been deployed)

Connecting Global Priorities: Biodiversity and Human Health 151

 and is in any case not associated with changes inappropriate immune response occur they result
in immunoregulatory circuits. Indeed, these in allergy, autoimmune disease or inflammatory
infections often act as triggers of allergy or bowel disease respectively. The immune system
autoimmunity (Yoo et al. 2007). The original has a number of complex mechanisms, known
formulation of the hygiene hypothesis focused collectively as immunoregulation, to suppress
attention on the crowd infections, but this was unwanted responses. While a full exploration of
an error, and the protection against allergic this topic falls outside the scope of this chapter, it
disorders attributed to the presence of older is important to note that the immunoregulatory
siblings (Strachan 1989), and assumed by many at effects of categories 1, 2 and 3 are well documented.
that time to be a protective effect of the childhood Old infections (such as helminths) have been
virus infections, is now attributed to enhanced shown to drive immunoregulation in humans
transmission of microbiota (Penders et al. 2013). (Babu et al. 2006; Correale and Farez 2013), and
to block or treat animal models of numerous
2.2 Lifestyle factors that reduce chronic inflammatory conditions (reviewed
exposure to microbial biodiversity in Osada and Kanazawa 2010). Molecular
structures responsible for immunoregulation are
While modern medicine tends to eliminate the being identified (Grainger et al. 2010; Harnett
Old infections, lifestyle factors in high-income et al. 2010; Kron et al. 2012). Regulatory T cells
urban settings reduce exposure both to maternal (Treg), provide one important immunoregulatory
microbiota and to organisms from the natural mechanism. When Argentinian multiple sclerosis
environment (categories 2 and 3 above). Delivery (MS) patients become infected with helminths,
by caesarean section, lack of breast feeding and the disease stops progressing and circulating
excessive use of antibiotics in early childhood all myelin-recognising regulatory T cells (Treg)
delay, reduce or modify accumulation of essential appear in the peripheral blood (Correale and Farez
microbiota (reviewed referenced in Rook et al. 2007), indicating that the helminths act as Treg
2014a). The protective effect of cleaning a child’s adjuvants. Thus some helminths can be shown to
dummy/pacifier by sucking it, and immediately specifically expand Treg populations (Grainger et
replacing it in the baby’s mouth is an elegant al. 2010), or to cause dendritic cells (DC) to switch
illustration of the need for trans-generational to regulatory phenotypes that preferentially drive
transmission of microbiota (Hesselmar et immunoregulation (Hang et al. 2010; Smits et
al. 2013). al. 2005).

2.3 Links to socioeconomic status (SES) Gut bacteria are also able to do this. A
polysaccharide from Bacteroides fragilis, commonly
The factors mentioned in the previous paragraph present in the human gut, can expand Treg
might be exacerbated in families of low SES, who populations (Round and Mazmanian 2010), as
tend to eat unvaried fast-food diets and more can some members of clusters IV and XIVa of the
highly processed foods that lack any trace of soil genus Clostridium (Atarashi et al. 2011), some
and its microbes, whose homes are less likely to lactobacilli (Poutahidis et al. 2013), and very
include gardens, and who lack access to travel, probably unidentified organisms from the natural
overseas holidays and rural second homes (Rook environment, discussed later (Lewis et al. 2012).
et al. 2013). Some of these effects are mediated via short chain
fatty acids (SCFA) that act on G-protein-coupled
2.4 Immunoregulatory pathways driven receptors (GPCR) (Thorburn et al. 2014). SCFA are
by organisms of categories 1, 2 and 3 generated by microbiota that ferment dietary fibre.
The immune system is potentially dangerous if
It seems unlikely that we will want to bring
it attacks inappropriate targets such as harmless
back all the Old infections, unless we create a
allergens in air or food, the host’s own tissues, or
‘domesticated’, perhaps genetically modified
essential gut microbiota. When these three types of

152 Connecting Global Priorities: Biodiversity and Human Health

helminth that could be administered to all children microbiota are beginning to be published
(Parker and Ollerton 2013). On the other hand we (Messaoudi et al. 2011).
should be able to compensate for loss of the Old
infections by optimizing exposure to categories Therefore, in the context of this chapter, crucial
2) and 3) the microbiotas and their supplements questions are: 1) are the human microbiotas losing
from the natural environment. From a medical biodiversity? And, if so: 2) To what extent is reduced
point of view the question is whether we can biodiversity of human microbiotas a consequence
compensate for loss of the Old infections and of changes in the biodiversity of the environment
depletion of our microbiotas by restoring those in which we live? 3) What are the implications for
microbiotas and restoring inputs from a carefully human health?
maintained and biodiverse natural environment.
4. Loss of biodiversity:
3. Commensal microbiotas and consequences for human health
environmental biodiversity Reduced gut microbial biodiversity is often found
From a biological perspective, humans are not to associate with poor control of inflammation.
individuals. We are ecosystems. Up to 90% of our Mice with lower microbial diversity have more
cells are microbial, and the various microbiotas, biomarkers of inflammation (Hildebrand et al.
particularly the gut microbiota, contain at least 2013). Gut microbiota of limited diversity is also
100 times more genes than does our human characteristic of human inflammation-associated
genome (Wikoff et al. 2009). Consequently, conditions such as obesity and inflammatory
approximately 30% of our metabolome (small bowel disease (Rehman et al. 2010; Turnbaugh
molecules circulating in the blood) are products et al. 2009). Similarly, diminished microbiota
of enzymatic processes encoded in microbial DNA biodiversity in institutionalized elderly people
rather than in the human genome (Wikoff et al. correlates with diminished health and raised
2009). We now know that the microbiotas play levels of peripheral inflammatory markers such
a role in virtually all aspects of our physiology, as interleukin 6 (IL-6) (Claesson et al. 2012).
in addition to priming the immune system and
its immunoregulatory pathways as described in The same is probably true for skin disorders
the previous section. While there is no such thing (Zeeuwen et al. 2013). There is an abnormal
as a germ-free human, work in experimental microbiota and reduced diversity on skin subject
animals has revealed that the microbiota influence to eczema, with a tendency to return to greater
development of the brain, hypothalamo-pituitary- diversity following effective treatment (Kong
adrenal axis (HPA), gut, bones etc. (Gilbert et al. et al. 2012), and similar findings in psoriasis
2012; McFall-Ngai et al. 2013). The microbiota (Fahlen et al. 2012). It has been suggested that
also influences energy retrieval from food sources throughout human evolution the skin microbiota
and the likelihood of obesity, cardiovascular have included ammonia-oxidising bacteria (AOB)
disease, metabolic syndrome and type 2 diabetes that would help to explain the presence of large
(Tremaroli and Backhed 2012). In animals, the quantities of ammonia and nitrate in human
microbiota modulate brain development and sweat (Whitlock and Feelisch 2009). The AOB
responses to psychosocial stressors (Bailey et al. convert this to rapidly absorbed nitrite and nitric
2011; Heijtz et al. 2011), and human experiments oxide (NO) that regulates blood pressure and
have shown that the gut microbiota influences the immune system. AOB are very sensitive to
aspects of cognition involved in human emotion triclosan and alkylbenzene sulfonate detergents,
and sensation (Tillisch et al. 2013). This finding so they are absent from human skin in modern
may have significant implications for better high-income settings.
understanding mental health, and attempts
to treat psychiatric states by modulating the

Connecting Global Priorities: Biodiversity and Human Health 153

 Further information and references on some å.1.1 ealth beneÍts of exposure to
of the conditions listed in this paragraph are farEs and farEland
described below.
Exposure of the pregnant mother or infant to
the farming environment protects the child
4.1 To what extent is reduced against allergic disorders and juvenile forms of
biodiversity of human microbiota inflammatory bowel disease (Radon et al. 2007;
a consequence of changes in the Riedler et al. 2001; Timm et al. 2014). This
biodiversity of the environment in protection appears to be at least partly attributable
which we live? to airborne microbial biodiversity assayed in
Humans and other mammals obtain much of their children’s bedrooms (Ege et al. 2011). Similarly
microbiota from their mothers during delivery, mere proximity to agricultural land rather than to
and via breast milk (which is not sterile) and urban agglomerations increased the biodiversity
from family members. However many, probably of skin microbiota, reduced atopic sensitization
all animal species (including humans), obtain and increased release by blood cells of IL-10, an
components of their microbiota from soil (Mulder anti-inflammatory mediator (Hanski et al. 2012).
et al. 2011; Troyer 1984). It is an interesting
possibility that geophagy (the eating of earth) å.1.ã FarE aniEals and do?s
by babies and infants is an evolved strategy for Some of the relevant microbiota come from
the uptake of soil organisms. This is manifested animals. Contact with cows and pigs protects
as the ‘oral’ phase, when all babies put whatever against allergic disorders (Riedler et al. 2001;
they can reach into their mouths. The quantities Sozanska et al. 2013). Contact with dogs, with
of soil and faecal matter that can be ingested by which humans have co-evolved for many millennia
human babies with access to these materials (for (Axelsson et al. 2013; Thalmann et al. 2013), also
example in an African village) are astonishing protects from allergic disorders (Aichbhaumik et
(Ngure et al. 2013). Circumstantial evidence that al. 2008; Ownby et al. 2002), and people share
humans acquire important microbial biodiversity their microbiota via dogs (Song et al. 2013), which
from the environment comes from studies of the also greatly increase the microbial biodiversity of
effects of contact with farms, animals, and green the home (Dunn et al. 2013; Fujimura et al. 2010).
spaces discussed below. Exposure to high levels of bacterial and fungal

CHRISSY BISCH / FLICKR

154 Connecting Global Priorities: Biodiversity and Human Health

components in house dust was associated with interferon and major histocompatibility complex
diminished risk of atopy (the tendency to develop class I (Mulder et al. 2009). Moreover, the piglets
allergic sensitisation to environmental allergens) deprived of environmental exposure had reduced
and wheeze, though the origins of the organisms numbers of regulatory T cells and a predisposition
was not ascertained (Karvonen et al. 2014; Lynch to making antibody following introduction of a
et al. 2014). In a developing country, the presence novel food (Lewis et al. 2012). This represents
of animal faeces in the home correlated with an elegant model of the way that human babies
better ability to control background inflammation are reared in high-income settings with minimal
(CRP levels) in adulthood (McDade et al. 2012b), contact with environmental biodiversity, and
and in Russian Karelia (where the prevalence parallels the rising incidence of food allergies and
of childhood atopy is 4 times lower, and type 1 other immunoregulatory abnormalities in such
diabetes is 6 times lower than in Finnish Karelia), babies.
house dust contained a 7-fold higher number
of clones of animal-associated species than was Thus the natural environment supplements
present in Finnish Karelian house dust (Pakarinen and modulates the microbiota in a way that
et al. 2008). is relevant to regulation of the immune
system. This area is currently under-investigated,
particularly the role of spore-forming bacteria
å.1.3 reen spa;e
that are usually considered to be soil organisms,
Living close to green spaces reduces overall but which can germinate and replicate in the
mortality, cardiovascular disease, and depressive human gut (Hong et al. 2009; discussed and
symptoms, and increases subjective feelings of referenced in Rook et al. 2014b). It is important
well-being (Aspinall et al. 2013; Dadvand et al. to note that we do not currently know how
2012; Maas et al. 2006; Mitchell and Popham much of the human microbiota is derived from
2008). This health benefit has been attributed the microbial environment, though work on this
to multiple factors including exercise, exposure point is in progress, and the overlaps between
to sunlight and psychological effects. A detailed gut and root microbiotas have been discussed
review and critique of these explanations has (Ramirez-Puebla et al. 2013). However it has been
been published elsewhere (Rook 2013). Recent demonstrated that germ-free mice can develop a
work suggests that the health benefits are not functioning gut microbiota following exposure to
attributable to exercise alone (Lachowycz and microbial communities from soil, and from other
Jones 2014; Maas et al. 2008), and in light of environmental sources, though these organisms
the clear-cut observations on exposure to farms get displaced by more mouse-adapted strains
and animals, exposure to diverse environmental when co-housed with mice carrying normal mouse
microbiota is becoming the most likely explanation. microbiota (Seedorf et al. 2014). A recent study,
For example, the gut microbiota of United States using novel computational strategies was able to
citizens is different from that of Amerindian assemble the complete genome of 238 intestinal
hunter-gatherers and Malawian rural farmers, bacteria, 76% of which were previously unknown
and strikingly less biodiverse (Yatsunenko et al. (Nielsen et al. 2014).  Similar methods have not,
2012). Particularly relevant experiments have to our knowledge at the time of publication,
been performed with piglets, showing that when been applied to the microbiota of the natural
maintained with the sow in a field they developed environment.
a characteristic gut microbiota rich in Firmicutes,
particularly Lactobacilli. On the other hand similar
å.1.å FerEented foods and beNera?es
piglets maintained with the sow on the same diet,
but in a clean indoor environment developed a gut Fermentation of vegetables (Breidt et al. 2013;
microbiota that was deficient in Firmicutes, and Swain et al. 2014), meat (Leroy et al. 2013) and
biopsies of the gut epithelium revealed increased beverages (McGovern et al. 2004) was another
expression of inflammatory genes such as Type 1 source of human intake of microbiota from the

Connecting Global Priorities: Biodiversity and Human Health 155

 environment. Chemical analyses of residues in their microbiota from environmental microbes
pottery reveal that some of these methods were of genes that enable the catabolism of novel
in use at least 9000 years ago (McGovern et al. seaweed-associated carbohydrates (Hehemann
2004) and probably a great deal earlier (McGovern et al. 2012). Thus the adaptability of the human
2009). A mutation in alcohol dehydrogenase 4 microbiota depends upon appropriate contact
that increased the efficiency of alcohol metabolism with potential sources of genetic innovation
appears to have arisen in distant ancestors of and diversity, and might therefore be threatened
mankind about 10 million years ago, perhaps by loss of biodiversity in the gene reservoir of
triggered by consumption of fruit that had environmental microbes.
fermented after falling to the ground (Carrigan et
al. 2014). Lactic fermentation of vegetables (e.g. 4.2 Life history plasticity, and
sauerkraut, kimchi, gundruk, khalpi, sinki etc) microbiota as epigenetic inheritance
or of meat (for example the Eskimo fermented
fish, walrus, sea lion and whale flippers, beaver Evolutionary biologists consider that life-history
tails, animal oils and birds) adds nutritional and variables (such as litter size, birth weight, age at
microbiological diversity to the diet (Leroy et sexual maturity, adult weight and height) can be
al. 2013; Selhub et al. 2014; Swain et al. 2014). crucial developmental adaptations to a changing
Fermentation increases the content of vitamins, environment. However these life history variables
lactoferrin, bioactive peptides and phytochemicals can change stepwise over several generations
such as flavonoids which may in turn modulate even when the driving environmental change
our own intestinal microbiota (Lu et al. 2013). The remains constant after it has first occurred (Price
increasing interest in modern fermented foods, et al. 1999; Wells and Stock 2011). For example,
and in sourcing new probiotics from fermentation improved nutrition in a colony of macaques
processes and from the environment is exploiting led to progressive increases in female adult
the fact that human metabolism has evolved in weight (and to increases in the birth weights of
the presence of such organisms and might have offspring) over 5 generations (Price et al. 1999).
developed a need for their presence. How is this mediated? Clearly a given genotype
would be expected to yield a fixed phenotype
under fixed conditions. Therefore epigenetic
4.1.5 Horizontal gene transfer
and developmental mechanisms are usually
In addition to exchange of whole organisms with invoked to explain these generational effects.
animals and the natural environment, we need to Such explanations are made more convincing
consider horizontal gene transfer (HGT) (Smillie when the microbiota are considered as part
et al. 2011). This is common between bacteria and of the epigenetic inheritance of the infant.
recent work has revealed the existence of a global (Interestingly some products of the microbiota
network of HGT between members of the human exert anti-inflammatory effects by inhibiting
microbiota, even between phylogenetically very histone deacetylases (HDACs), so the microbiota is
divergent bacteria separated by billions of years directly involved in epigenetic immunoregulation
of evolution. Exchange was related to similarity (Thorburn et al. 2014)). Dietary effects will alter
of ecology rather than phylogeny. Examples the microbiota, which when passed on to the next
include the horizontal transfer of genes encoding generation will programme the immune system
the antibiotic resistome from soil microbes so that it is different from that of the mother,
(Forsberg et al. 2012). This is worrying because and that immune system will then interact with
huge increases in antibiotic resistance genes are further environmentally-driven changes to the
being detected in the microbiota of farm waste as microbiota.
a result of antibiotic use in animal husbandry (Zhu
et al. 2013). However HGT also plays essential
beneficial roles. Consumption of seaweed by
Japanese people induces horizontal transfer to

156 Connecting Global Priorities: Biodiversity and Human Health

4.ã.1 etriEental Ei;robiota in 5.1.1 'besitQ Eetaboli; sQndroEe and
unhealthQ buildings tQpe ã diabetes.
The previous paragraphs emphasise that humans The gut microbiota of lean and obese human
evolved in a natural environment and in contact individuals differ, and can transfer the tendency
with animals. Until recently even our homes to leanness or adiposity to germ-free mice
were constructed with timber, mud, animal hair, maintained on a standard diet (Turnbaugh et
animal dung, thatch and other natural products, al. 2006). The mechanisms by which microbiota
and ventilated by outside air. By contrast, modern influence adiposity have been reviewed (Karlsson
buildings are constructed with synthetic materials, et al. 2013). They include effects on efficiency of
plastics and concrete, while the timber and energy harvest from ingested food, and complex
cardboard are treated with adhesives and biocides, effects on the function of the body fat-regulatory
and ventilated by air conditioning systems. When circuits that involve the central nervous system,
these modern structures degrade, or become leptin, neuropeptide Y, proglucagon and brain-
damp, or accumulate condensation in cavity walls, derived neurotrophic factor (Schele et al. 2013a;
they do not become colonized with the bacterial Schele et al. 2013b). Some of these neuroendocrine
strains with which we co-evolved. They harbour a phenomena may be secondary to central nervous
low biodiversity, and become habitats for unusual system effects of inflammatory mediators such
strains that we did not encounter during our as IL-1 and IL-6 (Schele et al. 2013a), and indeed
evolutionary history, some of which synthesise chronic inflammation contributes to insulin
toxic molecules that we are unable to inactivate resistance and obesity via several pathways
(Andersson et al. 1998; Sahlberg et al. 2010). (Shoelson et al. 2007). Anti-inflammatory
Some examples of “sick building syndrome” have Foxp3+ regulatory T cells (Treg) in abdominal fat
been tentatively attributed to prolonged exposure control the inflammatory state of adipose tissue,
to these inappropriate airborne microbiota and the abundance of Treg in abdominal fat is
(Andersson et al. 1998; Sahlberg et al. 2010). inversely related to insulin resistance (Feuerer et
al. 2009). A diet of western fast food aggravates
the immunoregulatory deficit, promotes a low
5. Commensal microbiota and
ratio of Treg to Th17 cells (pro-inflammatory),
noncommunicable diseases and drives abdominal adiposity in humans and
As outlined above, as societies become westernized mice (Poutahidis et al. 2013). This diet was shown
and urbanized, there are striking increases in epidemiologically to lead to obesity (Mozaffarian
chronic inflammatory disorders (autoimmunity, et al. 2011). Fatty diets and the accompanying
allergies and inflammatory bowel diseases (IBD)) dysbiosis can also increase gut leakiness and so
that are at least partly attributable to defective increase uptake of pro-inflammatory products
immunoregulation, in which the gut microbiota such as endotoxin (Cani et al. 2008).
plays a major role (reviewed in Rook et al. 2014b).
Most of the epidemiological evidence applies to The adipogenic and pro-inflammatory effects of
these three groups of conditions, covered in the the western fast food diet can be opposed by a
previous paragraphs. probiotic (Lactobacillus reuteri) via a pathway that
depends on the simultaneous presence of a normal
However other major health problems rise in gut microbiota, and is mediated by Treg (Poutahidis
parallel with the classic trio of chronic inflammatory et al. 2013). (Interestingly, some strains of L. reuteri
disorders already mentioned (autoimmunity, used in human food production might be derived
allergies and IBD), and in these conditions also from mouse gut microbiota (Su et al. 2012)). Thus
there are reasons for implicating the microbiota, the nature and diversity of the gut microbiota,
the environment and immunoregulation. together with the poorly documented inputs of
microorganisms from the natural environment,
may have multiple metabolic, neuroendocrine and
immune-mediated effects on obesity, metabolic

Connecting Global Priorities: Biodiversity and Human Health 157

 syndrome and insulin resistance, which are all Animal models have cast much light on the
major problems of our time. links between environmental organisms,
immunoregulation, inflammation and cancer
5.1.ã an;ers asso;iated Oith poorlQ (Erdman et al. 2010). Inflammatory signals
regulated inÎaEEation from bacteria in the gut can trigger mammary,
colorectal and prostate cancers in mice (Erdman
The incidence of a number of cancers also et al. 2010; Lakritz et al. 2014). Tumourigenesis
increases in high-income urbanized settings in can be attenuated by immunoregulatory pathways
parallel with the chronic inflammatory disorders. triggered by appropriate Treg-inducing organisms
These include cancer of the colorectum, breast (Erdman et al. 2010). For example, in two different
and prostate, classical Hodgkin’s lymphoma and mouse models (one genetic, and one dietary)
acute lymphatic leukaemia of childhood (Rook mammary carcinogenesis was inhibited by
and Dalgleish 2011; von Hertzen et al. 2011b). exposure to Lactobacillus reuteri. The mechanism
Inflammation can enhance mutation (Colotta et was found to be the induction of CD25+Foxp3+
al. 2009) and so play a role in carcinogenesis, but Treg (Lakritz et al. 2014).
‘smouldering’ inflammation that is not obviously
related to any external inflammatory stimulus Thus, although excessive immunoregulation might
is common in tumours (Porta et al. 2009) and be permissive for some cancers by decreasing
releases growth factors and angiogenic factors anti-tumour immunity, there is strong evidence
that enhance growth, vascularization and that faulty immunoregulation leading to chronic
metastasis (Balkwill 2009; O’Byrne et al. 2000; background inflammation can provoke mutation
Porta et al. 2009). Interestingly non-steroidal anti- and tumourigenesis, and contribute growth factors
inflammatory agents, such as cycloxygenase-2 that favour tumour development, vascularization
(COX-2) inhibitors, reduce the risk of developing and spread. Since the microbiota plays a major
colon and breast cancer and reduce the mortality role in immunoregulation and is supplemented
caused by them (Cuzick et al. 2009). by organisms from the natural environment, it
is reasonable to postulate that changes to the
The epidemiology of the cancers that increase in pool of environmental microorganisms have
high-income settings is strikingly similar to that of consequences for the risk of such tumours.
the chronic inflammatory disorders. For instance,
age-specific incidence rates for specific cancers
5.2 Depression, reduced stress
in Asians correlate with the state of economic
resilience and poorly regulated
development of their country of residence.
Incidences are much lower in Asians living in India
LQƪDPPDWLRQ
compared to those living in the United Kingdom It is estimated that depression will become the
or United States (Rastogi et al. 2008). Another second major cause of human disability by 2030
example is acute lymphatic leukaemia, which (Mathers and Loncar 2006). Chronically raised
shows striking parallels with the epidemiological levels of inflammatory mediators are routinely
findings that gave rise to the original version of associated with risk of depression in high-income
the hygiene hypothesis (Greaves 2006; Strachan countries (Dowlati et al. 2010; Gimeno et al.
1989). A study in northern California provided 2009; Howren et al. 2009; Rook et al. 2014b;
preliminary evidence that protection from acute Valkanova et al. 2013), and the mechanisms have
lymphatic leukaemia is proportional to the number been reviewed elsewhere (Miller et al. 2013).
and frequency of social contacts (Ma et al. 2002). It should be noted that clinical administration
A large population-based case-control study (The of interferon alpha (IFN-a) commonly causes
UK Childhood Cancer Study (UKCCS)) revealed depression as a side-effect (Raison et al. 2009).
further evidence that social contacts in infancy Interestingly, one study failed to find a correlation
can reduce the risk of childhood acute lymphatic between depression and raised CRP in a low-/
leukaemia (Gilham et al. 2005). middle-income country (McDade et al. 2012a).

158 Connecting Global Priorities: Biodiversity and Human Health

In low-income settings, exposure to microbial 6.1 Better understanding the links
biodiversity is greater and inflammation is shut between microbial diversity and health
off when episodes of infection are terminated, so
Practical recommendations are hampered by
that chronic elevated biomarkers of inflammation
lack of precise information. Important areas for
are not seen (McDade 2012). Thus decreasing
further research include:
exposure to microbial biodiversity, by reducing the
efficiency of immunoregulatory circuits, is likely to a.1) What are optimal compositions of the
be contributing to the increases in depression, and microbiota? The physiological, metabolic and
reduced stress resilience in high income settings immunoregulatory roles of the microbiota are
(Rook et al. 2013). not in doubt, and constitute one of the most
rapidly expanding and exciting branches of
6. Ways forward: preliminary medical research. Nevertheless the techniques
recommendations for global and used, despite rapid progress, remain imprecise
at the species level, and in most cases it is not
sectoral policy yet possible to reliably link particular microbial
What are the practical implications of these species with health or illness. Even if we did
links between microbial exposures, microbial have this knowledge, we do not yet know how to
biodiversity, regulation of the immune system, reliably bias the composition of the microbiota
and chronic inflammatory disorders? in the desired direction. We also do not know
whether humans with different genetics and

Box 1: lostridiuE diÏ;ile a practical example of modulating gut microbiota

A gastrointestinal disorder characterized by diarrhoea and pain, caused by overgrowth of

Clostridium difficile in the colon, provides a remarkable clinical example of the crucial importance
of a correct balance of organisms within the gut microbiota, and illustrates practical ways of
correcting such imbalance. Many people carry small numbers of C. difficile in their guts, but in
some individuals antibiotic use can lead to overgrowth of this species, and to potentially life-
threatening colitis aggravated by toxin production. (The same phenomenon is commonly seen
in antibiotic-treated pet guinea-pigs (Rothman 1981)). Recently it has been observed that faecal
microbiota transplantation (FMT) is an effective treatment in about 90% of patients (Cammarota
et al. 2014). FMT involves administering faecal organisms from a normal donor (often a healthy
family member). FMT suppresses growth of C. difficile and permits re-establishment of a normal
microbiota. FMT is also undergoing trials in IBD, irritable bowel syndrome, and other chronic
inflammatory conditions, though results remain variable (Borody et al. 2013).

Three important points need to be made here. First, as we learn more about the composition of
a healthy microbiota and develop better ways of driving appropriate stable modifications of the
microbiota, so our ability to treat diverse immunoregulatory and inflammatory disorders is likely
to increase: this might also involve use of organisms from the natural environment. Secondly, we
do not yet know whether people with different genetic backgrounds, or eating different diets, will
require a different microbiota, though this is likely. Thirdly, as the number of conditions known to
be modulated by the microbiota increases, so the selection of donors becomes more difficult. For
example the material outlined in previous sections implies in addition to screening the donors
for infections and load of C. difficile, we need to be sure that the donor is not obese, or at risk for
cancer, cardiovascular disease, autoimmune disease, IBD, allergies or depression.

Connecting Global Priorities: Biodiversity and Human Health 159

 different diets require different microbiotas, b.2) Human behaviour; targeted hygiene: The
although recent evidence suggests that this is public should be taught the concept of ‘targeted’
likely. hygiene. The sound bites generated by the ‘hygiene
hypothesis’ has led to erroneous media backing
a.2) The nature of beneficial organisms from the for the notion that “we are too clean for our
natural environment. The mother, family members own good”, despite the massive health benefits
and other people are major sources of microbiota, of hygiene. The public needs to understand, for
but the epidemiological data presented above example, the difference between the dangers
provide powerful evidence to suggest that these of the gut microbiota of an uncooked chicken,
microbiota are supplemented by organisms (and and the benefits of contact with maternal
genes via horizontal gene transfer) from the microbiota, green spaces, animals and the natural
natural environment and from animals. However, environment.
these organisms have not been formally identified.
Experimental work with piglets strongly supports b.3) Antibiotics: There is strong evidence that
the view that the natural environment provides antibiotic use in childhood increases the risk of a
organisms that drive immunoregulation and wide range of chronic inflammatory and metabolic
suppress immune responses to novel foods, but disorders in childhood and later life.
again, the organisms involved have not been
formally identified. This is a priority area for b.4) Health benefits of fermented foods/
research. traditional diets: Fermentation of vegetables,
meat, oils and beverages can be traced back
many millennia, as discussed in section 4.1.4.
6.2 Mainstreaming across health- and
The fermentation process adds nutrients and
biodiversity-related sectors
microbiological diversity (Selhub et al. 2014). It
It is difficult to make clear recommendations is likely that humans have evolved a requirement
until the questions addressed in the previous for the fermenting organisms and their products,
sub-section are better defined. As such knowledge and it is widely believed that these foods provide
increases we will be able to offer more precise health benefits. Although the science is strongly
guidance on some of the relevant issues listed suggestive and most workers in the field are
below. confident that fermented foods, probiotics and
prebiotics will one day play a role in treatment and
b.1) Agricultural methods: Extensive prevention of NCDs and inflammation-dependent
monoculture and chemical use will reduce psychiatric diseases, clinical trial data with the
environmental biodiversity, and so reduce the existing preparations have been inconsistent as
adaptability of the human microbiota, which revealed in recent rigorous reviews (Frei et al.
depends upon supplementation with organisms 2015; West et al. 2015). More effort should be
from the environment, and contact with made to ‘mine’ traditional fermentation processes
potential sources of genetic innovation and for novel probiotics before the diversity of strains
diversity. However the evidence that organic is lost (Swain et al. 2014), and clinical trials should
farming increases biodiversity at the floral, be more specifically targeted.
faunal (Schneider et al. 2014) and microbial level
is suggestive but incomplete and inconsistent b.5) Food supplements: Food companies
(Sugiyama et al. 2010). The use of antibiotics in potentially have a major role to play in this
animal husbandry results in large increases in the endeavour. Too much testing of probiotics (and
abundance of antibiotic resistance genes (Zhu et al. prebiotics) has been conducted with unsuitable
2013). Not only is this inherently undesirable, but organisms (and oligosaccharides) simply
is also likely to cause changes in the composition because the company concerned has the relevant
of the microbiota. intellectual property rights, or access to a bulk
manufacturer of the strain in question. Probiotics

160 Connecting Global Priorities: Biodiversity and Human Health

KIBAE PARK / UNITED NATION PHOTO / FLICKR

have multiple modes of action. For example, when bus stops where people congregate (http://www.
immunoregulation is required, it is obviously theediblebusstop.org/). These projects are mostly
essential to test a probiotic that has that particular driven by aesthetic considerations, whereas we
property (Frei et al. 2015), rather than a strain now have medical reasons for supporting and
that acts by blocking an ecological niche in the amplifying such movements. This concept will
gut and reducing pathogen access, however useful again be facilitated when we have clear answers
this property might be in other contexts. Some to question a.2) outlined above; what is the
probiotics based on the spores of environmental optimal flora to plant? How do we encourage the
Bacillus species are also marketed for human and organisms that we want? It is worrying that use of
animal use, but we are not aware of any systematic water supplies contaminated with antibiotics on
attempt to identify other relevant environmental city parkland is changing the pattern of antibiotic
organisms (as pointed out in a.2 above), though resistance genes in the local soil, and so inevitably
such work is in progress. distorting the natural microbiota of these urban
green spaces (Wang et al. 2014).
b.6) Design of cities: The realization that much
of the health benefit of green spaces is not b.7) Interdisciplinary publications and media
attributable to exercise alone and is likely to be due attention: The health world concentrates
to exposure to microbial biodiversity leads to the its reading, research and publications in
possibility that not all green spaces need to be large medically-orientated journals while ecologists,
parks appropriate for team sports. Multiple, small, environmental engineers, soil scientists and
high quality green spaces, designed to harbour city planners disseminate their information
the optimal fauna, flora and accompanying in quite different ways. We need to encourage
microbiota, might provide a major health benefit. cross-disciplinary media attention and review
These could include roof gardens, vegetated publications.
walls, grass verges etc. In London, environmental
engineers have created “edible bus stops”, which
are small community gardens often located at

Connecting Global Priorities: Biodiversity and Human Health 161

 6.3 Giving policy-makers an idea of also easy to collect. Questionnaires suitable
tools available for assessing health, disease prevalence and
mental state are well validated. The progress in
An important consideration for policy-makers is
developing DNA sequencing and bioinformatic
that our knowledge of the microbiome is changing
techniques has been rapid, and the microbial
extremely rapidly, but the tools to perform these
composition of any sample can be determined.
analyses and their limitations are also changing
Thus it is possible to couple disease epidemiology
very rapidly. It is therefore a substantial risk that
with biodiversity measurements. Similarly high-
technologies or findings will be adopted before they
sensitivity C-reactive protein (CRP) assays are easy
are robust, leading to unstable conclusions, but at
to perform and give a good measure of background
the same time a risk that powerful technologies of
inflammation levels. At present, most studies
findings that could have large impact on people’s
have focused on bacteria, although the viruses,
lives will not be deployed in a timely fashion. This
fungi and microbial eukaryotes in general are
section describes some of these considerations.
also important components of the microbiota
and are becoming increasingly feasible to assay.
ç.3.1 ssessEent Similarly, most studies have focused on marker
There is need for interdisciplinary studies, where genes such as the 16S ribosomal RNA gene, which
epidemiologists work closely with microbiologists provide very efficient readouts of who is present
studying the microbiota of the environment in an environment, but assays such as shotgun
(plants and soil), transport systems, homes, metagenomics (which identifies all genes present in
offices and public buildings. We already know a given sample) or metabolomics (which identifies
that microbial biodiversity in a child’s bedroom chemicals including those produced by microbial
correlates with reduced risk of asthma and metabolism) are increasingly approachable and
atopy (Ege et al. 2011). It will be important to may provide a much richer picture. However,
extend such studies to other situations. For techniques that carry a risk of sequencing human
example, how does the microbial biodiversity of DNA found in a given environment must be used
an underground train line (subway) that never with more caution in relation to human research
runs above ground, compare with that of a line ethics.
that is sometimes above ground (e.g. respectively,
the Victoria and Piccadilly lines in London)? Are Appropriate environmental measurements to
there detectable differences in the proportion of correlate with the human microbiota and health
organisms from the natural environment? Are data include:
there detectable influences on the health of the
1) Assessment of airborne microbial biodiversity,
passengers? Unfortunately transport companies
perhaps including fungal and viral diversity.
and organisations are extremely unwilling to allow
In general, outdoor air and indoor air differ
such investigations. Can we make the technology
substantially from each other (Kembel et al.
cheap enough and develop a robust enough
2012), and land use can also have a large effect
database that individual families are willing and
on microbial sources in outdoor air (Bowers et al.
able to perform microbial tests of their homes,
2011), with dog faeces being a substantial input
as they may already be doing when concerned
in cities under some circumstances (Bowers et al.
about fungi? Can relevant governmental entities
2011).
play an important role by facilitating rather than
obstructing the study of public buildings and the 2) Assessment of microbial biodiversity of
effects of features of their microbiology on the homes and public places. Crowdsourcing can be
health of their inhabitants or visitors? an effective method for obtaining such samples,
Methods available especially given the high public interest in such
studies (Dunn et al. 2013).
Skin microbiota can be sampled by lightly pressing
a sterile swab on the skin. Faecal samples are

162 Connecting Global Priorities: Biodiversity and Human Health

a) Traditional versus microbiota-damaging along several dimensions including production
building materials. Studies of the effects of methods, chemical inputs, amount of washing
building materials on environmental microbes, and remaining soil, and duration of storage, all of
rather than on individual species of interest, are which likely affect the microbes.
still very much in their infancy but are urgently
needed. ç.3.ã /aQs forOard
b) Open windows versus air conditioning, and Several remedies are also available from a
propagation of microbes from open windows policy perspective. Most urgently needed are
through the rest of a building. Given increased global policies to preserve the biodiversity of
automation of window shades and/or tinting for the natural environment. These would include
energy efficiency reasons, it may also be feasible major restrictions on antibiotic misuse both in
to automate window opening at temperature- human and agricultural settings and possibly
appropriate times to facilitate microbial exchange including antibiotic remediation of wastewater;
with the outdoors. It is also unknown whether assessing the effects of agricultural and building
exposure to beneficial microbes from the outdoors, practices on microbes, perhaps including microbial
or lack of ongoing exposure to largely human- biodiversity reserves in our houses, schools and
derived microbes trapped indoors, explains more offices, and identifying and preserving reservoirs
of the links between building microbes and human of human-associated microbes in hunter-gatherer
health. communities in Africa, Pacific Islands and South
America, and ancestral reservoirs of microbes in
c) City zones with and without green spaces. If the Great Rift Valley that represent the microbial
green spaces have an effect, the effects of large heritage with which our species coevolved.
parks versus small high quality green spaces, and City planning and architectural designs that
the composition of trees, flowers and grass should optimize biodiversity of microbial exposure in
also be assessed. urban settings are also needed, including green
spaces, opportunities for contact with microbes
d) Dog parks, urban farms/petting zoos, and other from wildlife and farm animals, and modified
sources of human–animal contact. air conditioning strategies that spread beneficial
microbial diversity rather than Legionella. Finally, a
Compare farming methods: broad-scale education initiative, including citizen-
science efforts parallel to those employed by
a) Mono- versus poly-culture: Is the diversity of
American Gut (where members of the public can
crops more or less important than which crop
both act as subjects and participate in an open data
species are present? Does diversity within a
analysis effort) and MOOCs (massive open online
species, e.g. growing multiple varieties of apples
courses), as well as more traditional classroom and
together rather than a monoculture, important?
online resources aimed at children, educators,
physicians, politicians, the press, advocacy
b) Organic versus intensive chemical use. The effects
organizations, and members of the general public
of agricultural chemicals, including herbicides and
will be needed both to communicate the results
pesticides, on leaf microbes or on soil microbes
obtained to date in this exciting field and to lay
that are known to be immunomodulatory in
the groundwork for appropriate assimilation
humans are largely unknown.
and deployment of new findings in this rapidly
c) Food in traditional farmers’ markets versus evolving field.
modern supermarkets. These foods tend to vary

Connecting Global Priorities: Biodiversity and Human Health 163

 9. Biodiversity and
biomedical discovery
SHUTTERSTOCK

1. Introduction developments depended, wholly or in part, on

biological diversity (Chivian and Bernstein 2008).
The diversity of life on earth has been an engine
of biomedical discovery and sustained human Antibiotics rank among the most significant
health for millennia, contributing to countless breakthroughs that have considerably improved
medical advances. Ironically, in many instances, human health in the twentieth century. Death from
the very organisms that have given humanity pneumonia was so prevalent in the early twentieth
vital insights into human diseases, or are the century, for instance, that Sir William Osler
sources of human medications, are endangered described it is as the “captain of the men of death”
with extinction because of human actions. While (see, for example, Barry 2005). With the arrival
other sources explore these subjects in detail of penicillin and its descendants, rates of death
(see Chivian and Bernstein 2008), this chapter from pneumonia plummeted (see, for example,
briefly explores the substantial contribution of Podolsky 2006). The penicillins as well as nine of
biodiversity to biomedical discovery, and discusses the thirteen other major classes of antibiotics in
key health challenges posed by accelerating rates use derive from microorganisms. Between 1981
of biodiversity loss. and 2010, 75% (78 of 104) of the antibacterials
newly approved by the United States (US) Food
2. Why biodiversity matters to and Drug Administration can be traced back to
natural product origins (Newman and Cragg
medical discovery
2012). Percentages of antivirals and antiparasitics
Many of the diseases that afflicted or killed most derived from natural products approved during
people a century ago are today largely curable that same period are similar or higher. The over-
or preventable. How did this happen? Applying and misuse of antibiotics has cultivated a slew of
scientific methods to medical research certainly highly resistant bacterial strains, which in some
contributed to this development, as did the instances cannot be effectively treated with any
engagement of many researchers and medical currently available antibiotic (Levy and Marshall
professionals. However, no amount of scientific 2004; Davies and Davies 2010). A race to find
rigour, researchers, or any other factor could new antibiotics to overcome so-called superbugs
suffice on its own to reduce the human suffering ensued (e.g. Spellberg et al. 2008). As of February
realized in the twentieth century, as many of these 2014, at least 45 new antibiotics that carry the
potential to treat serious bacterial infections are in

164 Connecting Global Priorities: Biodiversity and Human Health

development for use in the US. Most of these rely unique reproductive physiology was lost with
upon a natural product predecessor (Pew Health them, which could have alleviated the suffering
Initiatives 2014). of tens of millions of worldwide who have peptic
ulcer disease and related disorders.
For as long as we know, humanity has relied upon
compounds from nature designed to treat what Plants have been the single greatest source of
ails us (see also the chapter on traditional medicine natural product drugs to date, and although an
in this volume). Otzi, the oldest known natural estimated 400 000 plant species populate the
mummy, who was found under a thawing glacier earth, only a fraction of these have been studied
in the Italian Alps, died more than 5000 years for their pharmacological potential (Hostettmann
ago and carried with him a pouch that contained et al. 1998). For example, one of the largest plant
birch polypore fungus Piptoporus betulinus known specimen banks, the natural products repository
to reduce inflammation and kill bacteria (see, at the National Cancer Institute, contains ~60 000
for example, Bortenschlager and Oeggl 2000). specimens (Beutler et al. 2012). The same number
Reliance upon biodiversity for new drugs continues of species – 60 000 – are thought to be used for
to this day in most domains of medicine. More medicinal purposes worldwide and perhaps as
than half of the 1355 newly approved drugs by the many as 40% of these species are considered
US Food and Drug Administration between 1981 threatened with extinction (Biodiversity Indicators
and 2010 had natural product origins (Newman Partnership 2010; CBD 2014; see also the chapter
and Cragg 2012). on traditional medicines in this volume).

The success of drug development from natural Plant species as diverse as the Himalayan yew,
products manifests the common molecular Taxus wallichiana (and other Taxus spp.) or African
currency of life on earth.  Species as diverse as cherry, Prunus africana, long used in traditional
Conus geographus, Penicillium citrinum and Taxus medicines, have been threatened by factors such
brevifolia – a meat-eating marine snail, rice as overharvesting and international trade, driven
fungus and boreal conifer – produce molecules by high consumer demand (Hamilton 2003). Both
that in humans relieve pain, reduce cholesterol, are listed under the Convention of International
and treat breast, ovarian, lung and other cancers, Trade in Endangered Species of Flora and Fauna
respectively, because organisms, as diverse as they (CITES). The establishment and enforcement of
are, communicate within themselves and other effective management and trade of wild-collected
creatures using common molecular currencies species, both by governments and corporations,
(Chivian and Bernstein 2008). As discussed in remains a critical need in plant conservation (e.g.
the chapter on traditional medicine, this often Phelps et al. 2014).
increases the appeal for bioprospecting for
medicines.¹ Other realms of the living world, especially
the microbial and marine, are almost entirely
While most of the medicinal potential of nature unstudied and hold vast potential for the
has yet to be tapped, we may be losing potential development of new drugs, given both their
new cures with biodiversity loss. One of several diversity and the medicines already discovered
examples is the two species of gastric brooding from them (Chivian and Bernstein 2008).
frogs indigenous to the rainforests of Queensland,
Australia. These species employ perhaps the most
unusual reproductive strategies in the animal
kingdom, using their stomachs as wombs for their
young (Chivian and Bernstein 2008; McNeely
2006). Having gone extinct in the 1980s, their

¹ For further discussion on marine bioprospecting see, for example, Hunt and Vincent (2006).

Connecting Global Priorities: Biodiversity and Human Health 165

 Case study: plQsia ;aliforni;a and the human brain

Drugs derived from natural products may perhaps be the most direct and concrete bond that many
may nd between biodiversity and medicine. However, biodiversity holds much broader connections
with human health. In many arenas of biomedical inquiry, biodiversity has beenan invisible linchpin
of discovery. For example, of the 104 Nobel prizes in Medicine awarded since Emil von Behring
received the prizein 1901 for his research on guinea pigs to develop a treatment for diphtheria,
99 were given to scientists who either directly or indirectly made use of other species to do their
research.

In 2000, Eric Kandel shared the Nobel prize in Physiology or Medicine with Arvid Carlsson for his
groundbreaking research on memory. Kandel s research established, at a cellular and molecular
level, how our brains learn and form memories. He did not study human brains to do this. Instead,
he studied the nervous system of sea hares from the genus Aplysia. A human brain has about 86
billion neurons whereas Aplysia has, all told, around 20 000, and only about 100 of those neurons
are involved in memory. In addition, Aplysia’s memory cells are also among the largest of their
kind in the animal kingdom and can be visualized with the naked eye. This makes monitoring the
electrical messages that scurry across their membranes, and exploring how these messages may alter
genes and other molecules that control a neuron s inner workings, comparatively easy. With these
advantages, Kandel found what was di cult, if not impossible, otherwise. What was gleaned from
Aplysia’s nervous system made possible further research in other species, which has deepened our
understanding not only of learning and memory, but of a host of human ailments, from substance
abuse and Alzheimer disease to the lifelong consequences of early childhood trauma.

For more on research from Aplysia see: Kandel ER. (2007). In search of memory: the emergence of a
new science of mind. New ork, USA: WW Norton & Company.

ǡǤǢǰǭǠɻ Aplysia californica releasing ink that not only clouds predators’ view but masks their sense of smell
and taste.
GENEVIEVE ANDERSON

166 Connecting Global Priorities: Biodiversity and Human Health

 Case study: ,herEus aIuati;us and DNA research

Thermus aquaticus is another behind-the-scenes, though absolutely vital, species for biomedical
discovery. This bacterium was rst identi ed in the Mushroom Spring of ellowstone National Park
in 1966 as part of an expedition to nd life in places where it was not supposed to exist. The late
summer day that Thomas Brock and Hudson Freeze collected samples from Mushroom Spring, the
water temperature measured 69 ºC.

At rst, T. aquaticus was little more than a curiosity: an organism able to live at temperatures that
would cook most cells, including human cells. This reputation soon changed. Advances in the early
years of genetic research were many but were limited in part by di culties with replicating DNA in a
laboratory. All life replicates DNA in order to survive. To do this, paired strands of DNA are separated
and then copied using a specialized molecular copying machine known as DNA polymerase.
To separate the DNA strands, cells use a set of molecular machines. Using these machines in a
laboratory proved too di cult, so scientists turned to another method, heat. DNA strands reliably
separate at temperatures just over 90 ºC and remain separate at around 70 ºC, right near the optimal
temperature for T. aquaticus and its DNA polymerase known as Taq. The ability of Taq to copy DNA at
high temperature forms the foundation of the polymerase chain reaction, or PCR, which is arguably
the single most important tool in genetic research ever invented. In 2013 alone, nearly 27 000
articles make reference to PCR in the US National Library of Medicine s PubMed database.

ust as with the ability of natural products obtained from one species to exert in uence on many
others, the ability of Taq to work on DNA from multiple species underscores how all life shares some
basic features. At the same time, Taq also speaks of the importance of the diversity of life. Without life
thriving at high temperatures, there would be no polymerase suitable for PCR and, without PCR, the
modern-day genetic research juggernaut may never have got o the ground.

Source: Brock and Freeze (1969)

3. Biodiversity, the microbiome in isolation. Infections are attacked, or more

and antimicrobial resistance often prevented, through the secretion of several
compounds at once.
Far greater than what individual species offer
to medicine through molecules they contain Antibiotic use, aside from its potential to cultivate
or traits they possess, an understanding of resistance, also carries the potential to disrupt
biodiversity yields irreplaceable insights into how relationships between hosts and their symbiotic
life works, which bear upon current epidemic microbes. The human microbiome contains tenfold
diseases. Consider the multiple pandemics that more microorganisms than cells that comprise the
have resulted from antimicrobial or antibiotic human body, and antibiotic use can dramatically
resistance (see also the chapters on infectious alter its composition and function (Cho and Blaser
disease and health care and pharmaceuticals in 2012). Although much of the microbiome and
this volume). Human medicine tends to use a its relationship to its host remains unknown, it
paradigm for treating infections unknown in is already apparent that changes to the variety
nature, which is treating one pathogen with one and abundance of various microorganisms,
antibiotic. Most multicellular life (and a good as can occur with antibiotic use, may affect
share of single cellular life) produces compounds everything from the host’s weight and the risk of
with antibiotic properties but never uses them contracting autoimmune disease, to susceptibility

Connecting Global Priorities: Biodiversity and Human Health 167

 ǡǤǢǰǭǠɼ Mushroom Spring in Yosemite National Park. In this sulphurous hot spring was discovered Thermus
aquaticus, the source of Taq polymerase, which serves as the essential cog in the polymerase chain reaction,
arguably the single most important method used in genetic research.
JIM PEACO / US NATIONAL PARK SERVICE

to infections (Petersen and Round 2014). The 2011; Costello et al. 2013). About 2 million of an
microbiome may also shape mood and behaviour estimated 10 million species on earth have been
(see also the chapter on microbial biodiversity given scientific names (Wilson 2003). For many
and noncommunicable diseases in this volume). of these, we know little more than their names as
The influence of microorganisms on the larger they are known from only a single encounter in
life forms they cohabit is not terribly surprising, which an explorer observed a creature never before
given the history of life on earth. Several billion seen. Most of life’s diversity, however, cannot be
years elapsed between the appearance of the first seen by the naked eye, and of these microscopic
single-celled creatures and multicellular life, and creatures, we know far less.
single-celled creatures appear to have enmeshed
themselves with all their multicellular successors. Even with this limited view of the life we share
the planet with, we know that each year the
variety of organisms on earth continues to decline
4. Future challenges: implications (CBD 2014). Recent scientific estimates indicate
of biodiversity loss for medical that species are disappearing up to 1000 times
discovery faster than occurred before humanity populated
the planet (CBD 2010). Such statistics are often
In this time of technological advancement,
difficult for many people to grasp, especially as
when the precision of measurement comes at
most loss of biodiversity goes unnoticed. While
increasingly diminutive scales such as nanoseconds
each of us may in our own lifetimes recognize that
or nanometers, and we begin to explore the most
one, or even a few, species that were once common
minute forms of life on earth, we have at best a
in a place we know have disappeared, far more
first approximation of the numbers of organisms
often species vanish without notice.
we share the planet with (May 1988; Mora et al.

168 Connecting Global Priorities: Biodiversity and Human Health

In the coming decades, a great mass of life on As this volume attests, we know astonishingly
earth hangs in the balance for survival as pressure little about the life forms that inhabit the earth.
on the biosphere mounts, primarily from habitat Even so, we know that many have already
loss and, increasingly, climate change (see also the provided invaluable cures for human diseases
chapter on climate change in this volume). and tremendous insights into the workings of the
human body. Given our ignorance of biodiversity,
we would be foolish to try to conserve only what
5. Ways forward: conservation as
we deem important to ourselves. The dividends
a public health imperative of biodiversity realized in our economies must
Too often, biodiversity harnessed from one corner be widely shared to promote the conservation of
of the earth has benefited another corner, with biodiversity where it is needed the most (Pimentel
little payback to its origins. Existing frameworks, et al. 1997; Sukhdev 2014).
such as the Nagoya Protocol (see http://www.
cbd.int/abs/about/) or Fairwild Standard (see As compelling as arguments of the past have been
http://www.fairwild.org), seek to ensure that to conserve biodiversity, rates of extinction are
biodiversity’s value accrues in its place of origin. accelerating largely due to habitat destruction and,
These mechanisms, if successfully implemented, increasingly climate change (e.g. CBD 2014; Urban
could drive large investments in conservation 2015; Pounds et al. 2006; Franco et al. 2006).
where biodiversity is richest and most imperilled. To stem the tide of biodiversity loss, innovative
Happily, successes have already been had in India methods must be used to convince policy-makers
and Viet Nam for plant bioprospecting and in and the citizens of the world that biodiversity
Kenya, Kazakhstan, Bulgaria and Poland for must be saved.
certification of exported goods (see, for example,
Krishnakumar 2012; Meijaard et al. 2011).

Connecting Global Priorities: Biodiversity and Human Health 169

WORLD BANK PHOTO COLLECTION / FLICKR

10. Biodiversity, health care

& pharmaceuticals
1. Introduction A wide range of chemical substances is used to
support health care, including pharmaceuticals,
Other chapters of this state-of-knowledge report disinfectants, cleaning products, X-ray contrast
explore the role that biodiversity plays in shaping media, various personal care and hygiene
public health outcomes – including relationships products, and excipients. It is inevitable that
with infectious diseases, noncommunicable these will sometimes be released into the natural
diseases, and trauma associated with natural and environment through their manufacture, use
human-induced disasters. The contribution of or disposal, and that they could subsequently
these chapters to understanding how population affect biodiversity. Of particular interest, due
health and the delivery of primary health care are to their biological activity, are pharmaceuticals.
influenced by biodiversity is a central objective of Since at least the early 1990s, there has been
this state-of-knowledge review. However, to gain a increasing concern over the potential impacts of
complete understanding of the health–biodiversity pharmaceuticals used in health care on the natural
nexus, it is also important to recognize that environment (Halling-Sørensen et al. 1998;
policies and practices associated with the delivery Daughton and Ternes 1999; Kümmerer 2009).
of health care can have impacts on biodiversity and
the sustainability of ecosystem services, and that The particular focus of this chapter is the issue of
these impacts can subsequently have a negative the environmental side-effects of medication – the
effect on human health. Impacts can occur from potential impacts that drug entities and related
a number of sources, including health care- chemical compounds may have when they enter
associated manufacturing, health-care and health the environment. The presence of pharmaceuticals
research facilities (hospitals, clinics, etc.), and in the environment is an issue that has received a
health-care related transport and trade. Potential great deal of scientific attention since the 1990s,
environmental concerns include energy demand; and numerous studies have now been performed
emissions to the atmosphere, soil and water; aimed at assessing and understanding their
water use; waste disposal, including potentially environmental occurrence (i.e. how and to what
hazardous wastes; and the extraction/harvesting extent these compounds enter the environment),
of wild species for drug exploration or use. Box 1 fate (what happens to these compounds after
below provides an overview of some of the major release), and effects (particularly ecological and
environmental considerations associated with the (eco)toxicological impacts). There is increasing
delivery of health care. evidence that pharmaceuticals in the environment

170 Connecting Global Priorities: Biodiversity and Human Health

Box 1. Overview of some of the major environmental considerations associated with
the delivery of health care

Examples of potential impacts of health-care activities on ecosystems

Issue Example Potential impacts

Energy use Energy demand for health-care facilities Energy demand is associated with
can be signi cant, with 24-hour the consumption of fossil fuels,
requirements for medical equipment, emission of greenhouse gases and
lighting, heating and air-conditioning. other pollutants.

Water use Hospitals and other health-care facilities This adds signi cantly to
can use large quantities of water, community demand for water
particularly for patient hygiene, surface resources, potentially impacting
cleaning, food preparation and general on aquatic ecosystems or water-
sanitation. dependent habitats.

Water quality Health-care facilities use signi cant Release of PPCPs into the soil or
amounts of a wide variety of pharma- aquatic environments, including
ceuticals and personal care products some that act as endocrine-
(PPCPs), as well as sanitizers, and other disrupting compounds, is
chemicals, such as X-ray contrast media. implicated in a range of impacts
Many of these are not fully degraded by upon ecosystems and upon animal
modern wastewater treatment systems health and behaviour.
and end up in natural waters.
Waste production As well as large quantities of general Waste disposal poses challenges
paper and plastic waste, health-care for environmental and public
facilities can produce large quantities health authorities. Inappropriate
of food waste and hazardous waste waste management and disposal
materials, including biohazardous and infrastructure can impact the
radioactive substances. quality of water, soil and air, and
a ect human, plant and animal
health.
Air quality Many hospitals have incinerators to deal This has potential for local impacts
with hazardous and/or biological waste, on human or ecological health
which may release contaminants into (e.g. from NOx, SOx, particulates,
the local atmosphere. heavy metals), as well as the wider
release of greenhouse gases.
Emissions associated with health-
care-associated transport can also be
signi cant.

Medicinal species Much modern and traditional health care Unsustainable exploitation of
harvesting, medical depends on medicines derived from biodiversity for medicinal use or
research and drug nature, from modern drugs to herbal research can endanger species and
discovery remedies and complementary therapies. ecosystems, and threaten the well-
Modern medicine also utilizes wild and being of the human communities
captive species for animal studies. they support.

Source: Adapted from COHAB 2014

Connecting Global Priorities: Biodiversity and Human Health 171

 can have an adverse effect on biodiversity and these issues (Taylor 2010). As such, the issue of
ecosystem services, unintentional though these pharmaceuticals in the environment illustrates an
may be. Where these effects on ecosystems could important opportunity for collaboration between
lead to downstream effects on public health, health and environmental scientists, regulators
interventions initially intended to promote and the private sector to tackle a critical, cross-
public health (i.e. the manufacture, supply and cutting issue.
use of pharmaceutical products) may actually have
unforeseen indirect negative impacts on health In the sections that follow, evidence for the
and well-being. inputs and occurrence of pharmaceuticals in
the environment, and the potential impacts of
The issue of pharmaceuticals in the environment these on biodiversity is explored. Approaches
has come under the scrutiny of regulatory bodies, for reducing these inputs and impacts are also
including drug approval agencies such as the discussed.
United States (US) Food and Drug Administration
and the European Medicines Agency of the
2. Inputs and occurrence of active
European Union (EU), and others (Breton and
Boxall 2003; Kampa et al. 2010; Küster and pharmaceutical ingredients (APIs)
Adler 2014). It is also of particular interest to the Although pharmaceutical products have probably
pharmaceutical industry, with many major drug been entering the environment for as long
firms engaging with environmental chemists and as they have been manufactured and used,
regulators in order to understand and address this topic has begun to receive considerable

ǡǤǢǰǭǠɻ Major pathways of release for active pharmaceutical ingredients into the environment

Source: Reproduced from Boxall (2004) with permission from EMBO Reports

172 Connecting Global Priorities: Biodiversity and Human Health

attention only in recent years, as advances in have determined that public health risks from
environmental monitoring technologies and the consumption of individual APIs via drinking
a greater awareness of environmental risk has water are likely to be very low (Bruce et al. 2010;
promoted their detection and assessment. WHO 2011). However, the effects of this exposure
It is inevitable that during the life-cycle of a route are difficult to evaluate, and there have been
pharmaceutical product, active pharmaceutical few studies of the potential risks from long-term
ingredients (APIs) are released into the natural exposure to mixtures of APIs in drinking water
environment (Halling-Sørensen et al. 1998; (Smith 2014). Risks to certain vulnerable groups
Daughton and Ternes 1999; Boxall 2004). APIs require further assessment (Collier 2007).
can be released to rivers and streams during the
manufacturing process – either directly through It is therefore not surprising that a range of
fugitive (accidental or unmanaged) emissions, human APIs, including hormones, antibiotics,
or to wastewater treatment plants. Emissions non-steroidal anti-inflammatory drugs (NSAIDs),
from manufacturing can be particularly high in antidepressants and antifungal agents have been
developing regions with a high manufacturing detected in rivers and streams across the world
base and with limited regulation (Larsson et al. (Hirsch et al. 1999; Kolpin et al. 2002; Monteiro
2007; Fick et al. 2009; Cardoso et al. 2014). and Boxall 2010).

APIs also enter sewerage systems through human In contrast, veterinary APIs (i.e. pharmaceuticals
use (Santos et al. 2010); API molecules may be used for treating animals) can enter the
incompletely metabolized or broken down in the environment more directly, for example, by
body, and whole compounds or their metabolites, being excreted directly into the soil by pasture
daughter compounds (which are also sometimes animals (Boxall et al. 2004), or directly applied to
referred to as transformation products) may be surface waters and marine habitats in aquaculture
released with domestic wastewater. Following operations, with a risk of a build-up in sediments
use, in areas with sewerage connectivity, human- (e.g. Coyne et al. 1994; Daughton and Ternes
use APIs and their metabolites will be excreted 1999; Rico and Van den Brink 2014). In terrestrial
to the sewerage system and transported to ecosystems, the use of pharmaceuticals in
wastewater treatment plants. The complexity of livestock is likely to be the most significant source
some pharmaceutical molecules can limit their of veterinary APIs entering the environment
degradation in wastewater treatment plants, (including via spreading of manure or slurry as
with the result that APIs and their transformation fertilizer). However, the use for treatment of
products can be discharged to the environment domestic pets, wildlife and feral animals may also
in the final effluent (treated water) when it is be important. Of particular interest in this regard
released to surface waters such as rivers and may be long-term, widespread programmes for
streams. In areas with low sewage connectivity, eradication of wild animal diseases through baiting
APIs will be released directly to the environment. programmes, which run the risk of dosing non-
Human-use APIs may also be released into the soil target animals directly (see, for example, Hegglin
environment when contaminated sewage sludge et al. 2004; Campbell et al. 2006). A range of
or sewage effluent is applied to land. These may veterinary APIs have consequently been detected
then be transported to groundwater and surface in agricultural soils, in marine sediments, and in
waters through leaching, land drainage and storm surface waters receiving run-off from farmland
run-off. By these routes, APIs can also enter water (Boxall et al. 2004). In addition to the manufacture
resources used for drinking water supply. Drinking and normal use of APIs, environmental inputs
water treatment systems may not effectively can also arise from their disposal, either through
remove these compounds, and APIs have been domestic refuse or disposal to the sewer system.
found in treated drinking water, albeit at very Landfill sites have been shown to be a potentially
low (ng/L) concentrations. From a toxicological important source of API contamination in surface
perspective, several detailed risk assessments

Connecting Global Priorities: Biodiversity and Human Health 173

 and groundwater (Bound and Voulvoulis 2005; are designed to interact with a target (such as a
Musson and Townsend 2009). specific receptor, enzyme or biological process)
in humans and animals to deliver the desired
While the reported concentrations of APIs are therapeutic effect. If these targets are present in
generally low (i.e. <μg L 1 in surface waters), these organisms in the natural environment, exposure
substances have been observed across a variety to some pharmaceuticals might be able to elicit
of hydrological, climatic and land-use settings. effects in those organisms. Pharmaceuticals can
It is also known that some substances (e.g. the also cause side-effects in humans and it is possible
tetracycline and fluoroquinolone antibiotics, that these and other side-effects can also occur in
selected antiepileptics and some antidepressants) organisms in the environment.
persist in the environment for months to years (e.g.
Boxall et al. 2006; Kay et al. 2004), meaning that It is also possible that metabolites and other
organisms can be exposed to these compounds transformations products of APIs can have similar
throughout their lifetime. or entirely different biological activity in exposed
biota (Daughton and Ternes 1999). While the
individual or incidental exposure concentrations
3. Impacts of pharmaceuticals
of selected APIs may be very small, in some
on biodiversity and ecosystem instances, the exposure may occur over a long
services period, particularly where APIs are persistent, or
APIs are developed and used because of their where they are routinely emitted. Furthermore,
biological activity. While in many cases the modes in ecosystems receiving a combination of APIs,
of action of APIs are well established, for many e.g. in sewage treatment plants receiving water or
drugs the mechanism of action is not specifically sediment around fish farms, populations of wild
known or fully understood. This is true of human species are exposed to multiple different APIs and
and veterinary APIs. Most pharmaceuticals transformation products, leading to the risks of
additive effects (caused by exposure to different

VICTOR NEAGU / WORLD BANK PHOTO COLLECTION / FLICKR

174 Connecting Global Priorities: Biodiversity and Human Health

APIs with similar modes of action) or synergistic and streams) led to the complete collapse of an
effects (interaction between different APIs). The entire population of fish (Kidd et al. 2007).
kinds of potential impacts range from acutely
toxic events, including death for some species Another class of human APIs of current concern
(notably invertebrates), and sublethal impacts, is the antidepressants, which include compounds
including behavioural, endocrine, immunological, such as fluoxetine, escitalopram and paroxetine.
reproductive and mutagenic effects. This often Recent research has suggested that environmentally
occurs in a context where wildlife is exposed relevant concentrations of fluoxetine, linked to
to other forms of pollution or disturbance, so concentrations released in coastal and estuarine
that APIs should be seen as adding to a larger habitats in the United Kingdom (UK), cause a
environmental burden. change in behaviour of the marine amphipod
Echinogammarus marinus by altering levels of
Evidence for the ecotoxicological impacts of even serotonin. Exposed amphipods showed an
very low concentrations of APIs in the environment increased tendency to swim close to the water
has been noted in some studies. For human APIs, surface, which increases the likelihood of predation
a major area of concern is the impact of synthetic by fish or birds (Guler and Ford 2010). Bean et al.
hormones and hormonally active pharmaceutical (2014) also demonstrated that environmentally
compounds. These add to an already significant relevant levels of fluoxetine could have significant
environmental burden of endocrine-disrupting behavioural and physiological effects on starlings
compounds (EDCs), which comprise a wider range (Sturnus vulgaris), which could be exposed to the
of chemicals, including various detergents, flame drug when feeding at sewage treatment plants
retardants, pesticides, plant hormones and others, or fields treated with sewage sludge. Recent
as well as naturally occurring hormones that enter research has also indicated that environmentally
sewage treatment works. The ecological impacts relevant levels of antidepressants can affect the
of EDCs as a wider group of substances include reproduction, feeding and predator-avoidance
the occurrence of intersex characteristics in male behaviours of fathead minnows (Weinberger and
fish; this can be persistent and irreversible, with Klaper 2014). Brodin et al. (2014) demonstrated
subsequent impacts on fertility and population that low μg/L levels of the anxiolytic oxazepam in
stability (Orlando and Guillette 2007). These freshwater could lead to bioaccumulation in the
effects have been particularly noted in aquatic predatory European perch (Perca fluviatilis), with
ecosystems, where eggs can develop in the testes significant impacts on feeding behaviour.
of male fish exposed to EDCs. There is a large body
of evidence that suggests that one particular API, Impacts on wildlife have also been noted for
ethinylestradiol (EE2) plays a significant role even veterinary APIs. For example, Floate et al. (2005)
at very low environmental concentrations. EE2 is provide a comprehensive review of studies on
the active ingredient in the human contraceptive parasiticides applied to pasture animals. These
pill, which is used by approximately 100 million show that some classes of APIs are excreted to
people worldwide (Jobling and Owen 2012). As pasture environments in concentrations that can
well as it use in birth control, EE2 is also used be lethal to coprophagous (dung-eating) insects
for the treatment of various gynaecological and to other species inhabiting the pasture soil
and endocrine disorders. Laboratory research environment, over periods ranging from a few days
has shown that environmentally relevant to several months (see also Lumaret et al. 2012).
concentrations of EE2 alone can have dramatic This poses a potential risk to other species through
impacts on wildlife (Lange et al. 2001; Nash et al. the food chain, including bats and birds. While
2004), while in one study in Canada, involving the evidence for the direct toxicity of environmental
introduction of EE2 in a lake at a concentration concentrations to vertebrate predators of pasture
of just 5 parts per trillion (which is only slightly insects has not been determined, there is concern
higher than the concentrations expected in rivers that reductions in farmland invertebrates may lead
to locally significant reductions in prey availability,

Connecting Global Priorities: Biodiversity and Human Health 175

 including important prey items for certain species associated with the declines of several species
(e.g. Vickery et al. 2001; Wickramsinghe et al. of vultures in South Asia (see case study below),
2002; Boxall et al. 2007). resulting from the use of the pharmaceutical
diclofenac in veterinary preparations, leading to
Perhaps the most well-known incidence of near-extinction of once-abundant wildlife, with
veterinary drug impacts on wildlife have been

Case study: diclofenac and decline in the population of vultures

The Indian subcontinent was once home to several million vultures. These birds played a vital role
in the ecosystem, cleaning up carcasses of dead animals, and thereby helping to reduce the risk of
disease and contamination of soil and water resources. Their numbers were supported by the huge
numbers of livestock; India alone has the largest cattle population in the world. Dead livestock
are usually left out in the open for removal by vultures – the quickest, cheapest and most e cient
natural disposal method. But a drastic decline in vulture numbers began in the 1990s. The three
most abundant species – the oriental white-backed vulture (Gyps bengalensis), the Indian vulture
(G. indicus) and the slender-billed vulture (G. tenuirostris) declined by more than 95% in Pakistan,
India and Nepal between 1990 and 2001. It became evident that the decline in vulture numbers was
having an impact on ecosystem functioning, as evidenced by the number of animal carcasses that
were left to decay in elds across the Indian subcontinent. This has helped to boost numbers of feral
dogs, rats and other scavengers, resulting in a greatly increased threat of rabies and other diseases in
the human population.

Postmortems on vulture carcasses determined that massive numbers of vultures were dying
from visceral gout – the accumulation of uric acid deposits associated with kidney failure, but
microbiological and toxicological studies failed to pinpoint the cause as the decline progressed.
Eventually, an investigation of the primary food source of Gyps vultures – livestock carcasses – led
to the identi cation of a pharmaceutical compound, diclofenac sodium, as the cause. Diclofenac has
been widely administered by veterinarians and famers in analgesic, antirheumatic and antimicrobial
preparations, and its availability increased greatly in the early 1990s due to numerous market
factors. There have been reports of widespread abuse of the prescription laws that should restrict
drug sales, with poor dose controls for humans and livestock. This drug has been shown to be highly
toxic to vultures at the levels to which they are exposed from livestock carcasses. Diclofenac has
been banned in India, Pakistan and Nepal since 2008; however, there is concern that the ban is being
circumvented or ignored in some areas, and more widespread controls are required, as well as greater
cooperation with the farming community, if vulture populations are to recover in the region.

Studies have shown that African Gyps vultures are equally vulnerable to diclofenac poisoning,
suggesting that the risk may extend to all Gyps species, and there are concerns that many other
scavenging bird species are also susceptible. With the recent controversy over the approval of
diclofenac for veterinary use in parts of Europe, including Spain, which is internationally important
for avian scavengers, it is clear that there is a need for environmental risk assessments of veterinary
medicines to take a multidisciplinary perspective, based on the full scope of scienti c evidence, and
for regulatory authorities to take necessary precautions to prevent environmental contamination with
veterinary APIs.

Sources: Oaks et al. 2004; Markandya et al. 2008; Cuthbert et al. 2011; Naidoo et al. 2009; Margalida et al. 2014

176 Connecting Global Priorities: Biodiversity and Human Health

several potential knock-in impacts on human well- can be carried by wildlife, particularly by animals
being, including increased public health risks. associated with agriculture or human settlements
(Radimersky et al. 2010; Taylor et al. 2011; Carroll
Although numerous detailed risk assessments et al. 2015), and persist in agricultural soils
suggest that environmental concentrations of (Kyselková et al. 2015).
most APIs in isolation are unlikely to have any
significant impact on biodiversity, these examples
illustrate that there is reason for concern; there )XWXUHFKDOOHQJHVHƨHFWVRI
is a need for more integrated environmental social and environmental changes
risk assessments that account for ecological The range of factors affecting the occurrence
interactions, and more effort is needed to of APIs in the environment is by now well
understand the risks associated with mixtures of understood. The science of risk assessment for
APIs in the environment (Backhaus 2014). these pollutants is also increasingly advanced,
with product risk assessment based on product
Another issue of concern related to both human
usage (or estimated usage for novel drug entities),
and veterinary APIs in the environment, with
estimates of wastage, (bio)degradation studies,
more widespread implications for human health,
and assessment of ecological toxicity. However, a
is the link to the growing threat of antimicrobial
number of important issues surrounding inputs to
resistance. The number and diversity of drug-
the environment remain to be addressed.
resistant pathogens is increasing, and a slowdown
in the production of new antimicrobial drugs since For example, changing demographics are likely to
the 1980s means that existing treatments are significantly alter the type, range and quantities of
increasingly ineffective against several important APIs being utilized at the local and regional levels.
human diseases (WHO 2014). Research has shown For human APIs, ageing populations, increased
that drug-resistant infections accounted for a large migration, economic transitions in developing
number of emerging infectious diseases in the countries, and urbanization are all likely to
past 30 years, and that multidrug resistance (when see shifts in the use profiles of pharmaceutical
an infection shows resistance to a range of drugs products. Changes in agricultural practice –
normally used to treat it) is a serious and growing to accommodate the increased demand for
concern (Jones 2008; Levy and Marshall 2004). specific foods, including responses to nutrition
The causes of antimicrobial resistance are complex, transitions and conversion of natural habitats
and although genes for antibiotic resistance occur for food production – are likely to see changes
widely in nature without human influence, the in the quantities and kinds of animal health
inappropriate use and overuse of antimicrobials, products in use. Climate change is also expected
including the non-therapeutic use of antibiotics to have an impact by affecting the ecology of
as growth promoters in agriculture, is a major various pathogens in humans, domestic animals
cause of drug resistance (WHO 2012). The risk and wildlife, and thereby potentially leading to
of resistance is also increased by the routine demands for the increased use of certain drugs,
disposal of drugs and drug residues. The release and development of new drug entities to address
of antimicrobial drugs into the environment increased or emerging health threats. Climate
from human use and manufacturing, veterinary change may also affect how APIs occur in the
applications, disposal at landfill sites, or use in environment and their relative risks to biodiversity.
aquaculture increases the exposure of microbes to For example, changes in surface water run-off,
those drugs, and thereby increases the potential changing water and soil temperatures, and changes
for the development of drug resistance. Research in natural vegetation and wildlife populations
has shown that pollution and patterns of human may be expected to affect the movement and
water use are important risk factors (Pruden et degradation of APIs in the environment, their
al. 2012, 2013; Wellington et al. 2013), and that bioavailability, and the types of species exposed to
drug-resistant microbes are found in nature and different API compounds. Therefore, further work

Connecting Global Priorities: Biodiversity and Human Health 177

 SIMONE D. MCCOURTIE / WORLD BANK PHOTO COLLECTION / FLICKR

is required to understand the routes of exposure One of the most pressing concerns involves
of wild populations to APIs, and how these might the manner in which antibiotic, antifungal
change under different scenarios of future climate and antiparasitic APIs in the environment may
and population changes (Boxall et al. 2008; Kim present selection pressures for drug resistance
et al. 2010; Redshaw et al. 2013). in pathogenic organisms. The increasing threat
of antibiotic resistance, including the emergence
To date, much of the research into the and rapid spread of multidrug resistance, means
environmental occurrence, fate and effects of that there is a demand for novel drug responses
APIs has been focused on high-income countries, as well as for a greater understanding of how the
and more research effort is needed to understand use, abuse or overuse, and disposal of existing
the situation in least-developed countries, and to antimicrobials might promote the emergence
devise solutions to related environmental risks and spread of drug resistance. Related to this is
(Kookana et al. 2014). Risk assessments also the need for further research on how other forms
need to be strengthened to better account for the of pollution may enhance selection pressure
sublethal effects of APIs on wildlife populations for the development of antibiotic resistance in
(e.g. in situations of low dose but long exposure), environmental microbes (Baker-Austin et al. 2006;
particularly those that may have knock-on effects Finley et al. 2013), and on how drug-resistant
on predator–prey relationships and wider food pathogens may be spread by wildlife.
chain impacts. The potential risks of synergistic
or additive impacts – through combinations of Additional work is also required to prioritize
APIs in the environment, or co-occurrence with APIs for more detailed risk assessment. For
other pollutants (e.g. the added impacts of EE2 example, which types of drugs are likely to enter
in populations also exposed to other endocrine- the environment in ecologically significant
disrupting compounds) – also need to be better quantities? It is estimated that over 4000 different
understood (Backhaus 2014). pharmaceutical compounds are currently in

178 Connecting Global Priorities: Biodiversity and Human Health

widespread use (Boxall et al. 2012) and the There is also a need to more effectively regulate
majority of these have not been tested for the the use and disposal of APIs at the community
environmental effects. While new pharmaceutical level. This includes tackling the overuse and
products are subjected to risk assessment, overprescription of APIs, and perhaps exploring
it is unlikely that a significant proportion of opportunities for reduced-dose prescribing,
the existing APIs can be subjected to full risk and conducting information campaigns to
assessment in a timely manner. It is important promote wise use through sustainable health-
therefore that priority API pollutants are identified care campaigns. Health agencies that purchase
for study. medicines for public use should be made aware
of the environmental issues associated with APIs,
and discuss these with their suppliers. Waste drug
5. Ways forward: reducing the
take-back schemes should also be promoted, with
impact of APIs in the environment better education for customers from prescribers
In most developed countries with strong and at the point of sale. Similarly, for veterinary
regulatory systems for integrated prevention and APIs, the risks of overuse and misuse of these
control of pollution, it has long been considered products must be effectively communicated to
that outputs of waste and wastewater from farmers and larger food producers, food retailers
the manufacture of APIs are well regulated and and relevant regulatory bodies; appropriate
controlled, so that fugitive emissions of APIs to restrictions and support mechanisms can be put in
soil, groundwater and surface water would be place to limit the impact of veterinary APIs to the
minimal – not least because any significant fugitive intended target species. The use of veterinary APIs
loss of API from a manufacturing facility also to treat diseases in wild populations should also
represents a potential loss of revenue. However, be carefully controlled, and widespread baiting
research into the environmental burdens of APIs of APIs should be avoided or carefully managed
from sewage treatment plants receiving effluent to reduce non-target effects. In addition, while
from pharmaceutical factories has suggested recognizing that the causes of antimicrobial
that manufacturing facilities are a potentially resistance are complex, it is vital that greater
significant source of API inputs to surface water effort is made to understand the linkages between
and sewage sludge (Philips et al. 2010; Cardoso veterinary and human use of APIs, environmental
et al. 2014). In some developing countries, exposure, and the development and transfer of
environmental inputs from manufacturing sites antimicrobial resistance genes in pathogens.
have been found to be very high, particularly in
areas with weak or no regulatory frameworks It is important also that scientists, practitioners
or poor enforcement, and in areas with high and policy-makers in both the health and
concentrations of API factories (Fick et al. 2009; biodiversity sciences engage more closely with
Larsson et al. 2007; Larsson 2010). food producers, pharmacologists, environmental
chemists and other relevant stakeholders to
Therefore, it is important that greater efforts are better understand and address the potential risks
made to understand, regulate and minimize the associated with APIs, and assist with identifying
potential for API release from the manufacturing cross-cutting indicators – including priority
sector, particularly in developing countries. species and ecosystems for future monitoring of
This should include advancement and uptake of potential impacts – to better facilitate cooperation
more environmentally friendly manufacturing and effective action. This should become an
methods and of technologies to remove APIs from integral part of wider efforts to mainstream a
wastewater streams, and greater focus on so-called sustainable development agenda into policies and
green chemistry – creating APIs that are “benign practice in the health-care sector (Vatovec et al.
by design” and inherently carry a low ecological 2013; Schroeder et al. 2013; Morgon 2015). This
risk (Daughton 2014). will become increasingly important in the face of
future social and environmental change.

Connecting Global Priorities: Biodiversity and Human Health 179

EDWARD N. JOHNSON

11. Traditional medicine

1. Introduction large sections of the population across the globe,
and the health and development goals of many
The contribution of biodiversity and ecosystem communities remain unrealized (Kim et al. 2013;
services to our health care needs is significant, both Anonymous 2008). Consequently, health-seeking
for the development of modern pharmaceuticals behaviour in both urban and rural contexts around
(Chivian and Bernstein 2008; Newmann and the world is increasingly becoming pluralistic or
Cragg 2007; see also chapter on contribution of a mix of different medical systems. For example,
biodiversity to pharmaceuticals in this volume) in Peru, the plant knowledge of patients both at
and for their uses in traditional medicine (WHO herbalist shops and allopathic clinics was largely
2013). Long before the rise of pharmaceutical identical. This indicates that traditional medicinal
development, societies have been drawing on knowledge is a major part of a people’s culture that
their traditional knowledge, skills and customary is being maintained, while patients also embrace
practices, using various resources provided to the benefits of western medicine (Bussmann 2013;
them by nature to prevent, diagnose and treat Vandebroek & Balick 2012; Vandebroek 2013).
health problems. Today, these practices continue Given the interlinked nature of conservation,
to inform health-care delivery at the level of local health and development, it is relevant to consider
communities in many places around the world community-focused approaches¹ that also address
(WHO 2013). In socioecological contexts such traditional health knowledge and conservation
as these, several resources used for food, cultural strategies as a way to complement mainstream
and spiritual purposes are also used as medicines health systems, and fulfil the basic human right
(Unnikrishnan and Suneetha 2012). Traditional to health and well-being.
medicine practices provide more than health care
to these communities; they are considered a way
of life and are founded on endogenous strengths, 1.2 Traditional medicine and biological
including knowledge, skills and capabilities. resources
Biological resources have been used extensively
Despite noteworthy advances in public health, for health care and healing practices throughout
modern health-care systems worldwide still do history and across cultures. Such knowledge is
not adequately meet the health-care needs of often specific to particular groups living in distinct

¹ A community here is defined as a group of people sharing a common ecosystem/landscape and associated knowledge.

180 Connecting Global Priorities: Biodiversity and Human Health

environments, and is usually passed on over use of faunal resources is not as profuse as that of
generations (Etkins 1988; 2001; Shankar 1992; plant resources, illegal poaching and unwise use of
Balick and Cox 1996; Vandebroek 2013; see also these resources for traditional medicine and hobby
the chapter on mental health in this volume). pursuits has also taken a toll on the population
and diversity of fauna (Milliken and Shaw 2012).
Traditional knowledge in health care can range Combined, the drivers of change pose a dual threat
from home-level understanding of nutrition, to wild species and to the livelihoods of collectors,
management of simple ailments (see also who often belong to the poorest social groups. In
the chapter on nutrition in this volume) or this chapter, we highlight the various dimensions
reproductive health practices, to treating serious related to the conservation of biological resources
chronic illnesses or addressing public health and promotion of traditional health-care practices,
requirements. In local communities, health illustrating the relevance of significant areas with
practitioners trained in traditional and non-formal case study examples.
systems of medicine often play an instrumental
role in linking health-related knowledge to
affordable health-care delivery (e.g. Stephens 2. Trends in demand for biological
et al. 2006; Montenegro and Stephens 2006; resources
Reading and Wien 2009). There are also formally Plants used in traditional medicine are not only
recognized practitioners of traditional medical important for local health practices, but also
systems, often referred to as complementary for international trade, based on their broader
and alternative medicine (CAM) practitioners, commercial use and value (Fabricant and
formally trained in different systems of medicine Farnsworth 2001). Globally, an estimated 60 000
such as Ayurveda, Traditional Chinese Medicine, species are used for their medicinal, nutritional
Kampo, Siddha, Tibetan medicine, Unani and and aromatic properties and, every year, more
several others (WHO 2002; WHO 2005, Bodeker than 500 000 tonnes (UN Comtrade 2013) of
et al. 2005; Payyappallimana 2010). Such systems material from such species are traded. A complete
have been institutionalized and integrated into list of all plants used in traditional medicine does
health systems in their respective regions or not exist, but at least 30 000 species of plants
countries. These have led to the evolution and with documented use are included in the Global
standardization of local pharmacopoeias that Checklist; an extension of earlier efforts of the
capture the uniqueness of biological diversity World Health Organization (WHO) and Natural
and cultural practices of specific socioecological Products Alert Database (NAPRALERT) WHO
regions, and have specific and well-organized Collaborating Centre at the University of Illinois in
epistemological bases. Chicago. It is estimated that the value of the global
trade in plants used for medicinal purposes may
Unfortunately, both biological products and health-
exceed US$ 2.5 billion, and is increasingly driven
related traditional knowledge are increasingly
by industry demand (UN Comtrade 2013).
threatened (Reyes-García 2010). Overharvesting,
land-use change, and climate change are among the Fauna and their products are also extensively used
major drivers of the decline in wild plant resources, in traditional medicine; assessments of the use
including those used commercially for food and of fauna and their products are mostly region-,
medicinal purposes (Hawkins 2008; FRLHT 1999; country- or taxa-specific (Alves and Alves 2011;
2009; Ford et al. 2010). Analysing the individual Nunkoo et al. 2012). A variety of animal body
and combined impact of these drivers on the parts and secretions are included in traditional
biological resources used for food and medicine medicine pharmacopoeia (Alves and Rosa 2005).
at different spatial scales is also an important Overall, in fact, there is often not a clear line
area for further research. Research in the area of between the consumption for food or medicine,
medicinal plants and climate change is already with some species also being consumed for their
emerging (e.g. Zisca et al. 2005, 2008). Although “tonic” properties.²

Connecting Global Priorities: Biodiversity and Human Health 181

 Increasingly, there is a reverse “re-engineering” or countries like India, it has been estimated that
“reverse pharmacology” process being undertaken approximately 80% of medicinal plants are
by researchers, where novel medicines or medical collected from the wild, leading to an increasing
therapies are being developed using traditional pressure on natural resources (FRLHT 1999;
processes. Furthermore, institutionalized 2009). Due to overharvesting and habitat loss,
traditional medicine manufacturers are investing approximately 15 000 species (or 21%) of the
in developing new products that are value additions global medicinal plant species are now endangered
over existing forms of medicinal formulations (Schippmann et al. 2006). With rising demand and
(Unnikrishnan and Suneetha 2012). reducing populations, problems of substitution,
adulteration and mistaken identities between
The demand for herbal medicines is rising species are also on the rise, as illustrated by the
drastically, fuelled by factors such as cost– example in Box 1.
efficacy and higher perceptions of safety. In

Box 1. Traditional medicine in a changing world: the example of Peru

The demand for traditional medicine is increasing in Peru, as indicated by the increase in number of
herb vendors in recent years, in particular, in the markets of Trujillo. A wide variety of medicinal plants
from northern Peru can also be found in the global market. While this trend might help to maintain
traditional practices and give recognition to traditional knowledge, it poses a serious threat, as signs
of overharvesting of important species are becoming increasingly apparent.

More than two thirds of all species sold in Peruvian markets are claimed to originate from the
highlands (sierra), above the timberline, which represent areas often heavily used for agriculture
and livestock grazing. The overall value of medicinal plants in the markets of northern Peru alone
reaches US 1.2 million/year. Medicinal plants contribute signi cantly to the local economy. Such
an important market raises questions around the sustainability of this trade, especially because the
market analysis does not take into account any informal sales.

Most striking, perhaps, is the fact that seven indigenous and three exotic species, i.e. 2.5% of all
species traded, account for more than 40% of the total sales volume. Moreover, 31 native species
account for 50% of all sales, while only 16 introduced plants contribute to more than a quarter of
all material sold. About one third of this sales volume includes all exotic species traded. None of
these species are rare or endangered. However, the rising market demand might lead to increased
production of these exotics, which in turn could have negative e ects on the local ora (Bussmann et
al. 2007b).

A look at the indigenous species traded highlights important conservation threats. Croton lechleri
(dragon s blood), and Uncaria tomentosa (cat s claw) are immensely popular at a local level, and
each contributes to about 7% to the overall market value. Both species are also widely traded
internationally. The latex of Croton is harvested by cutting or debarking the whole tree. Uncaria is
mostly traded as bark, and again the whole plant is normally debarked. Croton is a pioneer species,
and apart from C. lechleri, a few other species of the genus have found their way into the market.
Sustainable production of this genus seems possible, but the process must be closely monitored,
and current practice does not appear sustainable because most Croton is wild harvested. The trade

² http://www.traffic.org/wild-meat/

182 Connecting Global Priorities: Biodiversity and Human Health

 in cat s claw is so immense that, in fact, years ago collectors of this primary forest liana began to
complain about a lack of resources and it was found that often other Uncaria species, or even Acacia
species have appeared in the market as “cat s claw”. This is clearly not sustainable.

Some of the other “most important traditional medicinal” species in northern Peru are either
common weeds (e.g. Desmodium molliculum), or have large populations (e.g. Equisetum giganteum).
Nevertheless, a number of species are very vulnerable: Gentianella alborosea, G. bicolor, G. graminea,
Geranium ayavacense and Laccopetalum giganteum are all high-altitude species with very limited
distribution. Their large-scale collection is clearly unsustainable. In the case of Laccopetalum,
collectors indicate that nding supplies is becoming increasingly di cult. The fate of a number
of species with similar habitat requirements raises comparable concerns. The only species under
cultivation at present are exotics, and a few common indigenous species.

There are profound challenges when it comes to the safety of the plants employed, in particular,
for applications that require long-term use. Some studies found that various species were often
sold under the same common names. Some of the di erent fresh species are readily identi able
(botanically), but neither the collectors nor the vendors make a direct distinction between species.
Often, material is sold in nely powdered form, which makes the morphological identi cation of
the species in the market impossible, and greatly increases the risk for the buyer. The best way
to ensure correct identi cation would be DNA bar-coding. The necessary technical infrastructure
is, however, not available locally. The use of DNA bar-coding as a quality control tool to verify
species composition of samples on a large scale would require careful sampling of every batch
of plant material sold in the market. The volatility of the markets makes this a very di cult task
from a logistical standpoint. Furthermore, there is no consistency in the dosage of plants used, and
vendors do not agree on the possible side-e ects. Even in the case of plant species used for clearly
circumscribed applications, patients run a considerable risk when purchasing their remedies in the
local markets. Much more control is needed, as well as stringent identi cation of the material sold in
public markets, and those that enter the global supply chain via Internet sales.

While in-situ and ex-situ approaches to Notwithstanding the inclusion of multiple

conservation are adopted to address the loss of stakeholders in the implementation of
medicinal resources, the success of conservation conservation programmes, the sustainability of
strategies often depends on the comprehensive such initiatives is also dependent on the value of
involvement of different stakeholders. In this a resource that can be captured by the different
context, the example from India in Box 2 illustrates actors. It is possible to address some of these
the potential of in-situ conservation through concerns through market-based mechanisms such
public–private partnership (PPP) arrangements. as certification to foster sustainable use standards
for medicinal plants, as is being piloted through
the FairWild example (Box 3).

Connecting Global Priorities: Biodiversity and Human Health 183

 Box 2. Conservation and sustainable use of medicinal plants in India

It is estimated that in India, around 300 plants and a few faunal species are in various threat categories
and their cultivation is not yet a viable economic option due to the preference for wild sourcing,
given lower costs (FRLHT 2009). There is also a general lack of information on agrotechniques
(Hamilton 2004).

To address these pressing issues, the Foundation for Revitalisation of Local Health Traditions (FRLHT)
in India initiated the establishment of the largest global in-situ conservation network by establishing
medicinal plant conservation areas (MPCAs) – as an integrated approach to in-situ and ex-situ
conservation programmes. The rationale is to conserve and study medicinal plants in their natural
habitats and preserve their gene pool, and to further develop strategies for the management of
rare, endangered and vulnerable species. The areas not only provide a good locale for studies on
threat assessment, population studies and mapping, but also for participatory forest management, as
well as for policy-makers, the community and civil society organizations. Between 1993 and 2014,
FRLHT, jointly with the State Forest Departments, established 110 MPCAs across 12 Indian states
in a globally unique model of PPP. The programme has been spearheaded in collaboration with the
Indian Ministry of Environment and Forests, and through the support of organizations such as the
Danish International Development Assistance (DANIDA), United Nations Development Programme
(UNDP) and Global Environmental Facility (GEF). Due to its success, the Planning Commission of India
recommended the establishment of 200 MPCAs across the country (Tenth Five- ear Plan, 2002).
There is also a recent move to recognize these locations as biodiversity heritage sites. A related
initiative is the establishment of medicinal plant conservation parks (MPCPs) – a community-based
ex-situ conservation initiative aimed at sustainable use of medicinal plant resources and preserving
knowledge associated with their use. Coordinated by FRLHT along with other nongovernmental
organizations (NGOs) and community-based organizations, a chain of MPCPs has been set up in
various parts of India. Attempts have also been made in pilot locations to integrate such medicinal
plant-based practices in formal primary health-care centres, apart from promoting them through
community health programmes. Within a geographical region, communities have been mobilized to
create:

• ethnomedicinal forests and resource centres housing herbaria and crude drug collections;

• local pharmacopoeia databases based on community knowledge;

• community and home herbal gardens and seed banks;

• outreach nurseries for the promotion of cultivation and a sustainable wild collection of medicinal
plants;

• trade and enterprise development that aids in income generation.

Moving up the value chain, FRLHT also established a medicinal plant conservation network (MPCN)
jointly with a number of NGOs working with di erent rural communities. As part of this e ort,
traditional healers associations have been formed at di erent levels of administration from the
province downwards. The associations conduct regular meetings and exchange of information

³ See: http://planningcommission.nic.in/plans/planrel/fiveyr/10th/volume2/10th_vol2.pdf
⁴ See: http://mpcpdb.frlht.org.

184 Connecting Global Priorities: Biodiversity and Human Health

among healers and act according to self-regulatory guidelines, which have been evolved through a
participatory process based on the contextual peculiarities of each province. Healers associations
along with NGOs and forest departments have been actively engaged in supporting medicinal plant
conservation programmes in various states.

The MPCN is also working on the following issues:

• establishing herbal gardens;

• developing appraisal systems of healers capacities and training programmes;

• conducting action research interventions in key health areas such as malaria;

• facilitating networking through organizing medical camps, and district- and state-level conventions
of healers associations, but also healer exchange visits within the country and among other Asian
and African countries.

Box 3. Sustainable harvest and standards – The FairWild Standard example

The FairWild Standard provides a set of best practice guidelines for the sustainable use and trade
of wild harvested medicinal plants. It provides a basis for assessing the harvest and trade of wild
plants against various ecological, social and economic requirements. It was developed through
a multistakeholder consultation process that has engaged a wide range of organizations and
individuals involved with the harvesting and trade of these resources.

Use of the FairWild Standard helps support e orts to ensure that plants are managed, harvested
and traded in a way that maintains populations in the wild and bene ts rural producers. Version
2.0 of the Standard was developed following the merger of two initiatives: International Standard
for Sustainable Wild Collection of Medicinal and Aromatic Plants (ISSC-MAP), which focused on
ecological conservation and some social/ethical aspects, and the original FairWild Standard, which
focused on social and fair trade aspects. The resulting set of principles and criteria covers eleven key
areas of sustainability. It is designed to be an applicable framework in a variety of implementation
contexts, as well as to be used as the basis for a third-party certi cation scheme.

During the development of the FairWild Standard, a number of pilot projects were carried out in
locations around the world to test its applicability. These projects included the collection of ingredients
used in traditional medicine; for example, the pilots of ISSC-MAP in India under the project “Saving
Plants that Save Lives and Livelihoods”, supported by the German Federal Ministry for Economic
Cooperation and Development (BMZ), and implemented by FRLHT and TRAFFIC India. One of the
rst studies was conducted in Karnataka, India. Through a participatory planning approach involving
various stakeholders such as scientists and community members, a task team was set up for mapping
resources and elaborating a sustainable harvesting strategy. As part of the methodology involved
documentation of medicinal plant-related knowledge and non-timber forest product (NTFP) collection
practices, resource assessments were conducted for selected species. Training was provided for
mapping and assessing di erent harvesting methods. It was found that a well-organized stakeholder
group can plan and implement an e ective participatory resource management strategy. Apart from

Connecting Global Priorities: Biodiversity and Human Health 185

 standardizing and eld-testing the methodology, training modules for wider user groups have been
developed. This will be a useful strategy for biodiversity or joint forest management committees
through a community-to-community training programme (Unnikrishnan and Suneetha 2012).

Innovation with the FairWild Standard continues in India, with a certi cation pilot now under way
in the Western Ghats. With nancial support from the United Kingdom (UK) s Department for
International Development (DfID)/Department for Environment, Food and Rural A airs (DEFRA)
Darwin Initiative and the Keidanren Nature Conservation Foundation, the project intends to increase
the capacity of targeted local communities to adapt to climate change and participate in biodiversity
conservation through the improved management of socioecological landscapes. It is implemented
by the Durrell Institute for Conservation and Ecology (DICE), the Indian NGO Applied Environmental
Research Foundation (AERF), UK manufacturer Pukka Herbs Ltd. and TRAFFIC. The project aims to
establish supply chains for sustainable harvesting and fair trade in fruit of two tree species used
in Ayurvedic medicine (Terminalia bellirica and T. chebula). A FairWild certi cation protocol is to be
developed for the collection of these species and for establishing a community-regulated mechanism
for access and bene t sharing.

The FairWild Standard has also been implemented in other countries of Asia, South America, Africa
and Europe (Kathe et al. 2010). In addition to being used by communities for the management of
medicinal plant resources, the principles of the FairWild Standard can be used by industry for the
development of a sourcing policy to support the development and/or strengthening of national
resource management policies and regulations. Of particular relevance to the topic of biodiversity
and traditional health is a project that is currently under way as part of the European Union (EU)–
China Environmental Governance Programme, which experiments with promoting the adoption of
sustainable sourcing according to the FairWild Standard in the traditional Chinese medicine sector, as
part of a corporate social responsibility framework. In the international arena, it has also been drawn
upon in the development of best practice methodologies for carrying out non-detriment ndings
(NDF) by the Convention on International Trade in Endangered Speciesof Wild Fauna and Flora
(CITES), and as a practical tool for implementing and reporting against the sustainable use objective
of the Global Strategy for Plant Conservation (GSPC), as well as the Convention on Biological Diversity
(CBD) s Aichi Targets 4 and 6.

2.1 Socioecological systems landscapes and related traditional knowledge

practices make important contributions to health
The survival and vitality of knowledge and
and well-being, therefore necessitating a close
resources depend on the sociocultural contexts
inquiry into the functional interlinkages within
in which they are embedded. Typically, such
such systems, and maintenance of their dynamism
knowledge and resources are found to be most
(Unnikrishnan and Suneetha 2012; Posey et al.
vibrant among communities (specifically,
2000; see also the chapter on mental health in
indigenous and local communities) close to
this volume). Highlighted below is the case of
culturally important landscapes. These could
the Mayan people and their relationship with
relate to socioecological production landscapes
nature and resources. A sensitive understanding
(e.g. satoyama in Japan) or conservation systems
of the cultural ties between societies and nature
(e.g. sacred groves, ceremonial sites) or therapeutic
is required to ensure sustainability of both
landscapes (e.g. sacred healing sites). Such
knowledge and practices.

186 Connecting Global Priorities: Biodiversity and Human Health

Box 4. Therapeutic and sacred landscapes

Mayan people maintain a healthy or whole relationship with mother earth and the cosmos through
an intricate system of practices and knowledge known as Maya Science (Monterroso & Azurdia Bravo
2008). This divine relationship is enacted by the measure of time using the stars and constellations
but also through the use of sacred sites and traditional medicine (Gomez & Caal 2003). The sacred
sites (natural and constructed) are places to connect with the ancestors and to contemplate one s
role in relation to the social and natural world, but they are also places for healing in the landscape
(Gomez et al. 2010). In Guatemala as well as in many other countries, these sacred places are often
viewed as a biocultural network that spans land and seascapes, and embody a spiritual dimension
of well-being and often underrecognized healing potential (Dobson & Mamyev 2010; Delgado et al.
2010; Verschuuren et al. 2014).

Reyes-García (2010) reviewed the literature on traditional medicine and concluded that the holistic
nature of traditional knowledge systems helps to not only understand a plant s e cacy in its cultural
context but also improves our understanding of how ethnopharmacological knowledge is distributed
in a society, and who bene ts from it. In Guatemala, spiritual leaders, midwives, paediatricians,
naturopaths, and other traditional healers help counteract the various health problems in
communities. To the traditional Mayan healer, the body is composed of the sacred elements; earth,
water, re and air, which correspond to the sun, moon and stars. Therefore, use of traditional medicine
is practised based on the date of birth in the sacred Mayan calendar (Monterroso & Bravo 2008).

Within the context of the Mayan calendar, traditional healers know that diseases stem from the
spiritual, physical and psychological imbalance of a person, either from wilful violation of proper
conduct or due to lack of awareness. Due to colonization and consequent impacts on local and
indigenous communities, many traditional practices are fragmented and often combined with
elements of western medicine. They are often under ideological pressure and suspicion for the
lack a homogeneous theory, while resource scarcity is also an increasing problem underlying the
production of many traditional medicines (Delgado & Gomez 2003). Viewing these problems as part
of the erosion of cultural knowledge and practices can help in determining suitable and culturally
appropriate solutions. For example, Pesek et al. (2009), who researched Maya eqchi knowledge on
medicinal plants and their ecosystems, concluded that traditional ways of protecting plant diversity
were better suited to medicinal plant conservation than external conservation solutions based on
conservation biology.

Garcia et al. (1999) describe how Mayan medicine in Mexico was reinforced by systematizing the
knowledge and experience of 40 traditional healers, and comparing these with other medical
traditions, such as Chinese health systems. Striking similarities were encountered, both in concepts
as well as practices, such as acupuncture, massage and the use of certain herbs and spiritual
healing techniques. This was used to reinforce the local traditional health system, as well as to
disseminate the experiences among traditional healers elsewhere in Central America. The exchange
of healers knowledge and practices is generally valued as an invigorating experience that can also
provide a platform for the legal recognition of traditional health practitioners (Traditional Health
Practioners 2010).

Connecting Global Priorities: Biodiversity and Human Health 187

 3. Traditional medicine and community health is understood as filling a gap
traditional knowledge at a in access to modern health care. However, it has
to be recognized that in most societies they do
crossroads play a critical complementary role in parallel with
With increasing urbanization and integration the mainstream health system, an aspect that
of mainstream worldviews, communities needs to be better appreciated. This calls for a
often experience alienation from the natural multipronged approach where various resources
environment (Roe 2010). Cultural systems, need to converge, including those related to local
including traditional health-care practices, are health traditions. Experiences over the past two
concomitantly being eroded. As a result, despite decades show that there is high relevance in
the wealth of traditional knowledge that exists, aligning biodiversity conservation goals with a
the practice of traditional medicine is declining community health approach (Miththapala 2006).
(Payyappalli 2010). This is further accentuated
by institutionalized education systems that often The customary absence of comprehensive
fail to recognize the relevance of these practices, approaches to assess the role, economic potential
thereby distancing younger generations from and policy implications of traditional knowledge
exploring such areas (Battiste 2010). The dominant have also been noted as key reasons due to which
education and research systems tend to emphasize traditional cultures are frequently disregarded in
knowledge and technologies with universal development programmes, making sustainable
standards, rather than supporting the needs of development objectives among vulnerable
specific regions or populations, and available populations more difficult to attain (Jenkins
resources and capabilities (Haverkort et al. 2003). 2000; Haverkort 2003). These issues must all be
A large part of traditional medical knowledge is considered in the context of a global health sector,
experience based and passed on through the which predominantly relies on universal models of
oral tradition, and such knowledge is not easily modern medicine, and continues to be inadequate
transmitted in classroom-based learning. The for large sections of the population around the
institutionalized traditional medical knowledge globe.
either gets harmonized with mainstream systems
or is not adequately integrated in public health New policy forums, such as the Intergovernmental
care (Bodeker and Burford 2007), which indicates Platform on Biodiversity and Ecosystem Services
inefficient use of knowledge and trained human (IPBES), are exploring ways of including traditional
resources. and mainstream perspectives and methods to
undertake an assessment of biodiversity and
Access to essential modern health care continues ecosystem services, and consequent impacts
to be a major challenge in many parts of the on human well-being. Guidance on the need to
world. Infectious diseases (such as HIV, malaria, understand different kinds of values held by people
tuberculosis, pneumonia, diarrhoeal diseases towards biodiversity and ecosystem services to
and several other neglected conditions), coupled inform methods of valuation and assessment
with chronic noncommunicable diseases (such as are being developed, with a specific focus on
diabetes and ischaemic heart disease), persistently adequate attention to public health (www.ipbes.
affect lives in these regions (see also the infectious net). This calls for stronger partnerships between
disease chapter in this volume). Indomitable stakeholders.
challenges such as high maternal and child
mortality, and emerging and re-emerging diseases A number of leading international NGOs are
(infectious, chronic, and lifestyle-related), are conducting capacity development activities for
typical constraints to well-being. For these reasons, traditional health practitioners, such as training,
the role of traditional health-care practitioners in and facilitating networks. One of these NGOs
is the Promotion of Traditional Medicines

⁵ See: http://www.prometra.org/representations_nationales/uganda.html

188 Connecting Global Priorities: Biodiversity and Human Health

(PROMETRA),⁵ which has been working to alleviate 4. Strengthening traditional
poor health conditions and services utilizing health practices and addressing
traditional medicine since 1971. Its unit in Uganda
conducts a wide range of capacity development
loss of resources
activities for healers, addressing issues such as To date, there have been several concerted efforts
exposure to potential value addition and income in the international arena to promote both the
generation activities, culturally sensitive disease conservation of biological resources, as well as
prevention and management of environmental traditional knowledge. What has been lacking,
conservation. A unique initiative includes training however, is a comprehensive effort to emphasize
programmes designed for healers and youth from the linkages between these elements using an
communities on the use of traditional medicinal integrated approach that draws on traditional
resources and practices under the banner of knowledge to complement and supplement
Buyijja Forest Schools. PROMETRA also works modern health-care systems.
on integrating traditional medicine in national
health systems to improve free choice of medicine With the Earth Summit and adoption of the
for citizens, protect biodiversity and participatory Convention on Biological Diversity (CBD) at Rio
forest management, promote research on de Janeiro in 1992, significant steps were taken
medicinal plants, protect traditional knowledge towards political recognition of the relevance of
and reinforce institutional capacities of civil traditional knowledge. In compliance with Article
society organizations for a healthy environment 8 (j) of the Convention, the respect, preservation
and sustainable development. Another relevant and maintenance of traditional knowledge, and
best practice example is “Friends of Lanka” based innovations and practices of indigenous and
in Sri Lanka. It has promoted documentation local communities are related to the recognition
of practices, and research and networking of of the practices by these communities of their
traditional health practitioners. For this reason, traditional knowledge. Other important aspects
around 75 healers have been identified among a of these obligations include promoting the wider
population of 8000, who treat various conditions application of such knowledge, innovations and
such as snake- and insect bites and certain food or practices with the approval and involvement of
natural poisons, which are considered as leading knowledge holders; and encouraging the equitable
causes of morbidity and mortality in rural areas sharing of the benefits arising from the use of
of developing countries. Friends of Lanka also such knowledge, innovations and practices.
formed an association of healers, which initiated These obligations are also applicable to traditional
an assessment of natural resource availability, and medicine as it relates to traditional knowledge.
methods for conservation and sustainable use Furthermore, Article 10 (c) of the CBD states that
through home and community gardens. Parties shall, as far as possible and as appropriate:
“Protect and encourage customary use of biological
Networks such as the MPCN and associations resources in accordance with traditional cultural
of healers established within its framework are a practices that are compatible with conservation
successful approach to facilitating knowledge and or sustainable use requirements.”
experience exchange among traditional healers
nationally, regionally and internationally, resulting Principle 22 of the Rio Declaration on Environment
in better health and conservation outcomes. and Development calls for the recognition of, and
respect for the knowledge and practices of local
and indigenous communities in environmental
management towards the achievement of
sustainable development.⁶ Agenda 21 further
specifically calls for an appropriate integration of

⁶ The full text of the Rio Declaration is available at: http://www.un.org/documents/ga/conf151/aconf15126–1annex1.htm

Connecting Global Priorities: Biodiversity and Human Health 189

 traditional knowledge and experience in national Many users of traditional medicines and
health systems, and for conducting research into practitioners claim that the effect of a treatment
traditional knowledge related to preventive and is obvious when there is an improvement in the
curative health practices (Chapter 6 of Social health status.⁷ However, most ailments tend to get
and economic dimensions – protecting and better over time even without any care. In clinical
promoting human health) (United Nations 1993). studies (with human subjects), observations are
Over the past six decades, two areas where the organized in a way that makes it possible to know
contemporary relevance of traditional knowledge whether observed outcomes can be attributed to
has been fairly well acknowledged include the a given treatment. This can be obtained through a
management of the environment and natural dose-escalating prospective study (comparing
resources, and the delivery of health care (WHO outcomes with different doses of a treatment), or
2002, 2005, 2013). The need to re-integrate with the leading benchmark of medical research
traditional medical approaches into healthcare and evidence-based medicine: a randomized
armamentarium is gaining more political and controlled trial.
social acceptance (UN 2010).
Before doing so, it is relevant to determine
which is the best among the various treatments
9DOLGDWLRQVDIHW\DQGHƫFDF\RI
used to treat the same ailment in a population.
traditional medicine
The “bedside-to-bench” approach has been used
When a traditional recipe is scientifically with some success to answer this question; it is
validated in terms of safety and effectiveness, based on precise clinical information on real cases
and is affordable, available and sustainable, it and statistical analysis of correlations between
provides valuable information. It may lead to an treatments and outcomes (Willcox et al. 2011).
officially recommended phytomedicine as well as The clinical effects of medicinal plants should be
improvement in the provision of health services studied using sound methods that are, insofar as
to households. In both cases, the aim remains to possible, the same as or compatible with methods
improve the quality of care in the community. used for testing conventional medicines. This
could produce results that are understandable
Integration of modern and traditional treatments and more widely acceptable to the scientific
is common today. Plural therapeutic itineraries community, health professionals and policy-
are followed by large numbers of those seeking makers. It can also provide information useful for
care.  However, this process is often disordered the quality of care in the community. However, it
and defined by factors completely extraneous is also important to acknowledge that traditional
to a rational choice of effective and safe formulations might sometimes require testing
treatment.  Scientific and clinical studies may within traditional epistemologies and methods,
provide essential information to adequately to avoid the potential misrepresentation of
respond to the situation. Research strategies can effectiveness due to incommensurability of
be based on various methods such as intercultural methods (Shankar et al. 2007). The examples
population studies, historical accounts or in Boxes 5, 6 and 7 illustrate examples of good
biological tests. Beginning with a collection of practices in Palau, Mali and India to validate and
clinical data during ethnopharmacological field revitalize traditional medicinal practices, mindful
studies may be a good start. of the safety, quality and efficacy of the practices,
and an inclusive approach with practitioners of
traditional medicine.

⁷ This observation is based on field work conducted by the authors of this chapter.

190 Connecting Global Priorities: Biodiversity and Human Health

 Box 5: Participatory approaches to validation: experiences from Palau and Mali

A relevant example linking traditional medicines and noncommunicable diseases (NCDs) is the
survey performed in Palau on traditional medicines (or health practices) and NCDs – chie y diabetes
and high blood pressure. A nationwide survey was carried out to determine which traditional
medicines are most commonly used to treat these conditions, and what was the perceived
e ectiveness. Data were collected as part of a training course on scienti c research. A distinctive
feature of the results obtained was that, among 30 plants used for diabetes, two were the most
common (Table 1).

Table 1: Ingredients of traditional treatments most commonly used for diabetes

(mentioned 4 times, among 45 respondents with diabetes) in Palau (unpublished, 2014)

No. of reported N (%) reported “lower

Name of the plant Palauan name uses sugar level in blood”
Phaleria nisidai delal a kar 13 6 (46%)
Vitex trifolia kelsechedui 4 1 (25%)
Scaevola taccada korai (kirrai) 4 1 (25%)
Morinda citrifolia ngel/noni 12 0 (0%)
Phyllanthus palauensis ukelel a chedib 4 1 (25%)

The di erence between the reported outcomes with the two most commonly used plants was
statistically tested. When comparing reported outcomes of P. nisidai and M. citrifolia, P. nisidai was
statistically more often associated with the reported outcome “lower blood sugar” (P=0.01). None of
the patients using M. citrifolia reported the outcome “lower blood sugar”, even though this plant was
the second most frequently used.

Following the identi cation of P. nisidai through this brief survey, a literature search was performed
to identify a potential link between the results obtained and what is known about the antidiabetic
properties of the plant. It was found that the high mangiferin content of P. nisidai could explain the
observed e ects. Indeed, in vitro and animal studies on this substance showed improvement in the
glucose tolerance test, inhibition of alpha amylase, alpha glucosidase and dipeptidyl peptidase IV (as
with some of the most recent antidiabetic drugs), increased insulin secretion and a hypolipidaemic
e ect (Kitalong 2012).

In a study on traditional treatments for malaria in Mali, use of the retrospective treatment outcome
(RTO) method resulted in a database of treatments taken for malaria cases in 952 households. From
the 66 plants used, alone or in various combinations, one was clearly associated with the best
outcomes: a decoction of Argemone mexicana (Table 2) (Diallo et al. 2007).

⁸ For a review of herbal medicines used to treat diabetes, see also Rao et al. 2010.

Connecting Global Priorities: Biodiversity and Human Health 191

 Table 2: Correlation between plants used and reported outcome in a study on
traditional treatments for malaria in Mali

Total number of % Healed P (Fisher

Plant people used on Healed Failed (95% CI) exact)
Argemone mexicana 30 30 0 100% Reference
(88–100)
Carica papaya 33 28 5 85% 0.05
(68–95)
Anogeissus leiocarpus 33 27 6 82% 0.03
(64–93)

The recipe that showed the best outcomes in patients, a single plant in its traditional mode of
preparation and utilization, was selected for a further dose-escalating observational study, followed
by a randomized, prospective, comparative clinical trial (randomized controlled trial with the selected
local remedy versus the standard, imported treatment). After these clinical studies, the search for
active compounds was undertaken. The whole research process was labelled “reverse pharmacology”
or, more speci cally, “bedside-to-bench” approach.

Box 6: Traditional antimalarials – RITAM experience

There are a number of successful models and programmes for preventive and curative health
interventions that use traditional medicine and practices to achieve the desired goals. In the eld
of malaria treatment, there is the Research Initiative on Traditional Antimalarial Methods (RITAM),
which was initiated in 2001 (Willcox et al. 2003; Willcox & Bodeker 2004 www.gifts-ritam.org). This
initiative is based on a group of international researchers exploring ways to increase the relevance
of including traditional medicine in the repertoire of choices available for the prevention and cure
of malaria. As such, RITAM is working on traditional antimalarials with more than 200 members from
over 30 countries. A systematic literature review by RITAM indicates that numerous plant species
are used to treat malaria or fever. In India, FRLHT has been assessing the e ectiveness of traditional
medicine for malaria prevention through a participatory community-based approach. This includes
conducting a literature survey on plant drugs used for malaria management, as well as documenting
traditional antimalarial remedies and dietary rules for malaria prevention. Finally, pharmacological
references of the toxicology and e cacy of these practices from Ayurvedic and modern medical
literature are compiled. As part of FRLHT s malaria prophylaxis approach, communities in selected
endemic areas follow a regimen of malaria prevention (mainly consisting of an herbal decoction)
during the monsoon season for a selected period. The safety of the practice is assured and the
remedy is prepared fresh on speci c days at a community centre. By using a cohort study approach,
groups based in several regions that do not follow this regimen are compared with those that do.
Data gathered in the documentation has shown positive results for malaria prevention, indicated by
statistically signi cant positive outcomes.

192 Connecting Global Priorities: Biodiversity and Human Health

The case of the RITAM initiative (in Box 6) in traditional systems of medicine (Fabricant
highlights that utilizing traditional medical and Farnsworth 2001). According to WHO,
knowledge through community -based approximately 25% of these are plant derived.¹⁰
participatory approaches is feasible and urgently Health-related traditional knowledge has been
needed to find solutions to the continuing high commonly accessed for developing new medicines,
incidence of preventable and curable diseases such although knowledge, practices and resources have
as malaria in regions where it is endemic. This also often been misappropriated (Timmermans 2003).
requires the consideration of ethical factors, e.g. The extent to which traditional medicine can guide
free, prior and informed consent (Unnikrishnan drug discovery has been subject to controversy,
and Prakash 2007). Home herbal gardens is a contributing to fluctuations in investment in
successful model to promote access to health care bioprospecting informed by ethnobotanical data
through sustainable natural resource management (Saslis-Lagoudakis 2012).
of medicinal plants.⁹ According to observations,
it has successfully reduced poverty in rural areas 5.1 Databases for health-related
and revived local knowledge of medicinal plants traditional knowledge
and traditional health practices. Today, 200 000
home gardens across 10 states in India are used to Searchable databases for health-related traditional
meet the primary health-care needs of some of the knowledge, which ensure the protection of
poorest households, while reducing their health related resources and knowledge, are currently
expenditure. A majority of participants are now being developed. A unique database project is
contributing fully to meet the costs of raising their the Traditional Knowledge Digital Library, which
medicinal plants. Some studies show that there is was developed through collaboration between
substantial health cost saving due to the use of the Council for Scientific and Industrial Research,
home remedies (e.g. Hariramamurthi et al. 2006; the Indian Ministry of Science and Technology,
Bode and Hariramamurthi 2015). and the Ministry of Health and Family Welfare
(Department of AYUSH). An interdisciplinary
team of experts from Ayurveda, Uniani, Siddha
5. Challenges to the protection of and Yoga as well as from information technology
traditional medical knowledge (IT), law and scientists manages the digital library.
Many pharmaceutical drugs used today have It involves documentation of the traditional
been derived from plants that were initially used knowledge available in the public domain in the
form of existing literature related to Ayurveda,

Box 7: Home herbal gardens as a self-reliant community health programme

A self-reliant approach to managing simple, common health conditions can reduce the health
expenditure of poor rural households and rural indebtedness in many developing countries (Van
Damme et al. 2003). Home herbal gardens, as conceived by the FRLHT, are a collection of 15–20
prioritized medicinal and nutritional plants, and have become a successful model for a self-reliant
community health programme. Apart from being a conservation milieu for medicinal plants, it also
addresses nutritional challenges. In most rural communities, knowledgeable women take care of
certain primary health needs of the family members and the gardens become a handy resource for
them. Some women, by taking on the role of suppliers of seedlings for the programme, also earn
supplementary incomes.

⁹ For other health benefits of home gardens, see also the nutrition chapter in this volume.
¹⁰ http://www.who.int/mediacentre/factsheets/fs134

Connecting Global Priorities: Biodiversity and Human Health 193

 Unani, Siddha and Yoga, in digitized format in by virtue of international and national laws,
five international languages: English, German, and provide a self-description of the community
French, Japanese and Spanish. Furthermore, profile, their resources, rights and responsibili-
for the purpose of systematic arrangement, ties. They also provide an indication of the terms
dissemination and retrieval, the Traditional of engagement with external agents. These doc-
Knowledge Resource Classification, an innovative uments therefore can be viewed as legal tools to
structured classification system, has been foster protection of the rights of communities.
developed for about 25 000 subgroups related to
medicinal plants, minerals, animal resources, their These databases are useful for exemplifying
therapeutic uses, clinical applications, methods of the value of encouraging the development and
preparation, modes of administration, etc. improvement of community knowledge registers
and biocultural protocols, and linking them with
By providing information on traditional national databases for protection. They also show
knowledge existing in the country, in languages that it is necessary to build on and scale up good
and formats comprehensible to patent examiners practices of ethical and equitable agreements
at international patent offices, the database with international collections and industries
contributes significantly to preventing the grant of related to the use of traditional knowledge and
wrong patents. In parallel, various organizations natural resources for research or commercial
are undertaking a similar exercise to document purposes. Moreover, despite all their inherent
oral knowledge or knowledge in the informal challenges, web-based databases can also be an
domains through the development of community important tool for the exchange of information
knowledge registers. Chiefly led by NGOs, these between ethnopharmacological studies and the
registers attempt to rally community members public, and for the dissemination of information
to discuss and document their knowledge and between researchers, planners and other users
practices in different categories of resource use (Ningthoujam et al. 2012).
or practices based on two premises: (1) that by
documentation, they establish prior art over the More recent trends show a process of “reverse
knowledge and resource use, and (2) it promotes engineering”, where traditional processes and
greater use and practice of the knowledge within methods are deployed for the development of
the community, eventually reinforcing such use as mainstream novel products. This again raises
strong social traditions. questions of the commensurability of attributions
to existing knowledge with the novelty definitions
Community biodiversity registers have been devel- of intellectual property laws.
oped and promoted as sui generis documentation
systems to protect biodiversity-related tradi- As most of the traditional environmental and
tional knowledge (Gadgil et al. 2000). These have medical knowledge among communities is oral
been incorporated in the national laws of various in nature, revival of the social processes of their
countries. In India, for example, these registers generation, preservation and transfer within
have been further executed through biodiver- communities needs to be well studied, despite
sity management committees (the lowest level of all the inherent challenges associated with this.
governance unit) that are engaged in systematic Furthermore, traditional medical knowledge
documentation of local resources and knowledge. can inspire industrial research and development
More recently, communities have been articulating processes in bioresource-based sectors, which
their rights over their knowledge and resources by require mechanisms to secure appropriate
developing their own biocultural community pro- attribution and sharing of rights and benefits with
tocols. Defined by communities, these highlight knowledge holders, as set out in the text of the
the legal rights that are vested in communities CBD and the Nagoya Protocol on Access to genetic

194 Connecting Global Priorities: Biodiversity and Human Health

resources and equitable sharing of benefits arising integrate these issues while raising the capacities
from their commercial utilization.¹¹ The example of multiple stakeholders in achieving better public
in Box 8 illustrates an initiative that attempts to health outcomes in Africa.

Box 8: Capacity building on plant research for better public health in Africa

The Bamako Global Ministerial Forum on Research for Health organized by WHO was held in November
2008 to strengthen research for health, development and equity. The Bamako call to action notably
prioritized the development of policies for research and innovation in health, especially related to
primary health care and the strengthening of research capacity by building a critical mass of young
researchers (WHO 2008). It was this call to action that led to the creation of the Multidisciplinary
University Traditional Health Initiative (MUTHI): Building Sustainable Research Capacity on Plants for
Better Public Health in Africa, initiated in anuary 2010 and set to be nalized in December 2014.

The MUTHI project was established with European Union funding (Framework 7 Programme) to build
more sustainable plant research capacity and research networks between key institutions in Africa
(Mali, South Africa and Uganda) and a group of partner research institutions in Europe (Norway, UK
and the Netherlands) to attain better health in Africa (MUTHI 2013). The project has provided a four-
year capacity-building programme, in which African researchers are trained in all the necessary
skills to produce and commercialize safe and standardized improved traditional medicines (ITM),
and are trained in intellectual property rights (IPR) regulations and principles of access and bene t-
sharing (ABS). The project is based on the needs of the African partner institutes to strengthen their
ethnopharmacological research capacities in the area of ITM.

For more e ectiveness, the MUTHI project has been divided into work packages that each focus on
a di erent aspect of the project: (1) training in medical anthropological and ethnopharmacological
research skills to conduct high-quality ethnobotanical and ethnopharmacological research on
medicinal plants; (2) quality control of phytomedicines and nutraceuticals; (3) investigative
bioactivity and safety of phytomedicines and nutraceuticals, with the objectives of assessing
the needs of African institutes and developing the capabilities of researchers for bioassays, data
management, quality assurance, bioactivity evaluation, safety aspects and developing guidelines; (4)
identify researchers needs for clinical and public health training, and build the capacity of traditional
medicine researchers on all aspects of the subject, including writing and data analysis; (5) examine
ethics and IPR, aiming to assess training and education requirements for stakeholders on IPR,
biodiversity legislation and regulation, ABS, and ethics of traditional medicine and research methods
(Bodeker et al. 2014, Bodeker et al. 2015). A sixth work package is charged with project management.

The benchmark referenced in the MUTHI project is the Code of Ethics of the International Society
of Ethnobiology (ISE), initiated in 1996 and completed in 2006. Contrary to other frameworks, the
ISE Code of Ethics addresses the rights of the individual knowledge holders. Participants of the
rst work package conducting an ethnobotanical and retrospective treatment outcome study have
been trained through workshops focused on research skills, ethics and IPR, and have received
online guidance in writing their research proposals, including a section on research ethics and free
prior informed consent (FPIC). The latter had to be established at individual and collective levels,

¹¹ The Nagoya Protocol on Access to genetic resources and equitable sharing of benefits arising from their commercial utilization
(Nagoya Protocol), adopted by the Tenth Conference of Parties to the CBD, was concluded on 29 October 2010 in Nagoya,
Japan. It provides the framework to facilitate access and benefit sharing. See http://www.cbd. int/nagoya/outcomes/

Connecting Global Priorities: Biodiversity and Human Health 195

 as determined by community governance structures before the start of the research. The a ected
communities were provided with complete, comprehensive information regarding the purpose and
nature of the proposed programme, project, study or activities, the probable results and implications,
including all reasonably foreseeable bene ts and risks of harm (be they tangible or intangible)
to a ected communities. The work package team that is responsible for all aspects related to IPR
and ABS within the MUTHI project provided a needs assessment followed by workshops on ethics
and IPR, and mentored participants from all of the partner countries in developing memoranda of
understanding between researchers and traditional healers, including aspects related to FPIC and
ABS. The drafting phase of the memoranda of understanding was an ongoing process between the
researchers and traditional healers in order to reach a nal memorandum of understanding approved
by all stakeholders (Bodeker et al. 2015).

6. Ways forward of different agencies to synergize multiple

efforts to achieve biodiversity conservation, and
Despite the multiplicity of policies, goals and
health and development, especially at the local
targets to address health, environment and
levels of implementation. Launched as a global
development challenges, we are still far from
multistakeholder initiative in 2012 during the
achieving the stated objectives of policy forums,
eleventh Conference of the Parties to the CBD
chiefly because of a lack of synergy and integration
in Hyderabad, India, it primarily aims to develop
in policy implementation. Moreover, mainstream
and mainstream community health approaches by
health sector practices often continue to neglect
supporting traditional knowledge and biodiversity
broader determinants of health or intersectoral
conservation, and promoting the sustainable use of
linkages to health. There is increasing recognition
biological resources by building on lessons learned.
from the academic community and public alike
It also aims to exchange knowledge with partners
that no single system of knowledge can solve
from both the government and nongovernment
the mounting problems of humanity (Rai et al.
sectors, as well as international organizations.
2010; Bodeker and Burford 2007), and a more
comprehensive multidisciplinary and pluralistic The Initiative underscores the role of the
strategy is needed. ecosystem as a reliable and low-cost service
provider, and supports sustainable natural
One possible way forward to address the
resource management. It also revitalizes effective
interconnected issues of conservation (of
traditional medical knowledge and local remedies
knowledge and biological resources), and
by developing knowledge, skills and capabilities
equitable and affordable health-care provision
of the populations living in close proximity to
is to undertake an integrated approach with the
biological resources. Under the coordination of
full involvement of communities. However, there
the United Nations University Institute for the
is no universal way to achieve this goal and no
Advanced Studies of Sustainability (UNU-IAS), the
homogeneous methodology that can be applied
BaCH is simultaneously addressing the following
(Wage et al. 2010). Traditional knowledge on
objectives: (i) the integration of conservation
health and biological resources is by its very nature
priorities in health system planning; (ii) raising the
context specific. Culturally sensitive and locally
contemporary relevance of traditional medicinal
appropriate approaches are required (see also the
practices; (iii) identifying and piloting best
chapter on mental health in this volume).
practices for local innovations through livelihood
programmes and for self-reliant health systems;
Some multipartner initiatives, such as the
and (iv) operationalizing a comprehensive health
Biodiversity and Community Health (BaCH)
and well-being approach by working with relevant
Initiative, attempt to pool the individual strengths
stakeholders and actors.

196 Connecting Global Priorities: Biodiversity and Human Health

6.1 Innovations and incentives traditional knowledge resources, prevention of
their erosion and linking them with scientific
It is important to leverage and strengthen the
research are related areas that also need further
high patronage for traditional medical care to
attention.
improve public health outcomes and achieve the
reemerging broader objectives of “Health for All” The value chains of traditional medicine and,
(WHO 1998) and “Good Health at Low Cost” generally, medicinal resources are often linked
(Balabanova et al. 2013). This requires enabling to various sectors, with much of the primary
decentralized approaches that allow better supplies provided by local communities reliant
access to health care, are culturally sensitive and on the same ecosystems and life-supporting
contribute to more comprehensive knowledge on services they provide. Harnessing their knowledge
the use of biological resources and health. on the identity and use of medicinal resources,
and their sustainability can be strengthened by
Implicit to decentralized conservation measures
improving the economic returns from their efforts
is the need to strengthen local innovation. This
by promoting value-added activities at the local
may be achieved through awards, assistance
level. Encouraging the development of enterprises
for livelihood programmes based on medicinal
based on medicinal and nutritional resources and
resources and local enterprises, appropriate
services, and of new, appropriate and feasible
intellectual property protection, and relevant
technologies that could enhance productivity and
cross-sectoral collaboration at all levels. It is
quality of resources would further complement
further relevant to develop the capacities of
conservation measures, as they serve as economic
traditional health practitioners to provide safe
and social incentives. Examples of innovative
and effective health care, and build sustainable
strategies and initiatives linking conservation and
partnerships with different collaborators (Brewer
community health are described in Boxes 9 and 10.
2014). Mechanisms for the protection of such

Box 9. Community livelihoods – linking conservation with community health

There are several successful cases that highlight how the sustainable management of medicinal
plants can impact community livelihoods, leading to income generation and improved community
health (see, for example, Hamilton 2004; Hamilton & Hamilton 2006).

One such initiative is the Muliru Farmers Conservation Group, a community-based organization
located near Kakamega forest in western Kenya. The group generates income through the commercial
cultivation and secondary processing of an indigenous medicinal plant, Ocimum kilimandscharicum to
produce the Naturub® brand of medicinal products.

The enterprise reduces pressure on the biodiverse Kakamega forest by o ering an alternative to the
exploitation of forest resources, while the commercialization of the medicinal plant has heightened
local appreciation of the value of the forest s biodiversity. Over half of the project participants are
women and 40% of participants rely entirely on this initiative for their income. The enterprise invests
a portion of its revenues in forest conservation and biodiversity.

Since the processing facility opened, over 770 tons of community cultivated O. kilimandscharicum
leaves have been processed. Over 400 000 units of Naturub® products have been sold in both
urban and rural areas of Kenya. The products have received wide acceptance in the market. The total
revenue from the project thus far has been over US 70 000. Currently, over 360 rural households
cultivate the plant on smallholder farms.

Connecting Global Priorities: Biodiversity and Human Health 197

 Box 10. Herbanisation: an open-access, medicinal street garden project for greening,
healing and connecting in Cape Town, South Africa

Cape Town, South Africa is home to a vast trade in medicinal plants, with 262 tonnes of wild
medicine being harvested from within the city annually (Petersen et al. 2014a; Reid 2014). The
illicit harvest of plant material from the city s protected areas, prompted by local demand and the
economic marginalization of many healers, has brought herbalists and conservation authorities into
con ict. The intersection of conservation priorities, livelihoods based on wild-harvested plants, and
health and well-being has resulted in a conservation conundrum (Petersen 2014b). It was in light of
this conundrum that the Sustainable Livelihoods Foundation, a nongovernmental organization based
in Cape Town, collaborated with Rasta bushdoctor (herbalist) partners to establish “Herbanisation”.

Herbanisation is an open-access, medicinal street garden project based in Cape Town. The project
aims to green degraded streetscapes in economically marginalized areas while contributing to the
livelihoods of local Rasta and Khoi herbalists, and reconnecting community members with medicinal
plants and indigenous knowledge. Herbanisation began as a pilot project of 250 medicinal plants
in 2012. Originating in Seawinds, an area of high unemployment and many social ills such as
gangsterism, drug abuse and violence, the garden was established on a pavement beside an existing
community nursery, with open access to local healers and the community. The project wanted to
connect, heal and green the community through plants. Since the inception of the pilot project in
2012, Herbanisation has expanded to include approximately 1700 plants in Seawinds, Cape Town,
and is set to reach 4500 by mid-2015.

Herbanisation has already resulted in groundbreaking engagement between Rasta herbalists,

conservation bodies and local botanical organizations. In addition, the project is strengthening
linkages between park activities and urban conservation e orts, making local nature a key driver
of urban renewal e orts. In terms of the impact on the local neighbourhood, many Seawinds
residents and local traditional healers harvest from the Herbanisation street gardens in order to treat
themselves and their families. Not only does this contribute to the health and well-being of the local
community, but it also empowers individuals to take their health into their own hands and feel proud
of their role as indigenous knowledge bearers.

Three guiding principles have been key to the success of the project to date. First, work with local
champions: our project was born out of a partnership with Neville van Schalkwyk, an accomplished
gardener and Rasta herbalist elder in Seawinds. Working with established, respected and dependable
individuals is key to project longevity and success. Second, use gardens as vehicles: while providing
herbalists and the community access to medicinal plants is a key aspect of the project, the gardens
also serve as places and processes through which conversation is enabled between herbalists,
conservation authorities and the government. This is vital in linking grass-roots community e orts
with regional policy design and implementation. Third, apply open-access principles: we have chosen
to establish gardens on disused public open spaces where plants are freely accessible to the local
people. This model encourages interaction between people and plants, while stimulating knowledge
exchange and fostering a sense of community participation and ownership.

198 Connecting Global Priorities: Biodiversity and Human Health

These cases highlight that promoting enterprises different actors in the supply chain. Furthermore,
through traditional medicinal resources and such partnerships could potentially enable the
products – where stakeholders in close proximity facilitation of financial support mechanisms to
to biological resources and knowledgeable about promote research and development, capacity
their use also gain a fair share from the value development and awareness activities related to
chain – are successful models that can address traditional medical knowledge.
both improved livelihoods and sustainable natural
resource management. Traditional approaches to health care have been
tested empirically, albeit without adequate
6.2 Capacity and research needs and documentation. Documenting such experiences
development approaches and thereby fostering a participatory learning
process to identify and supplement current
Sustainable medicinal resource management practices in a culturally sensitive way is a significant
for both captive breeding and wild collection is challenge. As seen from the examples from Palau,
important for the future of traditional medicine. Mali and India, there is also value to be gained
It should involve all stakeholders, including from reflexive methods of capacity development,
conservationists, private health-care sector, medical which foster learning between experts external
practitioners and consumers. It is important and internal to the traditional medical systems,
to increase partnerships at the local, national, at various levels of operation, including the
regional and global levels by supporting/facilitating sustainable use and protection of the resources.
enhanced networking among various stakeholders,
such as in value chain partnerships, and learning Further research is also needed to assess the
partnerships among and between peer groups. Good individual and combined impact of drivers of
examples include the development of standards change at the local, national and global scales,
and certification schemes, such as the FairWild which lead to the loss of species used for
Standard developed by TRAFFIC, International food, traditional medicines or as the basis for
Union for Conservation of Nature (IUCN), World pharmacological compounds. Unsustainable
Wildlife Fund (WWF) and other partners in a harvest, land-use change, urbanization, illegal
multistakeholder, inclusive consultation process trade and climate change are among the key drivers
as a best practice tool to verify that the wild that have already hindered access to and the
collection of plants is ecologically sustainable and potential long-term viability of these resources. It
trade is equitable. A complementary initiative is is important to examine the response of medicinal
the BioTrade Verification Framework for Native plants and other pharmacological compounds to
Natural Ingredients developed by the Union for climatic changes. Interdisciplinary research in
Ethical BioTrade. These efforts enable monitoring this area can provide valuable insights to public
of collection and trade practices, and tracing the health and conservation scientists, policy-makers
movement of resources, in addition to fostering and local communities, who depend on them for
sustainable use practices that allow benefits to their health, livelihood and well-being.

Connecting Global Priorities: Biodiversity and Human Health 199

 12. Contribution of biodiversity and
green spaces to mental and physical
ELLENM1 / FLICKR

ƩWQHVVDQGFXOWXUDOGLPHQVLRQVRIKHDOWK
1. Introduction connections between biodiversity, mental health
and physical activity are particularly relevant in
Examining the interlinkages between biodiversity, the context of a shifting global burden of disease,
mental health and health in all its dimensions as in which noncommunicable diseases (NCDs) are
defined by the World Health Organization (WHO) the most rapidly rising challenge to global public
(“a state of complete physical, mental and social health.
well-being and not merely the absence of disease
or infirmity”) demands that we explore the As discussed in the sections that follow, contact
interrelationships among biological and cultural with nature may not only be associated with
diversity, and between physical and mental health, positive mental health benefits, but can also
to foreground integrative and interdisciplinary promote physical activity and contribute to overall
approaches and research that draws from different well-being. Biodiversity can have both direct and
disciplines, and that we are able to accommodate indirect benefits for physical and mental health
diverse perspectives. Integrative approaches that (Pretty et al. 2011), just as it can sometimes pose
explicitly engage with biodiversity, physical and direct and indirect health threats, particularly
mental health, along with cultural and ecosystem when unsustainably managed or compounded by
dynamics, continue to emerge in fields such global threats such as climate change.
as ecosystem approaches to health, Ecohealth
and One Health, with a growing focus on Other indirect benefits, not traditionally
interrelationships among the health of humans, considered in the global public health agenda,
animals and other species in the context of social– include the contribution of biodiversity to the
ecological systems (see, for example, Charron provision and sustenance of a range of cultural
2012; Waltner-Toews 2004; Webb et al. 2010; ecosystem services such as spiritual values,
Wilcox et al. 2012). At the same time, scientific traditional food cultures, educational values
and clinical studies drawing from other fields and social relations.¹ If our cultural perspective
such as immunology can contribute invaluable assumes that “biodiversity” refers to “all life
insights into these multifaceted dimensions. The forms” then as humans we are inseparable, and

¹ From the Agenda 21 for Culture: cultural diversity is defined as “a means to achieve a more satisfactory intellectual,
emotional, moral and spiritual existence.” (Agenda 21 for Culture 2004). Based on this view, the starting proposition, that
there are linkages between biodiversity and human health, is more adequately framed by examining the diversity of life in
toto, rather than separate nature from culture.

200 Connecting Global Priorities: Biodiversity and Human Health

we interact with other life forms in a myriad of Between 1990 and 2010 alone, major depressive
ways that is life itself; indeed, without life forms disorders increased by 37% (Murray et al. 2012).
there would be no life on the planet, including our
own. A different cultural perspective might see the People with schizophrenia and psychosis suffer
interlinkages between biodiversity and health as from poorer physical health and die on average
important to explore because of a perceived loss of 15–20 years earlier than the general population
biodiversity, and the environmental degradation (Schizophrenia Commission 2012). This is
that has arisen as part of modern industrial aggravated by sedentary lifestyles, poor diets,
societies, rapid population growth and the smoking and weight gain from antipsychotic
urban/agricultural settings of the contemporary medications and antidepressants, in turn
anthropocene.² associated with an increased risk of obesity,
cardiovascular disease and diabetes (Schizophrenia
Accordingly, this chapter examines the Commission 2012).
interlinkages between biodiversity and mental
health, including with consideration for its Promoting physical activity in people and knowing
social and cultural dimensions and the way these more about where people with mental health
components of human health and well-being also problems should recreate could, therefore, be more
relate to cultural ecosystem services. In light of of a public health priority. Little is known about
the relationship between physical inactivity and the types of environments that can best support
NCDs, this chapter also examines the potential physical activity in this population or what types
links between biodiversity and physical fitness, of environment alleviate – or aggravate – psychotic
including in urban settings. As biodiversity is symptoms.
also central to cultures, cultural traditions and
overall well-being, building on the findings of the Green spaces in urban settings are linked to stress
chapters on traditional medicine and nutrition in reduction (Roe et al. 2013; Aspinall et al. 2013;
this volume, this often-neglected dimension of Ward Thompson et al. 2012), neighbourhood
health will be discussed in the fourth section of social cohesion (Maas et al. 2009), reductions
this chapter. in crime and violence (Branas et al. 2011; Kuo
and Sullivan 2001; Garvin et al. 2013), and a
range of other health benefits associated with
2. Biodiversity and mental health psychological, cognitive and physiological health
Mental health is defined by WHO as “a state of (see Box 1; for recent reviews, see Sandifer et al.
well-being in which every individual realizes his 2015; Logan 2015 and Rook et al. 2013). Green
or her own abilities, can cope with the normal space and tree canopy percentage have also been
stresses of life, can work productively and found to have a strong inverse correlation with
fruitfully, and is able to make a contribution to her objective measures of depression, anxiety and
or his community” (WHO 2001). In addition to an stress (Beyer et al. 2014)
increase in the incidence of NCDs such as as heart
disease, chronic obstructive pulmonary disease, There is strong evidence for the benefits of
stroke and cancer, mental disorders contribute to a interaction with nature – including domestic
significant proportion of the global disease burden animals, and wild animals in wild settings – in
(Beaglehole and Bonita 2008; Beaglehole et al. treatments for depression, anxiety and behavioural
2011). Depression alone accounts for 4.3% of the problems, particularly in children and teenagers
global burden of disease and is among the largest (e.g. Kuo and Taylor 2004; Markevych et al. 2014;
single causes of disability worldwide, particularly Wells 2014; Roe and Aspinall 2011a). It has been
for women (WHO 2013). argued that contact with nature is important for

² Pretty et al. (2008) embraced these different perspectives in the following way: “There is a common recognition around the
world that the diversity of life involves both the living forms (biological diversity) and the world views and cosmologies of
what life means (cultural diversity).”

Connecting Global Priorities: Biodiversity and Human Health 201

 childhood development, and children who grow up Recent studies have shown that it is not only the
with knowledge about the natural world and the availability and quantity of greenery that matters,
importance of conservation may be more likely but also the quality and depth of the green spaces,
to conserve nature themselves as adults (Kahn Jr in terms of species richness and heterogeneity
& Kellert 2002; Taylor et al. 2006). Conversely, a (e.g. Werner and Zahner 2010; Sandifer et al.
growing number of studies have suggested that 2015). Measurable positive associations between
children, particularly in developed countries, species richness, including microbial diversity,
increasingly suffer from a “nature-deficit and aspects of psychological well-being have
disorder”,³ due to a reduction in the time spent been demonstrated, suggesting that habitat
playing outdoors, potentially a result of increased heterogeneity could be a cue to the perceptions of,
use of technology, and parental and societal fears and positive outcomes from, biodiversity (Shwartz
for child safety (Mustapa et al. 2015; Derr and et al. 2014). Hence, the design and management
Lance 2012; McCurdy et al. 2010; Godbey 2009).⁴ of green spaces in urban environments should
take biological complexity into consideration
Nature connectedness refers to the degree to which for the enhancement of human well-being, on
individuals include nature as part of their identity top of the usual considerations of biodiversity
through a sense of oneness between themselves conservation that focuses on restoring the biotic
and the natural world (Dutcher et al. 2007; Schultz integrity of ecosystems themselves. Aspects of
2002). Beyond an evolutionary affiliation to other biological complexity include species composition,
life on earth, the hypothesis here is that a sense functional organization, relative abundance and
of connection between one’s self and biodiversity species numbers. These notions have been used
is also critical for mental, social, physical and for hospital design (see Box 2).
cultural health. Re-developing this connection
has been described as a series of steps involving As discussed in the chapters on microbial diversity
the acquisition of knowledge (information about and nutrition in this volume, there is a growing
nature), developing an understanding based body of scientific evidence that demonstrates the
on physical experiences in nature, and moving importance of (non-pathogenic) microbial inputs
towards being connected and committed (Zylstra from the environment and dietary patterns in
2014). determining public health outcomes. An increasing
proportion of this emerging research specifically
People with high nature connectedness tend to examines the relationship between the human
have frequent, long-term contact with nature microbiota, exposure to microbial biodiversity
and spend the most time outdoors (Chawla 1999), through the natural and built environments,
exhibit ecologically aware attitudes and behaviours and diets, with corresponding implications for
(Nisbet et al. 2009; Parks Canada, 2011; Wellman NCDs, including depression and anxiety (e.g. for a
et al. 1982; Williams & Huffman, 1986), and recent review, see Logan 2015 and Rook 2013 and
are happier (Zelenski & Nisbet, 2014). These references therein). Importantly, these studies also
characteristics translate to being more supportive consider how socioeconomic and environmental
of conservation and predict greater likelihood to factors may modulate and mediate health
express environmental concern (Dutcher et al. outcomes (see also section 3 in this chapter). These
2007; Mayer and Frantz 2004). findings are also useful to inform the design of
urban landscapes that jointly promote the mental
³ A term coined by journalist Richard Louv in 2005
⁴ Some research has suggested that some children, particularly those from urban areas, are fearful of spending time in certain
natural habitats (woodland and wetland) owing to perceived threats from isolation, wild animals or the actions of other
people (Bixler & Floyd 1997). The biophilia hypothesis asserts that humans have an evolutionary affiliation to nature (Wilson
1984). Although those with strong traditional or local ecological knowledge bonds are more likely to have maintained strong
connections to the natural world, today more than half of the world’s population lives in cities, often reducing contact with
biodiversity to infrequent time spent in green spaces and visits to parks. Consequently, Western cultures are increasingly
concerned about the growing disconnect between humans and nature (Dallimer et al. 2012; Louv 2008).

202 Connecting Global Priorities: Biodiversity and Human Health

health benefits of exposure to green spaces and co-benefits associated with cognition, emotion
biodiversity (including microbial diversity). and sensation. In doing so it will become a part
“Green spaces” and “natural environment” will of a more comprehensive approach to addressing
need explicit measures in research at this critical the growing global burden of NCDs, including
intersection, to enable the development of inflammatory, immunoregulatory and other
urban planning strategies in ways that maximize conditions.

Box 1. Enabling environments for mental health rehabilitation

Research by enny Roe and Peter A. Aspinall has indicated that some environments may be more
favourable to mood and cognitive recovery in people with severe mental health problems than
others. They compared the restorative bene ts of walking in urban and rural settings in a group
of adults with a range of mental health problems, including people with schizophrenia and other
psychotic disorders (N=24). Two aspects of psychological restoration were examined, rstly mood,
and the other using personal project techniques (Little 1983) to capture cognitive re ection on
everyday life tasks. Participants walked in small groups of around 8 in a variety of urban and rural
settings in central Scotland. As anticipated – and consistent with restorative theory – a walk in a
natural setting was advantageous to mood recovery and cognitive re ection on the management of
personal projects. However, contrary to other evidence showing negative e ects of walking in urban
settings on people with psychotic disorders (Ellett et al. 2008), in this instance, a walk in a busy
historic urban district generated a positive change in mental well-being.

Supporting qualitative research (via semi-structured interviews) (N=24) indicated stronger

preferences for walking in the natural setting further a eld, as compared to walking in the
hometown; being away from their everyday environments allowed mental health patients to escape
stigmatization and facilitated anonymity. Symptom relief from psychosis and schizophrenia included
a reduction in auditory hallucinations (i.e. hearing noises) in the natural setting.

The research concludes that walking in some urban environments (for example, historic districts and
city green spaces) – as well as further a eld natural settings – o ers the potential to promote physical
activity and mental well-being in people with severe mental health problems (Roe and Aspinall 2011b).
These ndings have in general informed UK health policy and in particular initiatives such as the
Scottish Government s “green prescriptions” and the Green Exercise Partnership between the National
Health Service (NHS) Health Scotland, Forestry Commission Scotland and Scottish Natural Heritage,
which are designed to promote greater use of the outdoors for better health and quality of life.

Box 2. Designing for a healing environment: Khoo Teck Puat Hospital, Singapore

Khoo Teck Puat Hospital, a 590-bed acute care hospital in Singapore, aptly presents a case where
urban greenery, including biological complexity in terms of species richness and habitat heterogeneity,
has been incorporated into the hospital design to reap the associative bene ts of healing and well-
being. The hospital s concept of “a healing environment” emphasizes the nexus between greenery and
well-being in three aspects: rst, direct bene ts of greenery towards the healing of patients; second,
capitalizing on the nexus to improve the livability of the urban environment for both the individual
resident and the community; and third, promoting biological complexity in terms of a biodiverse and
heterogeneous environment that also contributes to human well-being.

Connecting Global Priorities: Biodiversity and Human Health 203

 The wards and corridors of the hospital are
designed to support patients in the healing
process. At ground, the nexus between
biodiversity and well-being is explored
through the richly planted parklands and
the ishun Pond, whose lush environs are
attractive not only to patients and visitors,
but also to residents in the surrounding
neighbourhoods. The promenade along
the edges of the pond and the hospital
gardens connects to the adjacent housing
estate and train station beyond the hospital
grounds, providing seamless access to the
surrounding communities. The gardens
have attractive water features, including a
designed cascading waterfall, adding sound
and movement to the environment.

To extend the concept of integration with

the community, a rooftop farm grows
food crops that are tended by community
volunteers and former patients. The crops
provide a relatively cheap source of organic
food of approximately 208 kg per year for the hospital kitchen, while the harvesting and sale of
produce to the public contributes to the hospital green fund. There are over 50 species of fruit trees,
and 50 vegetables and herbs in this rooftop farm. The volunteers get to socialize, and bringing their
harvest home is both a source of pride and joy, and a therapeutic activity, particularly for the older
volunteers who are mostly retirees.

The planting in and around the hospital emphasizes biodiversity and habitat heterogeneity,
particularly in terms of birds and butter ies, and fruit trees. In the pond, 100 species of South-
East Asian tropical sh have been recorded, some of which were thought to have become extinct.
There are reported sightings of 48 species of birds, 44 species of butter ies and 21 species of
dragon ies and damsel ies. The “medicinal garden” has over 100 species of medicinal plants used
in traditional medicine. The pond with its owering plants at the edges, and its oating mounds,
attracts butter ies, dragon ies as well as bird species, which in turn feed on the sh, creating a
microecosystem of its own.

The hospital epitomizes the idea of a healing environment in its numerous design dimensions
and innovations. It exempli es an urban asset that goes beyond incorporating landscapes for their
aesthetic qualities, and also purposefully and meaningfully seeks to bring biodiversity into urban
spaces, all of which contribute to a pervasive sense of well-being that extends to the surrounding
community.

Alexandra Health are acknowledged for their input and support. For further information on the
gardens and landscaping, see Alexandra Health (2010).

204 Connecting Global Priorities: Biodiversity and Human Health

3. Biodiversity, green space, 3.1 Biodiversity, recreation and
exercise and health OHLVXUHDQGSK\VLFDOƩWQHVV
The relationships between biodiversity and “Time spent directly experiencing and interacting with
nature (a problematic term to define) has been shown
good physical health are inherently complex and
to improve psychological health and well-being, as well
multidimensional, with multiple confounding
as increase physical activity levels…” (Pretty et al. 2008).
and interrelated sociocultural, geographical and
economic mediators. The studies that exist often As human societies industrialize and urban centres
fail to provide clear empirical evidence of the continue to expand, the physical relationship
effects of biodiversity on physical health and well- with biodiversity sometimes shifts from a direct
being. While the majority of studies presented consumptive interaction to one of more abstracted
herein are examples of where a potential positive recreational and leisure activity (Keniger et al.
association between biodiversity and physical 2013). Regardless of our socioeconomic status,
health could be inferred, a large number of setting or motivations of subsistence or leisure,
studies also report inconclusive results (Lovell et our exposure to and interactions with biodiversity
al. 2014) and some report inverse relationships range from passive engagement from afar (e.g.
(Huynen et. al 2004; Dallimer et al. 2012). viewing through a window) to being within
Further multidisciplinary study is needed to more a natural space (e.g. sitting in a park), to the
clearly establish causal links to inform policy. direct active engagement of fishing, hunting or
Current analyses are methodologically diverse gardening. Much of our current body of evidence
and frequently focus only on urban and western documenting the health effects of exposure to
settings that are insufficiently interdisciplinary natural biodiverse environments is gleaned from
to test postulated relationships. Research needs urban, Western, developed world settings (Lovell
to have adequate involvement of the expertise et al. 2014; for a recent review, see Townsend
and standard methodological practices of et al. 2015). While biodiversity has rarely been
the social sciences (including psychology and measured directly in these studies, they do provide
sociology), health sciences (including physiology emerging evidence that interacting with natural
and epidemiology) and environmental sciences surroundings in urban settings can deliver a
(particularly ecology), rather than be dominated by range of measurable benefits (Bauman 2004;
selected disciplines, as is so often the case. In the Brown et al. 2007; Blair & Morris 2009), including
few studies in which a direct causal relationship positive effects on physical health (Berger & Motl
between biodiversity and physical and mental 2000; Street et al. 2007; Rethorst et al. 2009),
health has been sought, it is frequently the case psychological well-being (Barton & Pretty 2010;
that precise physiological elements of physical Kaplan & Kaplan 1989; Kaplan 1995), cognitive
health have not been correspondingly measured. ability (Ulrich 1983) and social cohesion (Maas et
With notable recent exceptions, including those al. 2006). Conversely, there is empirical evidence
noted above, few studies rigorously measure both at a global scale that more biodiverse settings
biodiversity and specific physiological effects on correlate with poorer health outcomes (Huynen
physical health. In addition, the evidence we have et. al 2004) and on a local scale, some self-reported
is from mostly affluent urban Western societies, measures of well-being are inversely related with
and further exploration across a range of cultures, natural biological diversity (Dallimer et al. 2012).
geographical regions and socioeconomic groups While interacting with nature can deliver health
is needed, including rural and developing world benefits, the converse is also true and the specific
settings. role of biodiversity in effecting these health
outcomes is still not well understood.

It is clear that exercise and physical activity have

positive impacts on health. Physical activity has
been shown to lead to improved physical fitness

Connecting Global Priorities: Biodiversity and Human Health 205

 and health (Bauman 2004; Brown et al. 2007; climate change and sustainable consumption in
Blair & Morris 2009), including a reduced risk this volume indicate, evaluating and monitoring
of several NCDs, as well as improved immune cumulative health impacts that may result from
function. Engaging in regular physical activity policy prescriptions (including as they relate to
has also been linked to improved mental health, urban planning) will therefore be critical. This
including lowering depression, through a includes the need for infrastructure and policy
combination of physiological effects as well as measures, in both developed and developing
through increased social engagement (Berger countries, that support active transit, reduce our
& Motl 2000; Street et al. 2007; Rethorst et al. reliance on fossil fuels, and concretize the goal
2009). Significant proportions of the global of an “urban advantage”, which itself “must be
population are experiencing epidemics of NCD, actively created and maintained” through robust
including heart and other circulatory diseases, and coherent policy interventions (Rydin et al.
diabetes type 2, and mental health disorders 2012).
(Beaglehole et al. 2011; Collins et al. 2011).
Particularly in urban settings, the management Access to parks and green spaces within urban
and prevention of some NCDs may be linked to residential neighbourhoods has been shown to be
the use, for recreational and fitness purposes, an important conduit to generating better physical
of natural environments or “green spaces”, as and mental health for individuals and communities
outlined below. The policy implications for such a (Kessel et al. 2009; Maas et al. 2006; O’Campo et
linkage are clear: as the global population becomes al. 2009). Urban parks and green spaces provide
increasingly urbanized, cross-sectoral consultation places for sport and active recreation, places to
between different sectors, including the health, relax and enjoy solitude, places to meet other
conservation, transport and other sectors, will be people and socialize, and places that evoke feelings
key to the development of healthy and sustainable of connection to the natural world (Maller et al.
urban landscapes (Box 3). As the chapters on 2008). A reduction in the prevalence of several

Box 3. Urban design for active transport and a healthy human habitat

The urban landscape has become the prototypical human habitat. Commuting by foot or bicycle,
so-called “active transport”, o ers the dual bene ts of reducing air pollution emissions – a key
driver of anthropogenic climate change – and promoting opportunities for personal tness.
Physical inactivity is a risk factor for NCDs and is estimated to be responsible for 3.2 million deaths
annually (Lim et al. 2013). Many studies show signi cant global health bene ts from shifting to
environmentally sustainable practices. For example, active commuting in Shanghai, China, reduced
risk of colon cancer by 48% in men and 44% in women (Hou et al. 2004), and active transport
led to an 11% reduction in cardiovascular risk across sample populations from Europe and Asia
(Hamer and Chida 2007). If active transport scenarios reached the levels of those in Copenhagen,
costs averted for England and Wales NHS would approximate US 25 billion over a 20-year period
( arret et al. 2012). In the United States (US), comparing cities with the highest versus lowest levels
of active transport, obesity and diabetes rates were 20% and 23% lower, respectively (Pucher et al.
2010), and over 1200 lives could be saved annually in the upper Midwest, US, by replacing short car
trips with bike transport (Grabow et al. 2012). More public health bene ts in developed countries
accrue from greater levels of exercise (Grabow et al. 2012; Pucher et al. 2010; Woodcock et al. 2009;
Maizlish et al. 2013; Hankey et al. 2012), whereas in low-income countries with air quality problems,
the bene ts are more from reduced air pollution (Woodcock et al. 2009). Pathways and bikeways in
parks and other green spaces will facilitate the adoption of active transport as a viable alternative.

206 Connecting Global Priorities: Biodiversity and Human Health

NCDs and their risk factors can be linked to the (2012) noted no association. Tilt et al. (2007)
quantity, proximity and usability of “natural” also found positive associations between walking
spaces in the local (residential) environment and subjective assessments of overall “greenness.”
(Carter & Horwitz 2014; Bowler et al. 2010; Other relevant findings include proximity to large
Lachowycz & Jones 2011; Lee and Maheswaran neighbourhood parks being positively associated
2010; Mitchell and Popham 2007, 2008). Results with increased physical activity (Giles-Corti
suggest that perception of park quality is one et al., 2005), neighbourhood greenness being
important factor in encouraging their use for positively associated with increased walking, social
physical activity (Crawford et al., 2008), lowering coherence and local social interaction (Sugiyama et
psychosocial distress (Francis et al. 2012), and al. 2008), and with reduced body weight (Pereira
supporting better self-reported general health and et al. 2013), improvements in park infrastructure
physical function (Carter & Horwitz, 2014). Bjork resulting in increased use (Veitch et al. 2012
et al. (2008) showed that participants with “lush” and Veitch et al. 2014), and how the design of
environmental features within 300 m of the home open spaces may influence the type of use and
engaged in greater self-reported physical activity length of stay (Goliˇcnika & Ward Thompson
than those with other environmental feature 2010). A concerted effort is being made by some
types. Similarly, de Jong et al. (2012) detected a governments to maximize these health benefits
positive association between “lush” environments through park management (see Box 4).
and physical activity, although Annestedt et al.

Box 4. Active in Parks Program, Victoria, Australia

The Active in Parks Program forms partnerships between park managers and health and community
service agencies to connect people to parks and open spaces to improve physical and mental
well-being. The outreach is through tailored activities that increase people s physical activity and
overcome barriers, such as transport, lack of awareness and fear, to support their access to parks and
other natural open spaces.

The Program commenced in 2010 as a pilot in Geelong, a major regional city in Victoria, Australia.
It addresses a number of key health issues, including social isolation, mental health, physical
inactivity and priority chronic diseases. Geelong is an area with a prevalence of preventable diseases,
particularly in low socioeconomic communities, and is surrounded by outstanding parks and open
spaces that are now part of the solution to getting more people more physically and socially active
more often, and improving individual and community health and well-being. This is the “Healthy
Parks Healthy People” approach to park
management.

The Program includes ve elements:

Green referrals: physically inactive people at

risk of developing or already su ering from
chronic illness are referred by their health
professional to a physical activity programme
based in local parks. They are supported by
quali ed instructors and encouraged to do
ongoing exercise.

Connecting Global Priorities: Biodiversity and Human Health 207

 Welcome to new migrants: park outings involving physical activity, such as sur ng, shing and
beach walking, help newly settled Victorians from diverse cultural and linguistic backgrounds to
independently engage in physical activity outdoors and reduce their risk of being socially isolated.

Youth park ambassadors: secondary school students at risk of developing a mental illness and/or
disengaging in school take part in outdoor adventure activities to build con dence, resilience and
connection with nature, then encourage others to get “Active in Parks”.

Adolescent education: young people with type 1 diabetes learn how to manage their chronic illness
and treatment while being physically active in nature and making social connections with others.

Parks walks: regular, volunteer walking groups enjoy parks and open spaces, while strengthening
community connectedness and encouraging regular outdoor enjoyment of nature.

Participants have credited the Program with restoring their con dence, improving their motor skills
and, most importantly, giving them a more positive attitude towards physical activity. Post-Program
surveys have unanimously rated the contribution of the Active in Parks Program as bene cial to
health and well-being.

Almost 100% of Program participants from uly 2013 to December 2013 reported gaining
friendships from the Program, with 30% of participants now meeting independently on a regular
basis. In 2014, over 66% of respondents reported that the Program increased the time they spent in
a park, and over 86% reported that the Program changed their attitude/behaviour towards physical
activity. Over 93% of respondents planned on continuing to exercise on their own.

Whereas some studies show that the use of and to be due to the perceptions of favourable
exposure to the natural environment is associated environmental conditions for people to exercise,
with better health (Keniger et al. 2013; Lee et al. thus improving motivation to continue physical
2011; Thompson-Coon et al. 2011), others more activity. Despite the evidence that urban “green”
explicitly link “condition” of the environment space can increase physical activity and contribute
to particular health outcomes (Cummins et al. to other dimensions of health, little explicit
2005; Mitchell and Popham 2008; van Dillen consideration has been given to the importance
et al. 2012). Environmental decline, including of the biodiversity itself (versus simply green or
loss of biodiversity, has also been shown to natural space) in delivering improved physical
have greater adverse health effects, particularly function or health.
on mental health, than the impacts associated
with economic decline, nutritional threats and We have scant evidence from studies in which
pollution (Speldewinde et al. 2009). standard ecological survey methodology has been
undertaken alongside an assessment of physical
This evidence suggests that among populations health. These few studies measure physical
for whom access to natural green spaces is health as subjective well-being rather than
limited, such as those in poorer inner-urban measuring specific physiological attributes that
areas of large cities, improving that access can reflect physical fitness or well-being. An urban
encourage regular physical activity, improve life Australian study found that personal well-being
expectancy and decrease health complaints. The and neighbourhood satisfaction were positively
psychological benefits and social outcomes may related to greater species richness and abundance
also increase motivation to further exercise and of birds, and with increased vegetative cover and
use the green space. Much of this is thought density (Luck et al. 2011). In urban UK, Dallimer et

208 Connecting Global Priorities: Biodiversity and Human Health

al. (2012) and Fuller et al. (2007) also showed that the activity associated with the gardening and
bird species richness was positively associated with the natural components of the environment (e.g.
measures of well-being, while butterfly species biodiversity) in promoting stress reduction. Some
richness was not shown to have any association. studies have concluded that the physiological
Fuller et al. (2007) found that enhanced well-being effects of stress are reduced in forest environments
was positively related to increased plant species and other natural environments.⁵ For example, a
richness, whereas Dallimer et al. (2012) showed Swiss study also found that a decrease in stress-
a decline in well-being under such conditions. induced headaches was significantly related to
Variation was also seen in relation to tree cover, physical activity in parks (Hansmann et al. 2007).
with Dallimer et al. (2012) reporting a positive
relationship with well-being and Fuller et al. (2007) Other physiological benefits that have been
finding no association. Local-scale urban studies studied are the relationships between natural
on the links between biodiversity in green leisure spaces and healing. In a study of cholecystectomy
spaces and self-reported well-being do suggest that patients in the US, postoperative healing time was
exposure to biodiversity may have demonstrable significantly reduced for patients in a hospital room
positive impacts on health (Dallimer et al. 2012; with a window view of nature in comparison with
de Jong et al. 2012; Fuller et al. 2007; Tilt et patients with a view of a brick wall (Ulrich 1984).
al. 2007), although without understanding the Patients with a view of trees also required fewer
specific effected aspects of physiological health. painkillers, received fewer negative evaluative
These variations may in part be explained by comments from nurses and had fewer postsurgical
differing cultural contexts, and even by differences complications. Another study demonstrates that
in how various groups within a community value outdoor therapeutic camping trips reduce the
their local landscapes, biodiversity or green spaces. probability of relapse among recovering substance
Such perspectives may in part be informed by abusers (Shin et al. 2001).
socioeconomic factors, or by the degree to which
different groups feel they can influence local Physiological responses to nature have also
decision-making affecting their environment (see, been shown to vary according to gender. A UK
for example, Cutts et al. 2009; Ernstson 2013). study shows that cardiovascular and respiratory
disease mortality rates among men decreased
Some studies do measure sets of physiological with increasing green space, with no significant
indicators of physical health in relation to natural relationship for women (Richardson and Mitchell
green space but do not measure biodiversity within 2010). Ulrich (1981) found that the positive
these natural settings. There is a growing body of physiological responses of exposure to nature,
evidence to suggest that interactions with nature as measured by heart rate and alpha amplitude
can alleviate some of the negative physiological while viewing images of nature, were significantly
effects of stress within urban environments. A stronger for women.
study from the Netherlands showed that outdoor
gardening led to significantly greater reduction in Studies on the effects of indoor plants in office
the stress hormone cortisol than indoor reading and classroom environments have also shown that
(Van den Berg & Custers 2011). This study cannot, their presence can improve physical health (Fjeld
however, determine the relative importance of et al.1998) and reduce the occurrence of illness
(Han 2009; Bringslimark et al. 2007).⁶ As with

⁵ A Chinese experimental study (Yamaguchi et al. 2006) measured stress in healthy males before and after exercise in both a
forest and an urban environment using salivary amylase activity as a physiological indicator. Enzyme activity significantly
reduced after exercise in forest environments.
⁶ A Norwegian study showed that the presence of plants in offices correlated with a reduction in dry skin, hoarse throat,
coughing and fatigue, suggesting that the introduction of foliage plants into an indoor environment may reduce symptoms
of physical discomfort and improve health (Fjeld et al. 1998). Related studies on the effects of indoor vegetation have found
that the diversity and presence of indoor plants in an office (Bringslimark et al. 2007) and a classroom (Han 2009) reduce
the occurrence and frequency of time taken off due to ill health.

Connecting Global Priorities: Biodiversity and Human Health 209

 many of the studies examining this relationship, A number of studies have investigated whether
and noted often already, nature is often not clearly the presence of larger amounts of green space
defined, biodiversity is not explicitly measured has a disproportionate impact on the health
and there is a lack of studies in rural, developing and well-being of those with the lowest levels of
countries in equatorial latitudes. socioeconomic status (e.g. Dadvand et al. 2012;
Logan 2015). In the Netherlands, Maas et al.
3.1.1 ,he Eoderating and Eediating (2006) found the strongest associations between
inÎuen;e of so;ioe;onoEi; status and proximity to natural environments and health
;ulture for people with the lowest socioeconomic status;
similarly, de Vries et al. (2003) found stronger
Socioeconomic status (and sociocultural context relationships for housewives, the elderly and “lower
to a lesser degree) is well established as a educated” people. Research using UK data found
determinant of health, with strong associations lower rates of income deprivation-related health
found between contributory factors such as inequalities in all-cause mortality and circulatory
income and employment or livelihood security, disease⁸ among those living in the greenest
and health and well-being. Similarly, and as noted places (Mitchell & Popham 2008). Importantly,
previously, exposure to and use of environments no association was found when considering
containing biodiverse elements have been shown outcomes unlikely to have an association with
to relate to health and well-being. However, it greater exposure to natural spaces (deaths from
is only recently that the interactions between lung cancer and intentional self-harm). Nearby
these two determinants of health – natural natural environments have also been found to
environments and socioeconomic status – have help women in low-income groups to better cope
begun to be investigated and, therefore, integrated with stress (Jennings et al. 2012). These studies
into and considered within socioecological or suggest that people with lower incomes and facing
ecosystem service models. other forms of social and economic disadvantage
do have better health when exposed to larger
Epidemiological work (predominantly undertaken quantities of natural environments. It has been
in residential urban areas) shows us that there is suggested that the presence of attractive, high-
often a linear relationship between proximity to, quality natural environments (in conjunction
or quantity of (biodiverse) natural environments⁷ with various other factors) moderates the health
within the residential living environment and effects of long-term deprivation (Cairns-Nagi &
health or well-being outcomes (Carter and Horwitz Bambra 2013). Further evidence has underlined
2014). However, these relationships are potentially the potential importance of the “quality” of
confounded by the likelihood that exposure and the environment; using the results of the UK
access to a large quantity of better-quality natural Census, larger quantities of green space in the
environments is strongly influenced by the greater living environment were associated with poorer
choices and resources of populations with higher health for those living in suburban low-income
socioeconomic status (i.e. those with higher areas (Mitchell & Popham 2007). Importantly, it
incomes and social and individual capital – who has been found that (e.g. Coen et al. 2006) green
therefore enjoy better health and well-being – spaces are likely to be of poorer quality in lower-
can afford to move to neighbourhoods with larger income areas.
proportions of green spaces and biodiversity).

⁷ The vast majority of this work has not sought to define the characteristics of the natural environment beyond contrasting
these “green spaces” with built urban spaces. Also, it is clear that concepts of green space, and discussions of “access to
countryside” are not relevant to large numbers of people, including many local and indigenous communities and diffuse
rural populations in much of the world.
⁸ Outcomes theorized to be influenced by exposure to or use of green spaces, through for instance mechanisms such as
physical activity or lowered psychological stress.

210 Connecting Global Priorities: Biodiversity and Human Health

UNITED NATIONS PHOTO / FLICKR

Recognition of these disproportionate impacts socioeconomic status (or other factors such as
of high-quality natural environments and high immigrant populations) and proximity to
biodiversity to the health of those with the environments with lower levels of biodiversity
lowest levels of socioeconomic status has led (Cohen et al. 2006, 2012; Hope et al. 2003;
statutory bodies, such as Natural England and the Kabisch & Haase 2014; Kinzig et al. 2005; Martin
Forestry Commission in the UK, to adopt policies et al. 2004; Strohbach et al. 2009). Strohbach
(for instance, Accessible Natural Green Space et al. (2009), for instance, found that wealthier
Standard⁹) encouraging or facilitating greater neighbourhoods, which were typically situated
equity of access. close to forests, parks, rivers and high-quality
green spaces, had a greater richness of species
Such policy interventions are welcome. In many than poorer neighbourhoods. The differences can
places, there is an inequitable spatial distribution be stark. For example, Kinzig et al. (2005) found
of biodiverse natural spaces (particularly in the an average of 28 avian species in parks in high-
urban context) according to socioeconomic status income areas compared with only 18 avian species
and other cultural and demographic factors (Astell- in parks in low-income areas.¹⁰
Burt et al. 2014; Ernstson 2013). If you live in a
low-income urban neighbourhood you are likely However, even where policies to facilitate exposure
to have fewer and lower-quality green spaces and, to biodiverse environments are acted upon and
therefore, fewer opportunities to experience and efforts are made to improve accessibility, it still
benefit from biodiversity than people in higher- may be the case that some groups, particularly
income neighbourhoods. Multiple descriptive those with lower socioeconomic status, face
studies have also shown strong correlations inequitable access (Jones et al. 2009).¹¹ Similar
between neighbourhoods characterized by lower disproportionate reliance on local environments

⁹ ‘Nature Nearby’ Accessible Natural Greenspace Guidance. www.naturalengland.org.uk

¹⁰ This inequality could, in some cases, have profound implications. Quality of life is strongly influenced by one’s environment,
particularly for the poor and marginalized who most need access to high-quality, local biodiverse environments, as they are
likely to be unable to travel frequently for any great distance to experience these places (Kinzig et al. 2005).

Connecting Global Priorities: Biodiversity and Human Health 211

 and biodiversity is also found for people with by environmental degradation but we have not
lower socioeconomic status in low- and middle- yet reached that point, and therefore the impacts
income countries. While the mechanisms can of the environment on well-being are not yet
be fundamentally different, perhaps relating detectable.
more strongly to other determinants of health
such as adequate nutrition and clean water, the
4. The contribution of biodiversity
ability to access, and to make use of, biodiversity-
related resources can have a greater impact on the to cultural ecosystem services that
health and well-being of the poorest members of support health and well-being
a particular society (Daw et al. 2011; Millennium An accepted characterization for cultural services
Ecosystem Assessment 2005; see also Dallimer is provided by the Millennium Ecosystem
et al. 2012 ). Likewise, the loss of biodiversity is Assessment (MEA) (2005), described as the non-
likely to disproportionately impact on the health material benefits people obtain from ecosystems
and well-being of the poorest (Díaz et al. 2006; through spiritual enrichment, cognitive
Raudsepp-Hearne et al. 2010). development, reflection, recreation and aesthetic
experiences, and including ten different forms of
Raudsepp-Hearne et al. (2010) explored four
values. Given the often discussed overlaps between
potential hypotheses (in relation to global
services, benefits and values, and the consideration
biodiversity loss) to explain why we are not able
of both use and non-use (or non-consumptive)
to consistently show how biodiversity relates to
values of cultural ecosystem services, this chapter
well-being: (i) we may be looking at the “wrong”
follows the convention established by Milcu et al.
aspects of well-being, and the ones we have
(2013) and others (e.g. Gee and Burkhard 2010) to
considered may not be sensitive to environmental
include existence, bequest and option values, and
influences, and that practices such as aggregation
the intrinsic value of ecosystems as a subcategory
could mask shifts in well-being (see also Lovell et
of cultural ecosystem services.
al. 2014 and Daw et al. 2011); (ii) our well-being
is only actually sensitive to certain environmental In a comprehensive review, Pretty et al. (2008)
influences, particularly those associated with explored how biological and cultural diversity
the provisioning services and especially food; intersect, describing “nature” as “the setting in
(iii) there has been a “decoupling” of human which cultural processes, activities and belief
well-being’s dependency on the environment systems develop, all of which feed back to shape
through technological and social innovation; the local environment and its diversity”.¹² There
other factors such as access to mental health are of course other models that depict pathways
care, the socioeconomic context or just familial between biodiversity, culture, and physical and
circumstances might exert a greater influence mental health, but the point made here is that they
than the natural environment. If the environment are extraordinarily diverse, where it is difficult to
has a relatively small impact then detecting that generalize or to derive universal statements.
influence is difficult and the measures used need
to be sensitive; and (iv) well-being will be affected

¹¹ For example, Byrne et al. (2009) cite the case of Los Angeles’ Santa Monica Mountains National Recreation Area, the result
of policies in the 1970s which aimed to “to bring nature and recreational opportunities to socio-economically disadvantaged
communities in the USA”, but where visitors were found to be predominantly white and affluent. Huynen et al. (2004)
describe the association between low socioeconomic status, race and ethnicity and poor access to biodiverse environments
as “yet another instance of urban environmental inequality”.
¹² They described four key bridges interlinking nature with culture: (i) beliefs, meanings and worldviews that underpin the way
humans see their place in nature; (ii) livelihoods, practices and resource management systems, where nature is managed;
(iii) knowledge bases and languages, where how people know the world governs behaviours, understanding and values that
shape human interactions with nature; and (iv) socially embedded norms and institutions, where normative rule systems
govern human interactions and behaviours towards the natural environment.

212 Connecting Global Priorities: Biodiversity and Human Health

While many community-specific linkages between whatever levels of richness; they are inseparable.
health, culture and biodiversity have been Formal recognition of cultural diversity has
documented and measured, much of the evidence demonstrable health benefits for cultures (often
for a more universal relationship is sparse beyond minorities) that have suffered from domination
anecdotal accounts. However, there is growing and oppression; replacement with other biological
recognition of the role of biodiversity and elements might have poorer health outcomes for
ecosystem services in shaping broad perspectives the same reasons.
of the quality of life. The WHO Quality Of Life
Assessment (WHOQOL) was devised as a method Spiritual and religious values. Sacred elements of
to determine an individual’s quality of life in the the biota, worship of biota, kindness and gratitude
context of their culture and value systems; use toward biota together or individually make a
of the WHOQOL method has shown that the contribution to spiritual well-being, and a sense
environmental domain – including aspects of of wholeness and being “at one”, everywhere and
safety, security, access to resources and interaction forever (connecting the present with the past and
with local environments – is an important part the future).
of the quality-of-life concept (WHOQOL Group
1994; see also Skevington 2009). Knowledge systems (traditional and formal). This
includes knowledge of pharmaceuticals, food
Clark et al. (2014) conceptualized the direct products and knowledge contributing to rituals,
linkages between biodiversity and human health and socializing processes. These together provide
via disease regulation and pollution control, people with understanding on when and where
and the indirect linkages between biodiversity to use biological materials for alleviating poor
and human health as being “cultural”, where health or disease, including when and where to use
biodiversity yields cultural goods, cultural values them for better diet and nutrition, and spiritual
are placed on those goods, and when they are well-being.
derived there is a well-being benefit and therefore
a human health outcome. Educational values. Ecosystems and their
components and processes provide the basis
Culturally competent health practice must for both formal and informal education in
account for the influence of culture on attitudes, many societies. These learned capacities provide
beliefs and behaviours, including the relationship the ability to avoid environmental hazards
between people and their local biodiversity and and physical injury or death, and to alleviate
ecosystem services. The relationship between psychosocial stress-related disorders.
culture and population health is complex. The
delivery of primary health care at the community Inspiration. Ecosystems in general, and elements
level is generally organized around predominant of biodiversity in particular, provide a rich source
local cultural norms, but must also increasingly of inspiration for art, folklore, national symbols,
account for cultural diversity and the cultural architecture and advertising. These contribute to
characteristics of minority groups. well-being in a myriad of ways.

For each of the well-known categories of cultural Aesthetic values. People find beauty or aesthetic
ecosystem services, it can be demonstrated that value in various aspects of ecosystems, as reflected
biodiversity plays a role in the way physical and in the support for parks, scenic drives and the
mental health and well-being have been or can be selection of housing locations. These values have
derived. been linked to stress relief, with therapeutic
benefits.
Cultural diversity. Reciprocal relationships have
been described between cultural diversity and Social relations. Ecosystems influence the types of
biological diversity in the diversity of life, at social relations that are established in particular
cultures. Sharing ecosystem experiences, like

Connecting Global Priorities: Biodiversity and Human Health 213

 volunteering for land and water rehabilitation or threats they face (see the major review on this
species conservation activities, has been shown to topic by Maffi 2005): “… the ongoing worldwide
have positive psychosocial outcomes. loss of biodiversity is paralleled by and seems
interrelated to the ‘extinction crisis’ affecting
Sense of place. Many people value the “sense of linguistic and cultural diversity”.¹³ Maffi reviews
place” that is associated with recognized features the studies that have shown overlaps (also referred
of their environment, including elements of the to as correlations) between linguistic diversity at
biota (rare, common, iconic, endemic) and aspects the global level, and both vertebrate diversity
of the ecosystem. Psychosocial disorders have and plant diversity. Hypotheses explaining this
been described to be associated with the loss of, or fact are contested but invariably detail the role of
inability to derive, solace connected to the present sociocultural factors, along with biogeographical
state of one’s home environment (see Albrecht et factors.
al. 2007).
To some, the intricacies of the relationships
Cultural heritage values. Many societies place high between linguistic, cultural and biological diversity
value on the maintenance of either historically suggest a co-evolution, or reciprocal development.
important landscapes (“cultural landscapes”) or Gorenflo et al. (2012) suggest that, in many
culturally significant species. Protection of heritage instances, this co-occurrence between biological
values will enhance cultural recognition, with and linguistic diversity may hint at some form
health and well-being benefits, particularly where of functional connection – perhaps founded
done without the continuation of any domination in a need to describe culturally or nutritionally
or oppression that might have occurred in the past, important species, habitats or landscape elements
allowing the continuation of cultural practices – though there is much local variability and the
where they have health-related outcomes. relationships are complex (see also Gavin and
Sibanda 2012; Axelsen and Manrubia 2014).
Recreation and ecotourism. People often choose
where to spend their leisure time based in part Pretty et al. (2008), drawing on the work of Berkes
on the characteristics of the natural or cultivated (2008) and others, conclude that cultural diversity
landscapes in a particular area. Recreation also and biological diversity are reciprocally developed
occurs in relation to animals or plants, caring and maintained.¹⁴ The links between language
for pets, or gardens, parks and reserves. Health and biodiversity also reflect a wider connection
outcomes relate to physical exercise, fitness between nature and a community’s sense of place.
and the myriad contributions this makes to Loss of language, and its concomitant cultural loss,
physical and mental health, and the alleviation of may be a source of considerable demoralization
psychosocial disorders. and anguish. In this sense, and assuming the
reciprocal relation, biodiversity loss is indirectly or
4.1 Indigenous health and well-being directly associated with these health consequences.
Moreover, the links between biodiversity and
The key literature on biocultural diversity – the
cultural and linguistic diversity suggest that the
intimate, inextricable links between linguistic,
protection of human rights can be connected to
cultural and biological diversity, as manifestations
the affirmation of human responsibilities toward
of the diversity of life – demonstrate their
and stewardship over humanity’s heritage in
overlapping global distributions, and the common
nature and culture (Maffi 2005).

¹³ Maffi describes the philosophical tradition that regards linguistic diversity as an adequate correlate for cultural diversity,
citing Harmon’s work that the perception of diversity is the basic condition for the functioning of human consciousness,
and Wollock’s observation that all great metaphysical traditions recognize endless diversity as the reality of the planet.
¹⁴ “How we know the world… governs our behaviour and practices that, in turn, shape landscapes, which form a cultural
archive of human endeavours. Amidst a diversity of cultures comes a diversity of meanings, leading to a diversity of actions,
providing an array of biodiversity outcomes.” (Pretty et al. 2008)

214 Connecting Global Priorities: Biodiversity and Human Health

Therapeutic and biocultural landscapes are an the guardians of our global biodiversity and its
important dimension to achieve health at the medicines, foods, shelter and spiritual resources
local level. Survival and vitality of knowledge and for millennia – built on a holistic communal
resources depend on the sociocultural contexts view of humanity and its links to the ecosystem.
in which they are embedded (see also the chapter Yet now, in the new millennium, indigenous
on traditional medicine in this volume). Typically, peoples are among those most marginalized
such knowledge and resources are found to be within many nation states, they have the worst
most vibrant among communities (specifically, health indicators, and their knowledge is fast
indigenous and local communities) close to disappearing as their land is appropriated and
culturally important landscapes. These could their environment destroyed.
relate to socioecological production landscapes
(e.g. Satoyama in Japan) or conservation systems But indigenous peoples also often have an intimate
(e.g. sacred groves, ceremonial sites) or therapeutic knowledge of the other valuable living resources
landscapes (such as sacred healing sites). Such available in their biodiverse settings – including
landscapes and related traditional knowledge medicines and foods that are vital for global
practices contribute to health and well-being, and local health (Box 5, Box 6). Instances where
therefore necessitating a close inquiry into the indigenous peoples have retained a profound
functional interlinkages within such systems, and connection to the land and water and living
maintenance of their dynamism. components of their territories, and instances
where socioeconomic and political forces have
As described in the chapters on nutrition and combined to alienate indigenous peoples from their
traditional medicines, indigenous peoples are cultural values and traditions, both demonstrate the
often a potent symbol of our human diversity of saliency of connections across biodiversity, cultural
culture, language and spirit. Many have also been knowledge, and human health and well-being.

Box 5. Biodiversity, essential for Mbya Guarani well-being and health

Those indigenous people that survive as hunters, gatherers and small-scale agriculturalists display
complex relationships between territory, biodiversity and ecodiversity (Montenegro 1992; 2006).
Among the Mbya Guarani who live in relatively self-decided isolation, like the communities of Tekoa
ma and Tekoa Kapi i vate in the subtropical forest of aboti (Misiones, Argentina), their well-being
and health system is the result of complex sustainable interactions. The main variables involved are
growing knowledge of the social and natural environment, e cient intergenerational transmission of
information, entire life educative schemes, lack of permanent private property and adaptive nomadic
behaviour. Their dominant long food chain strategy ensures direct and seasonal relationships with
di erent arrangements for biodiversity. Contemporary communities use, for example, 150 species
of medicinal plants, 35 plant species and 94 animal species as food, 54 species as raw materials for
rituals, artifacts, weapons and building, and 61 species as fuel (biomass) (Keller 2001; Montenegro
2004). Deforestation and biodiversity loss, mainly produced by foreigners, negatively a ects not
just their health system but also their rituals and well-being. Ñemongarai, the ceremony where the
opygua (= shaman) delivers names to children, demands – for boys – fruits of guembe epiphyte
(Philodendron bipinnatiƲdum) and honey from the wild bee jate’i (Tetragonisca angustula). Their
growing scarcity in abotí, as a result of biodiversity reduction, distresses both families of children
and the community (Montenegro 2004). Currently, most indigenous peoples develop hybrid
strategies that combine both traditional and foreign medicine (cf. Montenegro & Stephens 2006).

Indigenous well-being and health system are the result of “n” interacting variables organized in
seven Boxes (Figure 1), where biodiversity plus ecodiversity of the territory (A1) and of remnant

Connecting Global Priorities: Biodiversity and Human Health 215

 Parananse ecosystem (A2) are essential. Approaches that do not consider this minimum organization
of variables are unreal and cannot represent the complex source of indigenous well-being patterns
(Montenegro 2004).

ǡǤǢǰǭǠɻ Indigenous peoples health and the ecosystem

Group A: The ecosystem. A1: Indigenous territory and its biodiversity plus ecodiversity (>6000 hectares
for Tekoa Yma and Tekoa Kapi’i Yvate) within Paranaense subtropical ecosystem. A2: The remnant of the
Paranaense subtropical ecosystem (less than 5% of the original surface in Brazil and Argentina). Group
B: Resources obtained from the ecosystem. B1: Drinking water. B2: Fresh air. B3: Materials, e.g. for rituals,
artifacts and building. B4: Natural foods (plants, animals). B5: Space for houses (oo), temple (opy) and
the Tekoa (village). B6: Small-scale agriculture (mainly maize). B7: Medicinal plants. B8: Natural odours,
sounds and landscape colours. Group C: Well-being of the community, C1, and C2: “Ñande reko”, ancestral
happiness. Group D: Indigenous culture D1, which includes D2.1: Traditional medicine and D2.2: Traditional
health knowledge. Group E: Foreign culture, which includes E1.1: Non-indigenous culture and technology,
E1.2: Non-indigenous food; E2.1: Foreign medicine and E2.2: Foreign medicinal knowledge. Group F:
Indigenous health. Group G: Environmental destruction and biodiversity loss by deforestation, hunting
and other activities; G1: Environmental pressure (external, generated by foreign people and companies);
G2: Environmental pressure (internal, of indigenous activities, usually more diluted).

Source: Adapted from Montenegro 2004

216 Connecting Global Priorities: Biodiversity and Human Health

 Box 6. Ko Omapere te wai, Aotearoa (New Zealand)

The largest lake in Northland, Omapere (1197 ha), once a wetland forest, is shallow (2.6 m) and
feeds the Utakura River that ows west to the Hokianga Harbour. Omapere is a taonga (treasure)
to Ngapuhi, who maintain manawhenua (ownership) and kaitiaki (guardianship) rights and
responsibilities through indigenous leadership. Ngapuhi have fought for the protection of Omapere,
articulating the signi cance of its ecological integrity: use of the lake is determined by the health of the
lake; the health of the lake and the health of the people are intertwined (Henwood and Henwood 2011).

Omapere was a “food basket” that supplied tuna (eel), torewai (freshwater mussels) and other
resources, including raupo (bulrush), kapangawha (clubrush) and harakeke ( ax).

Clearing of native vegetation and dairy farming in the surrounding catchment led to dense growths
of invasive oxygen weed (Tanner et al. 1986) that eventually collapsed, leaving Omapere turbid and
algae dominated (Champion and Burns 2001). In 1985, the Northland Area Health Board advised the
municipality to abandon its water for domestic supply due to a severe cyanobacterial bloom that
polluted the Utakura River and upper reaches of the Hokianga, leaving traditional sh and shell sh
stocks unsafe to eat (Grey 2012).

In 2004, tribal leadership brought together community stakeholders and responsible agencies to
identify restoration and management strategies, implement monitoring and shing regulations, and
commission studies. The ma uta ki tai (catchmentwide) process adopted emphasized the physical
and social interconnectedness of waterways and human activities, and recommended integrated
solutions. Community-led fencing of the lake edges, riparian planting and a local species nursery
plus farm environmental plans reduced fertilizer run-o and dissolved nitrogen and phosphate levels
(Grey 2012).

There have been no algal blooms in the lake since 2007 and recent improvements in water quality
have been linked to increased water- ltering torewai populations (Grey 2012). Many customary
community practices of water use in the catchment have resumed and in 2011 tuna returned to the
tables of Mokonui-a-rangi Marae, welcoming guests with this traditional kai (food) for the rst time in
more than a decade.

4.2 Biodiversity and local and government policies and in life experiences. These
community health and well-being divisions not only undermine individual health
and well-being, but may also threaten community
Biodiversity is often central to cultures, cultural
cohesion, including among indigenous and local
traditions and cultural well-being. Species,
communities.
habitats, ecosystems and landscapes influence
forms of music, language, art, literature and dance. As discussed in the chapter on traditional medicine,
They form essential elements of food production indigenous and local communities often act as
systems, culinary traditions, traditional medicine, stewards of local-living natural resources based on
rituals, worldviews, attachments to place and generations of accumulated traditional knowledge,
community, and social systems. The divisive including knowledge of agricultural biodiversity,
nature of modern societies is evident in the gaps and biodiversity that supports traditional
between the rich and the poor, the able-bodied medicinal knowledge. Where local traditions
and those with disabilities, the employed and the and cultural identity are closely associated with
unemployed, and these are increasingly obvious in

Connecting Global Priorities: Biodiversity and Human Health 217

 Box 7. Biodiversity, physical health and community well-being

The “Feel Blue, Touch Green” project (Townsend & Ebden 2006) in 2005 engaged people
experiencing depression and/or anxiety in hands-on conservation activities in partnership with
ANGAIR (the Anglesea and Airey s Inlet Society for Protection of Flora and Fauna). Participants
committed to 10 hours of conservation activities over 5–8 weeks, and the project and its impacts
were evaluated using mood scales and in-depth interviews. The results showed that participants
experienced positive emotional changes, with the most positive changes being an improved sense
of relaxation, higher levels of interest and greater life satisfaction. Participants also scored highly
in terms of improved health and happiness. These ndings were corroborated through interviews
in which participants identi ed the importance of the context for and the focus of the activities
(particularly the emphasis on biodiversity maintenance) in fostering the bene ts they were gaining
and in transforming their interactions with the natural environment and with other people.

Those “bridging” bene ts were echoed in a study in 2007 (O Brien et al. 2008); using similar
evaluation methods, motivations, barriers and bene ts of environmental volunteering in southern
Scotland and northern England were explored. The groups studied ranged from local groups working
with councils or NGOs to restore degraded local environments through to a group of volunteers who
had raised £350 000 to purchase a valley in Scotland and were working to return it to the “wildwood”
it would have been 6000 years ago! Volunteers typically experienced positive emotional changes
on all parameters except pain, and even that was interpreted positively as indicating that they had
worked hard, thus contributing to satisfaction!

Face-to-face interviews with volunteers and representatives of the organizations hosting the
activities con rmed the individual, community and ecosystem well-being bene ts, many of which
can be characterized using this notion of “bridging”.

However, the most telling example of this bridging across the divides came on the day when four
diverse groups came together at Eskdale in the Lake District to do some coppicing (removal of
invasive species to allow room for the native vegetation to grow). The volunteers included four
persons from “Friends of the Lake District”, 10 “Environment Agency” sta members (i.e. corporate
volunteers), two Lake District National Park volunteers, and two sta and three residents of West
House (a facility for adults with developmental delays).

biodiversity and ecosystem services, declines in and ecosystem well-being. As the examples in
the availability and abundance of such resources Box 7 indicate, there are many more benefits that
can have a detrimental impact on community well- flow from human engagement in efforts to restore
being, with implications for mental and physical and maintain biodiversity through environmental
health, social welfare and community cohesion volunteering. Key among them is connectedness:
(see, for example, Box 8). to our own inner beings, to others and to the
natural environment; revisiting calls for “reciprocal
Efforts to promote and sustain biodiversity have maintenance” that have been foundational to
been shown to build bridges across these divides health promotion since the Ottawa Charter (WHO
and to offer new hope for individual, community 1986; Parkes and Horwitz 2009).

218 Connecting Global Priorities: Biodiversity and Human Health

 %R[3V\FKRVRFLDOKHDOWKDQGƩVKELRGLYHUVLW\LQ)LML

The high biodiversity ecosystems within the Paci c are the settings for health where cultural
identity, subsistence life and social systems exist (sensu Horwitz and Finlayson 2011). In a set of
studies from the small-island developing state of Fiji, enkins et al. (2010) demonstrated the notable
absence from degraded river basins of suites of sh that traditionally formed the staple diets of
inland communities. Notably absent species in heavily modi ed catchments include many migratory
species that form important commercial and cultural sheries for Paci c islanders. These e ects
are largely seasonal and magni ed in degraded catchments, with pronounced negative impacts
on food-provisioning services and biodiversity during heavy rainfall and severe storms ( enkins &
upiter 2011). These e ects will likely become more severe under predicted future climate scenarios.
Community bans on harvesting and clearing within riparian wetlands can be e ective in maintaining
sh diversity, even in areas where forests have previously been extensively cleared ( enkins et
al. 2010). However, these bene ts are rapidly lost once the ban is lifted and sh from rivers again
become scarce ( enkins & upiter 2011). Fresh sh often contributes more than 75% of the sh
consumption of both rural and urban areas of the Paci c, with the remainder comprising canned
sh (Bell et. al 2009). Given the high levels of sh consumption, and the limited opportunities for
agriculture and animal husbandry in small islands, sh usually contributes the majority of animal
protein in the diet at the national level (Bell et al. 2009). For many Fijian inland communities,
freshwater sh not only comprise a major part of the diet but also have important cultural totemic
values. Loss of freshwater sh biodiversity therefore has important implications for physical and
cultural well-being. Some authors note an ecology-driven model of well-being in many Paci c islands
that is based on the vitality and abundance of natural resources relied upon for subsistence and
cultural practices (McGregor et al. 2003). Within this ecological model, the collective family unit
forms the core social unit within which the individual lives and interacts, which is interdependent
upon the lands and associated resources for health (physical, mental and emotional) and social
well-being. This case illustrates the potential for physical and psychosocial health to be e ected
through loss in sh biodiversity. However, like many studies, while biodiversity loss can be clearly
demonstrated, the precise nature of impact on physical health through nutritional or cultural de cit
has not been investigated.

5. Conclusions and ways forward between biological diversity and cultural diversity,
and human health and well-being. The cultural
This chapter has presented an account of evidence
services provided by an ecosystem provide a useful
that suggests that biodiversity plays a role in
lens through which the interlinkages between
people’s lives, in their cultural traditions and in
biodiversity and health can be seen.
their social interactions, and that health outcomes
are a consequence of these relationships. Over half of the world’s population already lives
in cities and the transition toward urban and peri-
Species, habitats, ecosystems, and landscapes
urban areas is steadily increasing, which will be
form essential elements of food production
a major challenge for all countries, with notably
systems, culinary traditions, traditional medicine,
pronounced impacts in developing countries
rituals, worldviews, attachments to place and
(UN-Habitat & UNHSP 2010; Cohen 2006;
community, and social systems. The constructs
Cohen et al. 2012; Montgomery 2008). There is
of cultural ecosystem services, and ecosystems as
a rising trend for people, especially within poor
settings, can be used to frame the relationships
communities, to be separated from nature and

Connecting Global Priorities: Biodiversity and Human Health 219

 AMIRA_A / FOTER / CC BY
to be deprived of the physical, physiological and immunological analyses. In other instances, the
psychological benefits that ecosystems provide relationship is explored with spiritual, emotional
(Sandifer et al. 2015). This is not insignificant or intuitive worldviews, informed by the social
in the context of the shifting global burden of sciences. Research from all of these disciplines
disease, in which NCDs continue to account for an will provide for a comprehensive treatment of
increasing proportion of the burden. At the same the subject.
time, the rise in physical inactivity, combined
with dietary changes that often accompany the The diverse and interrelated implications of the
transition from rural to urban and peri-urban cultural appreciation of biodiversity for well-
areas, also importantly contribute to the burden being, including outcomes for physical and mental
of NCDs. These rising challenges present new health, are embraced by interlinkages that range
opportunities to produce benefits for biodiversity from obvious, direct and linear ones, to ones that
conservation and public health, through: are indirect and more complicated, often mediated
by socioeconomic factors and issues of scale, to
– urban planning to encourage active transport; ones that are more reciprocal, where biodiversity,
culture and human health are interdependent.
– building designs that enhance local
environments and cultural traditions; The interlinkages can be obscured or confounded by
the trade-offs of natural capital for other forms of
– creating settings for restorative health that capital, such as built, infrastructural and financial.
draw upon cultural ecosystem services; and While trade-offs are sometimes inevitable and even
necessary, these other forms of capital often give
– a deeper understanding of the ways in which a shorter-term well-being benefit, even though
positive and negative exposures to biodiversity are ecosystem services may have been degraded and
felt by individuals. biodiversity may have been lost. Exploring further
interdisciplinary study of the interlinkages between
Exploring these associations has been, and needs
biodiversity, physical and mental health, and
to be, an interdisciplinary and cross-sectoral
cultural ecosystem services provides both a framing
pursuit. In some instances, an empirical and/or
device for the post-2015 sustainable development
rational inquiry will demand and reveal evidence
goals, and a set of integrated indicators that will
to demonstrate a particular relationship, much
allow targets to be set.
like that expected of sound epidemiological or
ISTOCKPHOTO

220 Connecting Global Priorities: Biodiversity and Human Health

PART III
Cross-Cutting Issues,
Tools & Ways Forward
 13. Climate change, biodiversity
WORLD BANK PHOTO COLLECTION

and human health

1. Introduction from anthropogenic activity have risen more
rapidly between 2000 to 2010 than in any other
Climate change is one of the greatest challenges of period in human history (IPCC 2014b),⁴ and the
our time. It is now widely recognized that climate potential impacts of anthropogenic activity on
change and biodiversity loss¹ are interconnected, biodiversity under business-as-usual scenarios
and that both are increasingly influenced by are but another reminder of the critical need for
human activity (IPCC 2014; Pereira et al. 2010; action (CBD 2010; 2014). The impacts of climate
Campbell et al. 2009; Bellard et al. 2012; Parmesan change will be amplified as it interacts with a
et al. 2011; Rockström et al. 2009; Beaumont et al. range of other drivers; a warming climate not
2011; CBD 2009, 2003). The recently released Fifth only threatens the stability and functioning of our
Assessment Report (AR5) of the Intergovernmental planet’s biological and physical systems but also
Panel on Climate Change (IPCC) supports previous poses direct and indirect threats to global public
findings that climatic change will probably be health, with more pronounced impacts on the
perilously aggravated unless robust climate world’s most vulnerable populations (McMichael
adaptation and mitigation measures are adopted.² et al. 2006, 2012; Parmesan and Martens 2009;
Total greenhouse gas (GHG) emissions³ resulting Haines et al. 2006).

¹ The Fifth Conference of the Parties (COP) to the CBD highlighted the risks of climate change, in particular, to coral reefs
(decision V/3) and to forest ecosystems (decision V/4), and drew attention to the serious impacts of biodiversity loss on
these systems and their associated livelihoods. The cross-cutting issue on biodiversity and climate change was included in
the work under the Convention in 2004 through decision VII/15 of the COP. Among other subsequent COP decisions on
climate change, at its tenth meeting the COP in decision X/20 para 17b requested the executive Secretary to explore avenues
for bridging the gaps between work being carried out to address the impacts of climate change on public health and work
to address the impacts of climate change on biodiversity.
² These reports of the working groups and the synthesis report of AR5 are available at http://www.ipcc.ch/report/ar5/.
³ Based on the most recent IPCC estimates, the greatest contributors of greenhouse gases are: CO2 (76%); CH4 (about 16%),
N2O (about 6%) and the combined F-gases contribute about 2% (IPCC 2014a).
⁴ From 2000 to 2010, GHG emissions grew on average 2.2% per year compared to 1.3% per year over the entire period from
1970 to 2000. Moreover, although more recent data are not available for all gases, “initial evidence suggests that growth in
global CO2 emissions from fossil fuel combustion has continued with emissions increasing by about 3% between 2010 and
2011 and by about 1–2% between 2011 and 2012” (IPCC 2014b). By sector, the largest sources of GHG emissions came
from energy production, agriculture, forestry and land use (AFOLU), and industry (IPCC 2014a).

222 Connecting Global Priorities: Biodiversity and Human Health

The chapters in this volume have drawn attention In the health literature, recognition of links
to a number of risks posed to human societies between public health and climate change is
by the degradation of the earth’s ecological and now over a quarter century old, with pioneering
climatic systems, including threats to water papers in 1989⁵ published in the world’s two
and food security, air quality, the availability of leading English-language medical journals – the
natural resources used for medicinal, spiritual or Lancet and the New England Journal of Medicine
recreational purposes and livelihoods, population (Anonymous 1989; Leaf 1989). In the latter,
displacement, conflict and disasters, and potential Alexander Leaf stated that the “United States,
influences on patterns of disease. These burdens, with more than 19,000 km of coastline, will not
however, are not evenly distributed. The greatest be spared. For example, much of Florida sits
impacts often fall upon the most vulnerable on porous limestone. Miami has such a porous
populations, including women, children and aquifer that a protective dike against rising sea
poverty-stricken communities who are often levels would have to start more than 45 m (150
least directly responsible for global environmental ft) beneath the surface to prevent salt water
change, yet particularly vulnerable to the risks from welling up behind it. Displaced people and
posed by multiple environmental stresses less arable land would compound the problem
(Türkeş 2014). They are also, most frequently, of feeding the world’s increasing population.”
the least able to assess and address these risks. He added: “Probably the most widespread and
Vulnerable communities face a double challenge: devastating consequences of global environmental
the combined effects of climate change and changes are likely to result from their effects on
biodiversity loss undermine the partial progress agriculture and food supplies for the world’s
made to achieve the Millennium Development burgeoning population” (Leaf 1989).⁶
Goals (MDGs), which in turn further weakens
not only ecosystem integrity but also country or Health awareness and expertise on the subject of
community ability to respond to these risks. climate change and health was too young for the
topic to be explicitly included in the first IPCC
report (1990). This was corrected in the second
1.1 Impacts of climate change on
report, shortly followed by publication of the
human health
first edited book on climate change and health
Though anthropogenic climate change has been (McMichael et al. 1996; see also McMichael et al.
scientifically recognized since the nineteenth 2003). The World Health Organization (WHO) –
century, real interest in the topic began in 1957, which published the books – continues to play
during the International Geophysical year, with a leading role in developing the topic. Today,
the prophetic remark that “human beings are now the issue of climate change and health attracts
carrying out a large-scale geophysical experiment widespread interest from the public health sector
of a kind which could not have happened in the and is increasingly prominent in the international
past nor be reproduced in the future”(Callendar scientific literature. Increased attention by the
1958). By the time of the establishment of the scientific community has been accompanied by
IPCC by the World Meteorological Organization growing awareness of the issues among broader
(WMO) and the United Nations Environment public and civil society. Some analysts have
Programme (UNEP) in 1988, this was clearly expressed the hope that a general awakening by
understood, as the IPCC was called on to assess the public to the health risks of climate change will
“the scientific, technical and socioeconomic accelerate the nascent “sustainability transition”
information relevant for the understanding of the needed to ensure the survival of civilization
risk of human-induced climate change.”

⁵ That same year, the World Health Organization (WHO) set up a task group on the subject and in 1990 published a report
on the “potential health effects of climate change”. Available at http://whqlibdoc.who.int/hq/1990/WHO_PEP_90_10.pdf
⁶ An article published in the Lancet that same year raised the additional possibility of conflict associated with climate change
(Anonymous 1989).

Connecting Global Priorities: Biodiversity and Human Health 223

 (McMichael et al. 2000), even beyond that of difficult to catalogue all the impacts of climate
commensurate awareness in other disciplines. change on human health, Box 1 summarizes a
threefold approach that can help us conceive
The myriad health effects of climate change can primary, secondary and tertiary impacts that
be categorized into three broad categories (Butler affect the biodiversity–health nexus.
2014a): direct, indirect and tertiary. While it is

Box 1. Direct, indirect and tertiary impacts of climate change on human health

Direct

Direct health impacts are those that are directly, causally attributable to climate change and/or
climate variability, such as cardiovascular risk associated with heat waves, or risk of injury associated
with more intense and frequent storms. The recent ndings of Working Group III of the IPCC have
indicated, with a high degree of con dence, that the impacts of recent climate-related extremes,
including heat waves, droughts, oods, cyclones and wild res, have already led to vulnerability
and exposure of some ecosystems and several human systems to current climate variability. Such
extreme weather events impact vulnerable groups such as the poor and elderly the most, though the
adverse e ects on human health can be ameliorated to a certain extent by social and technological
mediators, such as improved urban design and building standards (e.g. Santamouris 2013; Brown and
Southworth 2004; Birkman et al. 2010).

Despite scienti c argument over whether the witnessed increase in heat waves, res and adverse
crop yields in Eurasia in 2010 were random or had been exacerbated by anthropogenic climate
change, the event still directly contributed to 50 000 excess deaths (Barriopedro et al. 2011). The
subsequent rise in global grain prices further indirectly impacted human health and food security
among vulnerable populations worldwide ( ohnstone and Mazo 2011). As such, the e ects of climate
change on water, food security and extreme climatic events are likely to have profound direct impacts
on global public health (Costello et al. 2009). Heat-wave induced mortality of food source species,
ecological keystone species, and disease vectors and reservoirs are other examples of primary e ects.

Indirect

Indirect health impacts arise as downstream e ects of climate change and variability. These impacts
are broad and variable in their etiology, such as change in infectious disease vector distribution and
air pollution interacting with heat waves.

The changing ecology of disease-bearing vectors was raised by Leaf in 1989, though the health impacts
of climate change on vector-borne diseases has been contested by some ecologists (e.g. La erty
2009) and experts from within the disease community (e.g. Gething et al. 2010; Randolph 2009). The
debate is nally showing signs of abatement for some of the most prevalent vector-borne diseases,
including malaria. Consensus is emerging that, indeed, climate change does magnify such risks (Siraj et

⁷ Several plausible reasons have been put forth to explain their lack of prominence – the most likely being the interdisciplinary
nature of these issues in the context of a scientific community that is still poorly equipped to equitably hear, consolidate
and incorporate numerous competing interests, including those of social scientists (Castree et al. 2014; Heller and Zavaleta
2009). Thus, recent scientific culture has been reluctant to venture beyond a fairly narrow band of thinking, effectively
tabooing integrative cross-sectoral analysis and written reflection on challenges such as differences in economic, political,
cultural and other forms of power, population growth, the “right” to unbridled consumption and limits to growth and
corresponding impacts on health, biodiversity and life-sustaining ecosystem services.

224 Connecting Global Priorities: Biodiversity and Human Health

 al. 2014), though advances in technology, prevention and treatment can combine to reduce the burden
of diseases like malaria (Feachem et al. 2010). Climate change directly contributes to damage of both
infrastructure and human settlements, resulting in human mortality and morbidity that includes the
mental health and well-being of survivors (IPCC 2014d). In countries at all stages of development, these
impacts are consistent with a lack of preparedness for climatic variability in some sectors; the most
salient manifestations will be among the poorest and most vulnerable populations (IPCC, 2014d).

Tertiary

The third – “tertiary impacts” – category is, by a number of magnitudes, the most important health
risk associated with climate change (Butler 2014b). These include the health impacts of large-scale
famine, forced migration and human con ict, which result from the geophysical and ecological
consequences of climate change, including the alteration of ecosystems, sea-level rise, and long-
term disruptions in water supply and food production. Surprisingly, with rare exceptions, this group
of e ects has been little mentioned in the intervening decades, including in the most recent IPCC
reports released in 2014. These must be considered more holistically as we prepare to embark upon
new global commitments on climate change and a post-2015 Development Agenda.

Many authors in this volume point to numerous it has undergone multiple evolutionary changes
synergies (“co-benefits”) that could flow to both and adopted natural adaptive strategies. Until
human well-being and ecological “health” from a the advent of industrialization, changes in
more biosensitive approach to our relationship climate occurred over an extended period of
with nature (Boyden 2004), such as the co-benefits time, in a landscape much less degraded and
of cycling on both health and environment. fragmented than today, and with considerably
Awareness of these co-benefits may also accelerate less – if any – pressure from anthropogenic
global social transformation (Haines et al. 2009; activity. Habitat fragmentation has confined
Raskin et al. 2002). On the other hand, many many species to relatively small areas within
forms of inertia: social, institutional, technological their previous ranges, resulting in reduced genetic
and perhaps, above all, climatological, slow and variability (Parmesan and Matthews 2006) and
impede the likelihood of a successful transition, other changes to structure and composition (CBD
most notably an enormous countermovement, 2009). Warming beyond the highest temperatures
funded and fuelled by vested interests profiting reached during the Pleistocene will continue to
from “environmental brinkmanship” (Butler stress biodiversity and ecosystems far beyond
2000). Delay is also worsened by the scientific the levels imposed by the climatic changes that
knowledge gaps of many economists and policy- occurred in the evolutionary past (Templeton et
makers, who have been very slow to awaken to the al. 1990; Parmesan 2006).
risks we face, and who are instead wedded to more
conservative or sectoral measures of progress, or The impacts of climate change on biodiversity
to the hope that technological innovation alone operate at different levels (including microbial,
will eventually solve the problem. individual, population, species, community,
ecosystem and biome), with variable responses
at each level (Bellard et al. 2012; Parmesan
1.2 Vulnerability of biodiversity to
and Martens 2009). For example, increased
impacts of climate change
temperatures coupled with decreases in the
The earth’s biota was shaped by fluctuating distribution of precipitation may reduce
Pleistocene concentrations of atmospheric freshwater levels in lakes and rivers (Campbell
carbon dioxide, temperature and precipitation; et al. 2009). Warmer temperatures cause fish

Connecting Global Priorities: Biodiversity and Human Health 225

 populations to redistribute towards the poles, and (Bellard et al. 2012). Pollution is another pressure
tropical oceans to become relatively less diverse interacting with climate change (Seinfeld and
(CBD 2010). In other systems, drought may cause Pandis 2012), and causing disruption to aquatic
some tree species to disappear and in turn also (Schiedek et al. 2007), terrestrial (Cramer et al.
fundamentally affect both vegetation structure 2001) and marine ecosystems (Harvey et al. 2006).
and species composition (February et al. 2007).
It is difficult to analytically separate the influence
Models of future biome distributions in tropical of each of these drivers, as anthropogenic climate
South America have found that substantial change and its effects are intimately dependent on
shifts in the region may lead to the substitution interactions with other pressures such as land-use
of Amazonian forest cover by savannah-like change and attendant habitat loss, and changes in
vegetation (Salazar et al. 2007; Lapola et al. water use, which themselves feed back into the
2009). The interaction between climate change, hydroclimatic cycle (Elmhagen et al. 2015). These
deforestation and fire can also lead to widespread interactions in turn influence the ability of natural
forest dieback, with some parts moving into a systems to respond at various spatial and temporal
self-perpetuating cycle of more frequent fires and scales (Campbell et al. 2009). Further research on
intense droughts. At the same time, more frequent the complex interactions between these variables is
and powerful forest fires can compromise both the critical, and we must also consider the underlying
productivity of forests and their ability to store socioeconomic and other drivers of land-use change
carbon (Barlow and Peres 2008; Bush et al. 2008). at multiple scales (Elmhagen et al. 2015; Lambin
These combined impacts often lead to a reduction et al. 2001; Myers et al. 2013), and integrate input
in regional rainfall, compromising agricultural from a larger number of disciplines.¹⁰
production, livelihoods and food security (CBD
2010). Other models examining changes in natural An abundant number of predictive scenarios
vegetation structure and function in response to have shown no signs of abatement without the
climate change predict that changes in vegetation implementation of additional measures, including
cover in the tropics,⁸ particularly in portions of robust climate mitigation and adaptation
West and southern Africa and South America, strategies (e.g. IPCC 2014; CBD 2014). Alarmingly,
also include forest dieback (Alo and Wang 2008; some recent studies suggest that the impact of
Barlow and Peres 2008). Continued warming climate change on biodiversity has been estimated
trends in oceans will accompany acidification as to have surpassed that attributed to land-use
a result of increased carbon emissions, resulting change and habitat loss (Selwood et al. 2014). As
in widespread degradation of tropical coral scientific research on individual drivers continues
reefs⁹ (Doney et al. 2009; Carpenter et al. 2008; to proliferate, the impact of simultaneous multiple
Hoegh-Guldberg et al. 2007; Orr et al. 2005), and drivers, such as climatic changes driven by human
affecting the genetic and species diversity and water use for both food and energy production,
composition of marine species such as molluscs, remains a critical area for further research (Bellard
with corresponding impacts on our own sources et al. 2012; Destouni et al. 2013; Elmhagen et al.
of food, medicines, recreation and transportation 2015).

⁸ It should be noted that simulated biosphere responses are model-dependent.

⁹ Tropical coral reefs and amphibians have already been among the most negatively affected global biota, and range-restricted
species, most notably polar and mountaintop species, have already led to species extinctions (Parmesan 2006). Current
rates and magnitude of species extinctions (terrestrial, freshwater and marine) far exceed normal background rates, with
increases of up to 1000 times that of historical background rates (MA 2005).
¹⁰ For example, Lambin et al. (2001) suggest that land-use change is driven by both proximate causes (which are local and
direct, and explain how and why anthropogenic activity acts on land cover and on ecosystem processes at a local scale), and
underlying causes (indirect or root causes based on regional and sometimes global policies, economic forces and technological
advancement that interact with and mediate the relationship at the local scale). The complex interactions between proximate
and underlying causes interact over time (in a limited number of ways) to drive land management decisions and practices.

226 Connecting Global Priorities: Biodiversity and Human Health

2. Climate change challenges at Climate-driven shifts in species distribution,
the intersection of biodiversity abundance, seasonal cycles, desynchronized timing
of life history events and ecosystem disruptions
and human health caused by extreme weather events have profound
Climate change and variability have irreversible potential to disrupt and erode ecosystem services,
impacts on the global environment by altering release pathogens from previous constraints, and
hydrological systems and freshwater supplies, leave human populations ill-equipped to deal with
advancing land degradation and loss of compounding health challenges. However, studies
biodiversity, and debilitating food production of human health as a complex social–ecological
systems and ecosystem services, thus affecting system, replete with climate vulnerability,
health outcomes (WHO 2005). These factors are are relatively recent (McMichael and Wilcox
closely interrelated, as deforestation, industrial 2009). Figure 1 shows the complexity of the
agriculture and centralized livestock production nexus between climate, biodiversity and social
systems further accelerate climate change and interactions. Resilient or vulnerable communities
biodiversity loss, thus contributing potential risks may cope better, or worse, with both climate and
to food security, nutrition, and other aspects of biodiversity changes. Although building resilient
health, livelihoods and well-being. communities is essential, in particular, given
existing pressures on climate and ecosystems, the
The IPCC has identified key risks across sectors most efficient response is to jointly halt carbon
and regions including, among others: (i) risk of loss emissions and ecosystem destruction.
of biodiversity of marine and coastal ecosystems,
the goods and services they provide for coastal Attributing causality is complex (Parmesan et al.
livelihoods, especially for fishing communities 2011; Parmesan and Yohe 2003) and presents a
in the tropics and the Arctic, challenging challenge to meta-analyses and the translation
sustained fisheries and aquaculture; (ii) risk of of scientific research into simple strategies for
loss of terrestrial and inland water ecosystems, health or conservation agencies. Despite this
biodiversity, and the ecosystem goods, functions challenge, observation and predictive studies
and services they provide for livelihoods; and (iii) of the direct, indirect and cumulative effects of
risk of food insecurity and the breakdown of food climate change on human health acting through
systems linked to warming, drought, flooding, multiple levels of biodiversity are increasing. This
and precipitation variability and extremes, body of information is guiding surveillance and
particularly for poorer populations (Field et al. further targeted research.
2014). In addition, rising CO2 levels over the next
century is likely to affect food nutritional quality, The breadth of interest in addressing climate
including the decrease of protein concentration change within the context of interlinked human,
and other nutrients of many human plant foods animal and ecosystem health at a global scale
(Taub 2008; Fernando 2012; Myers 2014). Ocean is discussed in the subsections below. We can
acidification due to increased CO2 concentration identify several complex relationships with the
poses substantial risks to marine ecosystems, primary, secondary and tertiary effects introduced
especially polar ecosystems and the biodiversity in Box 1.
of coral reefs, thus challenging invertebrate
fisheries and aquaculture (Portner et al 2014). 2.1 Climate change, food security and
Reductions in marine biodiversity due to climate nutrition
change and ocean acidification might reduce the
discovery of marine genetic resources useful in the The combined risks noted in the preceding section
pharmaceutical, aquaculture and other industries and in the chapters on agricultural biodiversity and
(Arrieta et al. 2010). nutrition constitute a challenge for food security
and nutrition. This is particularly the case for the
least developed countries and most vulnerable

Connecting Global Priorities: Biodiversity and Human Health 227

 ǡǤǢǰǭǠɻ Interactions between climate, biodiversity and social factors. Health is at the centre, in the
intersection of these three drivers. The arrows are not causal but an expression of the dynamics inherent
in the drivers. Social factors may be protective or harmful to health and well-being; climate drivers impact
on biodiversity, on the social factors and directly or indirectly on health. Changes in biodiversity and
ecosystems interact synergistically with climate change and are inƦuenced by social factors. These feedback
loops may magnify biological change and they sometimes exacerbate negative human health outcomes,
directly or indirectly.

Bi

ol
ge

og
han

ica
Climate drivers: Water FuncƟoning

l div
Climate c

Temperature Food or impaired

PrecipitaƟon Air ecosystem

ersity
Extreme climate services
Health
Direct,
Indirect,
Health & TerƟary Community
impacts Engagement,
nutriƟonal
status TradiƟonal
MigraƟon knowledge

Resilient or
vulnerable
communiƟes

S o cial
factors

communities, such as indigenous populations, agricultural inputs, infrastructure and education

subsistence farmers and gatherers, pastoralists, (Field 2014). Indigenous peoples rely on their
coastal populations and artisanal fisherfolk (FAO natural resources for the provision of traditional
2008; Tirado et al. 2010). According to the IPCC, foods, fuel and medicines, and will be particularly
the risks of global aggregate impacts are moderate affected by the impacts of climate on ecosystems,
for additional warming between 1°C and 2°C, biodiversity and the environment (FAO 2008;
reflecting impacts to both the earth’s biodiversity Tirado et al. 2010). Traditional food systems are
and the overall global economy. However, further threatened because of increasing loss of
extensive biodiversity loss with associated loss indigenous peoples’ traditional territories due to
of ecosystem goods and services results in high climate change mitigation measures such as carbon
risks at around 3°C additional warming (Field et sinks and renewable energy projects (FAO 2008).
al. 2014). The demand for biofuel is likely to remain high,
and this may result in the clearing of biodiverse
Major climate impacts on water availability and land, such as tropical forests and wetlands, for the
food security affect disproportionately the welfare purpose of biofuel cultivation (Tirado et. al 2010).
of the poor, including indigenous populations,
women and girls, female-headed households In this context, it is essential to look for the
and those with limited access to land, modern co-benefits of nutrition-sensitive climate

228 Connecting Global Priorities: Biodiversity and Human Health

adaptation and mitigation strategies (Tirado et al. 2012). In this context, effective responses will
al. 2013). Across varying global landscapes, the necessitate innovative cross-sectoral initiatives
ability for family farms, integrated agroforestry and integrative climate adaptation and mitigation
and farming systems to conserve, restore or strategies, such as ecosystem based-adaptation
augment biodiversity (e.g. species, genetic (e.g. see Box 3).
and ecosystem diversity) offer opportunities
to enhance dietary diversity and nutrition, 2.3 Climate change impacts on
and promote climate resilience, especially as traditional medicines, pharmacology
considered within broader social, economic and and toxicology
environmental policy frameworks. Adaptation
measures targeting biodiversity (and ecosystem Diversity in the production of secondary chemical
diversity) can simultaneously provide nutrient- products remains an important source of existing
rich food, and benefit the environment through and new metabolites of pharmacological interest
supporting services such as pollination, nutrient in medicinal plants, and this may be affected by
cycling, temperature and water regulation, soil climate change (Ziska et al 2009). Few studies
formation and pest control (CBD 2010). have examined how pharmacological compounds
might respond to recent or projected changes in
CO2 and/or temperature. For example, increases
2.2 Climate change and water security
in growth temperature and CO2 affect the
As the chapter on freshwater and agricultural production and concentration of atropine and
biodiversity in this volume describes, the scopolamine in jimson weed (Datura stromonium)
provision of clean water for drinking, sanitation (Ziska et al. 2005), and recent and projected
and agricultural uses is both an essential service CO2 concentrations increase the production of
regulated by ecosystems and an important health morphine in wild poppy (Papaver setigerum) (Ziska
determinant (WHO 2012). While the long-term et al. 2008).
impacts of climate change on water resources
are difficult to quantify, it is well established that More than 700 plant species are poisonous to
human communities are reliant on groundwater humans. Rising temperatures and longer growing
for drinking, sanitation and other uses essential to seasons would in principle increase the presence
human survival; yet rising sea levels cause saline of such species in the environment, but the
water intrusion into essential groundwater aquifers interaction between CO2 and on the concentration
near coastal regions, decreasing the availability of or production of such poisons and plant toxicology
water resources for human purposes (Vörösmarty is largely unknown (Ziska 2015) and needs to be
et al. 2000). Climate change contributes to more explored. More than 100 different plant species
intermittent and intense precipitation patterns, are associated with contact dermatitis, which
increases the risks of floods, droughts and other occurs by contact with plant chemical irritants
hazards, causes the melting of glaciers and present in leaves, flowers, savia roots, etc. One
increases evapotranspiration rates, amplifies well-known chemical is urushiol that induces
existing global public health challenges, and contact dermatitis in the poison ivy group
further destabilizes the balance of environmental (Toxicodendron/Rhus spp.). Poison ivy growth and
and social systems (WHO 2012). urushiol congeners are highly sensitive to rising
CO2 levels (Mohan et al. 2006). These results
Variations in the hydrological cycle resulting suggest possible links among rising CO2, plant
from climate change must be closely monitored biology and increased contact dermatitis. This area
(Vörösmarty et al. 2000), together with the deserves further research.
physical, biological and chemical processes that
drive them at multiple levels, with consideration
for the socioeconomic and political contexts of
our human-dominated earth system (Bogardi et

Connecting Global Priorities: Biodiversity and Human Health 229

 2.4 Climate change and infectious a major public health problem, with ongoing
disease emergence and re-emergence outbreaks occurring in low-income countries with
poor access to sanitation infrastructure¹² (Ali et
The complex interactions between ecological
al. 2012). Rising ocean temperatures affect the
factors and climate change increasingly predict
ecology of the aquatic environment, for example,
changes in the global epidemiology of many
by increasing algal blooms, with corresponding
vector-borne and waterborne diseases (WHO
implications for the epidemiology of diseases
2012). This is of growing interest and concern
such as cholera. The population dynamics of this
for scientists from a variety of fields, including
pathogenic microorganism in the environment is
ecology, microbiology, epidemiology and related
strongly influenced by environmental factors such
medical fields (Lipp et al. 2002). Additionally,
as salinity, seasonal patterns and the presence of
interest is garnered from experts in the social
copepods,¹³ which in turn are modulated by larger-
sciences, aware of the close relationship between
scale changes in climate (Lipp et al. 2002; Vineis et
the geophysical environment and the economic
al. 2011). Prolonged floods and droughts may also
and social systems it sustains. Such interest
contribute to water contamination and potentially
emerges from concerns over human and animal
exacerbate the risks of cholera and other forms of
health problems vulnerable to the interaction
diarrhoeal disease (WHO 2012).
between climate change and other factors, such
as increasing antibiotic resistance (Patz et al. In natural systems, changing climatic variables can
2005; Epstein 2001), emerging infectious diseases fundamentally influence successional processes
(Jones et al. 2008; Wilson 1991), and potential and community dynamics. For example, a 12-year
vulnerabilities of medicinal and aromatic plant warming experiment in Colorado, USA, to evaluate
(MAP) species.¹¹ These, in turn, have subsequent the damage of pathogens and herbivores on six
influence on the cultural and socioeconomic of the most common plant species (i.e. Artemisia
determinants of health (Cavaliere 2009; Padulosi tridentata, Helianthella quinquenervis, Erigeron
et al. 2011). speciosus, Potentilla gracilis, Potentilla hippiana and
Lathyrus leucanthus) found that plants exposed to
There is mounting evidence that climate change
warmer temperatures suffered the most damage
will alter the patterns of animal (Altizer et al. 2013;
and were attacked by a larger number of species.
Harvell et al. 2002), plant (Pautasso et al. 2012)
The study concluded that climatic changes
and human (Patz et al. 2005; Purse et al. 2005)
are likely to result in changes to community
diseases. Additional evidence suggests that rising
composition (Roy et al. 2004). Although there are
temperatures and changing humidity and rainfall
few long-term datasets (for examples, see Jeger
patterns have already altered the distribution of
and Pautasso 2008; Fabre et al. 2011), a large
some waterborne illnesses and disease vectors
number of other scientific analyses and modelling
(IPCC 2014d), notably affecting populations
projects have been carried out to examine the
with little or no acquired resistance and, as such,
impacts of climate change on plant pathogens
causing health systems to be destabilized (WHO
and many have reached similar conclusions (see
2012). For example, as the chapter on water
Pautasso et al. 2012 and references therein).
quality indicates, cholera (causative agents Vibrio
cholerae O1 and Vibrio cholerae 0139) remains

¹¹ Whether climate change poses a more prominent threat to MAP species than other threats such as unsustainable use is
not established. However, the potential effects on MAPs may be particularly significant due to their cultural and medical
value within traditional medicine systems (Cavaliere 2009). Moreover, given that many wild species, including MAPs, grow
in mountainous regions, it is likely that at least some will be at risk (Padulosi et al. 2014).
¹² According to recent WHO estimates, only 5–10% of the actual number of cholera cases occurring worldwide are reported,
and of the estimated 3–5 million cases that occur globally every year, about 100 000 to 120 000 people die (Ali et al. 2012).
¹³ The causative agents of cholera include brackish waters (Tamplin et al. 1990) and crustacean copepods (Huq et al. 1983),
and climate change contributes to an increase in both.

230 Connecting Global Priorities: Biodiversity and Human Health

Box 2 discusses the impact of heat waves and other within it, including altitudinal and latitudinal
extreme weather events on fruit bats and bat-borne range shifts in Africa and South America (Siraj
diseases. Loss of host predators and competitors, et al. 2014). While for many human diseases the
changes in parasite and pathogen survival and potential effects of climate change are obscured
reproduction are additional mechanisms by which by socioeconomic factors and control efforts,
climate change impacts infectious disease. For strong evidence of climate effects on infectious
malaria, disease transmission-enhancing changes disease comes from invertebrate, animal and plant
have been described in the population dynamics diseases (Altizer et al. 2013).
of both the mosquito vector, and the pathogen

Box 2. Bat-borne diseases, climate, heat waves and extreme weather events:
mounting evidence of important relationships

Bats, and fruit bats in particular, became the focus of increased human health interest after
novel diseases, including Nipah virus disease and SARS, emerged in the 1990s–2000s. Land-use
change and bush meat hunting are the suspected primary reasons for shifts in host and pathogen
relationships (Luis et al. 2013) but the impact of climate is likely to be an additional factor in their
emergence and continued transmission, as these species are capable of ying long distances to
optimize resources and nd alternative roosts. Widespread bush res in Sumatra were suspected of
in uencing fruit bat–pathogen dynamics prior to the emergence of Nipah virus in Malaysia in 1998
(Chua 2003). While epidemic enhancement and agricultural intensi cation are co-factors (Pulliam et
al. 2012), it remains possible that the res and other climatic stress factors on food resources have
in uenced viral loads and spillover (Daszak et al. 2013).

More speculatively, climate change, together with deforestation and other land-use changes, has
been hypothesized as a contributing factor in the recent outbreak of Ebola virus in West Africa (see
also the chapter on infectious diseases in this volume). It is di cult to isolate climate as a driver in
the context of extensive deforestation and profound economic and public health failures, further
undermined by years of civil con ict (Bausch and Schwarz 2014). However, prolonged depression
of primary forest production during lengthy droughts in central Africa followed by sudden rainfall
events appears to enhance the opportunity for Ebola transmission between bats and other wildlife
that concentrate on available resources (Tucker et al. 2002).

During the Australian summer of 2014, an estimated 100 000 fruit bats fell dead in the streets
of Brisbane and south-eastern Queensland towns. (The number that died outside urban areas is
unknown.) The bats are highly temperature sensitive (Welbergen et al. 2008) and it is unlikely they
could survive a heat wave with temperatures above 43°C. Removing corpses was a major exercise
for the urban authorities, and gloves and collection bins were supplied to residents. At least 16
people were treated for possible Australian bat lyssavirus (related to rabies and fatal without
immunoglobulins) after they were scratched or bitten by dying bats. It is yet to be understood
what e ect the deaths will have on the bat colonies themselves. The 2011 spike and dispersed
distribution of another zoonotic (transmissible to humans) Australian bat-borne disease, Hendra
virus, is believed to be a consequence of the dispersal of bats after widespread ooding in south-
east Queensland following Cyclone asi in 2010. The higher latitude range extension of two host
species of this disease, and increased urbanization of all four, in preceding decades are suspected
factors in disease emergence (Plowright et al. 2011).

Connecting Global Priorities: Biodiversity and Human Health 231

 2.5 Climate change and disaster risk increase the number of people exposed to coastal
reduction flooding more than tenfold by 2080 (a rise of
more than 100 million people a year) (CBD 2010).
Based on recent data from the United Nations
Rising seas could also impact on human health
International Strategy for Disaster Reduction
and well-being through an increase in salination
(UNISDR), well over 80% of disasters are related
of coastal freshwater aquifers, and by disrupting
to climate, contribute enormously to economic
storm water drainage and sewage disposal (Patz
losses and, as the chapter on disaster risk
2001). In turn, repeated flooding or increased
reduction in this volume also indicates, trigger
salination can lead to population displacement,
short- and long-term population displacement.¹⁴
thereby further heightening the vulnerability
The impact of climate change on the frequency
of populations (Costello et al. 2009). As several
and intensity of extreme weather events, such as
case studies in the chapter on disaster risk have
extreme precipitation, coastal flooding and heat
shown, refugees suffer substantial health burdens,
waves, is already exacerbating risks to unique and
overcrowding, lack of shelter and competition for
threatened ecosystems, costing human lives and
resources, which is also often associated with
decreasing the viability of human settlements. In
conflict (WHO 2012).
the last decade of the twentieth century, extreme
weather events accounted for the death of some The United Nations (UN) World Conference on
600 000 people and caused damages worth billions Disaster Risk Reduction recently adopted the
of dollars (Hales et al. 2003). Based on the most Sendai Framework for Disaster Risk Reduction
recent findings of Working Group II of the IPCC, 2015–2030, recognizing the intimate links
the risks posed by some extreme events, such as between disaster risk, climate change and
heat waves, are likely to be enhanced with only 1°C poverty. The confluence of these conditions lead
of additional warming. A large number of species to a convergence of less resilient built, natural and
and systems with limited adaptive capacities, human environments, making populations more
including Artic sea ice and coral reef systems, are vulnerable to displacement, disease and the loss
considerably threatened by a warming climate of livelihoods. To meet the resulting ambitious
and, from a human perspective, many cultures global targets, as well as those that may emerge
are already at risk. The distribution of impacts from other global frameworks in 2015 – including
from extreme weather events is uneven, with under the UN Framework Convention on Climate
disadvantaged and vulnerable populations in Change (UNFCCC) process on climate change and
countries at all levels of development being at in the UN post-2015 Development Agenda – each
greatest risk (IPCC 2014d). of the sectors must meaningfully engage, together
with political authorities, local communities, civil
Rising sea levels caused by the warming of the
society, and the public at large to understand and
ocean, glacial melt and wetlands alteration (e.g.
address the combined risks of poverty, land-use
Syvitski et al. 2009) can cause increased flooding
change, ecosystem degradation, climate change
and the erosion and inundation of coastal
and poor urban planning.
ecosystems, further endangering wetlands
and posing concomitant threats to coastal
communities, including those of small island
developing states (SIDS).¹⁵ Without a significant
scaling up of climate adaptation efforts, it has
been projected that the rise in sea levels could

¹⁴ See http://www.unisdr.org/archive/42862 from 6 March 2015.

¹⁵ The recently concluded “SAMOA Pathway” that emerged from the third UN Conference on Small Island Developing States
held in September 2014 highlights the importance of a range of issues at the nexus of biodiversity, health and development,
including climate change, in the context of particular threats faced by SIDS. See for example: http://www.sids2014.org/
index.php?menu=1537.

232 Connecting Global Priorities: Biodiversity and Human Health

ã.5.1 %ountain e;osQsteEs and ;liEate power), downstream industries and livelihoods
;hange at the interse;tion of Oater and (Price 1998). The large majority of the planet’s
food se;uritQ disease eEergen;e and major rivers and tributaries depend on water
extreEe Oeather eNents that begins the terrestrial phase of its cycle in
mountain regions (Bajracharya and Shrestha
Mountain ecosystems are critically important
2011; Bandyopadhyay et al. 1997; MA 2005; CBD
centres of biodiversity. They play a unique role in
2012). In arid and semi-arid regions, over 90% of
the supply of services essential to human survival,
river flow is derived from mountains (Price, 1998).
especially critical to mountain dwellers and
lowland communities. Occupying approximately Mountain ecosystems are particularly vulnerable
one fifth of the land’s surface, mountains play a to the impacts of climate change, with
critical role in the water cycle both by capturing corresponding impacts on the populations reliant
moisture from air masses and as water sources¹⁶ upon the critical resources and services they
stored as snow, ice and permafrost, which provide provide, including water, energy, timber and food
fresh water to sustain communities, agriculture, (see Box 3).
energy production (primarily hydroelectric

Box 3. Climate change and ecosystem-based adaptation in the Hindu Kush HimalayasƸƾ

The Hindu Kush Himalayas (HKH), otherwise referred to as the greater Himalayan region, extend
from eastern Nepal and Bhutan to northern Afghanistan, and have among the most extensive areas
covered by glaciers and permafrost on the planet. They contain water resources that drain through
ten of the largest rivers in Asia, from which over 1.3 million people derive their livelihoods and
upon which many more depend for water and other resources (Eriksson et al. 2009). The region has
been recognized as a uniquely biodiversity-rich area with equally unique topographic characteristics
and socioeconomic and environmental challenges. The accelerated rate of warming, glacier ice
melt and related implications on the hydrological systems of central, south and east Asia are among
the most widely cited (Armstrong 2010; Eriksson et al. 2009). The retreating of glaciers (in this region
and elsewhere) is a sentinel indicator of climate change but also one of the most di cult to quantify,
given the physical and spatial complexity of glaciers and data collection.

Ongoing challenges in regions in which large proportions of the population live in mountain
communities, such as Bhutan and Nepal, include poverty, poor medical support, less access to
education and shorter life expectancies. While climate change may bring some bene ts to mountain

¹⁶ In the greater Himalaya region, it is estimated that snow and glacial melting contribute approximately 50% of annual river
flows (Eriksson et al. 2009).
¹⁷ Here, the term Hindu Kush Himalayan (HKH) sometimes referred to as greater Himalayan region, includes the Himalayan,
Hindu Kush, Karakoram, Pamir and Tien Shan mountain ranges, where there is currently glacier coverage. The HKH,
however, does not constitute one single region, as the eastern Himalayas are separated from the Karakoram–Hindu Kush
mountains by approximately 2000 km, though there is no sharp separation between east and west. Differences in climate
and in glacier behaviour and dynamics have been reported across the area, with variations in these conditions throughout
(Armstrong 2010).
¹⁸ These are the Amu Darya, Brahmaputra, Ganges, Indus, Irrawaddy, Mekong, Salween, Tarim, Yangtze and Yellow Rivers.
¹⁹ It has been estimated that global warming in the region has been 0.6 ºC per decade versus 0.74 ºC per hundred years as a
global average (Eriksson et al. 2009).
²⁰ Several glaciers in the extended HKH region are retreating but the extent of the impact of climate change on glacier ice is not
well known as glacier data in the Himalayas and surrounding mountains are very sparse and conditions vary significantly
along the south–east to north–west transect of the Himalayan–Karakoram–Hindu Kush mountain ranges (Armstrong 2010).

Connecting Global Priorities: Biodiversity and Human Health 233

 regions (e.g. longer growing seasons), mountain dwellers and lowland communities also face a
broad and unique range of climate-related health risks. These include water and food shortages,
increased risk of natural disasters and the expansion of water-related and vector-borne diseases
(Ebi et al. 2007; Ahmed and Suphachalasai 2014). Increased variability in precipitation patterns
(including variability in monsoon and more frequent extreme rainfall), coupled with increased risk
of extreme weather events and glacial ice melt are predicted to increase the risk of oods (carrying
rock, sediments and debris), landslides, threats to forest ecoregions including increased forest res
in some areas, soil erosion, and habitat and ecosystem disruption, damage to infrastructure and
property, injury and loss of human life (Ahmed and Suphachalasai 2014; Armstrong 2010; Ebi et
al. 2007). Of particular concern in the region are the potentially devastating impacts on mountain
dwellers and lowland communities from glacial lake outburst oods, which have become more
frequent since the latter half of the twentieth century (WHO 2005; Armstrong 2010).

Addressing the threats posed or compounded by climate change demands the development of
integrated and holistic approaches for the management of mountain ecosystems that sustain the
ow of life-supporting services. This can be achieved with innovative adaptation solutions (including
ecosystem-based adaptation), such as sustaining highland wetland systems that provide water
regulation, other services and habitats for critical animal and plant species (including medicinal
plants), or new technologies such as drip irrigation systems (CBD 2012; Chettri 2011).

Ecosystem-based adaptation in fragile mountain ecosystems such as HKH can not only provide
co-bene ts at the global or national level but may also be integrated into regional policies to
jointly encourage climate change adaptation, biodiversity conservation and sustainable use, and
development at a landscape level (Sharma et al. 2010). In the HKH, holistic ecosystem-based
adaptation strategies that emphasize adaptation as an interdisciplinary issue have been advocated.
These interventions seek to achieve the sustainable management of the transboundary reserve
system through the application of landscape-based solutions to jointly reduce the vulnerabilities
of biodiversity and local communities to climate change and other drivers by restoring endemic
vegetation, developing connectivity between ecosystems, and monitoring large-scale changes to
increase the social and economic resilience of local populations (Chattra et al. 2009).

2.6 Climate change and urbanization dwellers worldwide. Most future population
growth will be in small- and medium-sized
The global urban transition provides challenges cities in low- and middle-income countries.
and opportunities for health at the intersection Urban health inequalities are well documented
of climate change and biodiversity. Currently, (WHO and UN-HABITAT 2010), and rapid,
urban populations are growing by more than unplanned urbanization threatens biodiversity
1 million people every week and, by 2030, it is and exacerbates public health challenges across
estimated that 2 in every 3 people will live in different levels of economic development. Climate
urban areas – a total of more than 6 billion urban change especially amplifies health risks among

²¹ For example, the reduced availability and quality of freshwater or changes in monsoon patterns can at once affect agricultural
production by decreasing crop yield, increasing water and food insecurity (particularly for those living at altitudes of 2500
m or higher) and lead to a rise in the prevalence of waterborne diseases such as diarrhoeal disease (Ebi et al. 2007). The
impacts on agriculture and food production can also be especially severe. For example, in Nepal, an estimated 64% of all
cultivated area is dependent on monsoon rainfall (Chaudhary and Aryal 2009).
²² Some species may even become extinct as a result of gradual habitat loss resulting from global warming, particularly in
mountain biota above the tree line, and in high latitude and high altitude biomes (Chaudhary and Aryal 2014; Chapin 2004).

234 Connecting Global Priorities: Biodiversity and Human Health

poor and vulnerable communities, including subnational levels (Puppim de Oliveira et al.
through inundation in low-lying cities and the 2010). Further multidisciplinary study of these
health risks from inadequate water supply, various intersections and greater collaboration
sanitation and housing. However, affluent urban across various scales of governance, including
areas also face new challenges. In addition to other local governance and communities, are a necessary
negative health impacts described throughout prerequisite to meeting these challenges (Reid
this volume, recent findings suggest that climate 2015). As the next section discusses, ecosystem-
change may contribute to an increased incidence based conservation and adaptation provide
in allergies, particularly in urban areas. important opportunities for communities to play
a central role in the development of strategies to
Climate change may alter the diversity, address climate change.
production, allergenicity, distribution and timing
of airborne allergens. These changes contribute
to the severity and prevalence of allergic disease 3. Ways forward
in humans. Increased CO2 and temperature
3.1 Ecosystem-based adaptation and
is altering seasonality and beginning to affect
ecosystem-based mitigation
the quantitative and/or qualitative aspects of
the three distinct plant-based contributions to Biodiversity conservation can support efforts
allergenic pollen: trees in the spring, grasses and to reduce the negative effects of climate change
weeds in the summer, and ragweed (Ambrosia through ecosystem-based approaches to mitigation
spp.) in the fall (autumn) (Ziska et al. 2015). For and adaptation.²³ Conserved or restored habitats
example, a recent study on changes in climate can remove CO2 from the atmosphere, thus helping
in the United States has found that rising to address climate change by storing carbon (for
temperatures, altered precipitation patterns, example, reducing emissions from deforestation
and increasing atmospheric CO2 are expected to and forest degradation). Mangroves are natural
contribute to increasing levels of some airborne sources of biodiverse food, fish, shells, fruits,
allergens, and associated increases in asthma fuel, medicines, and they act as natural bioshields
episodes and other allergic illnesses, compared that protect coastal lands and local communities
to a future without climate change (Neal et al. from the impacts of climate-related extreme
2015). Several prior studies using urban areas as weather events, and also contribute to carbon
proxies for both higher temperatures and CO2 also sequestration. Adaptation strategies to conserve
showed earlier flowering of pollen species, which intact mangrove ecosystems or to repopulate them
may lead to a longer total pollen season (Neil can thereby help attenuate potentially severe
and Wu 2006; George et al. 2007). Microclimatic impacts of climate change, including flooding
effects of urbanization have been associated with and storm surges, while contributing to climate
longer pollen seasons and earlier floral initiation mitigation efforts and saving human lives (Das
in European cities (Rodriguez-Rajo et al. 2010). and Vincent 2009).
As climate change, biodiversity loss and other
pressures combine to pose new challenges, they Many successful examples of ecosystem-based
also present new opportunities for positive approaches are beginning to emerge.²⁴ Ecosystem-
development to protecting biodiversity, health based adaptation (EBA) activities can include:
and well-being, including in urban areas and at establishing diverse agroforestry systems to

²³ Ecosystem-based adaptation (EBA) integrates the use of biodiversity and ecosystem services into an overall climate change
adaptation strategy, while ecosystem-based mitigation (EBM) involves using ecosystems for their carbon storage and
sequestration abilities, by creating, restoring and sustainably managing ecosystems as a climate mitigation strategy.
²⁴ For example, the forest rehabilitation project in Krkonoše and Sumaya National Parks in the Czech Republic is one of several
examples of the implementation of ecosystem-based adaptation strategies and the challenges they have encountered (see
Naumann et al. 2011; Dowald and Osti 2011).

Connecting Global Priorities: Biodiversity and Human Health 235

 cope with increased risk from climate change;²⁵ these strategies through mainstreaming and
sustainable management of upland wetlands diversification across sectors (Reid 2015).
and floodplains for maintenance of water flow
and quality; conserving agrobiodiversity to
4. Conclusion
provide specific gene pools for crop and livestock
adaptation to climate change; maintaining or A range of local (e.g. invasive species) and global (e.g.
restoring mangroves or other coastal wetlands long-range pollution) stressors can make natural
to reduce coastal flooding and erosion; and adaptation more difficult in the face of accelerating
conservation and restoration of forests to climate change. In the absence of robust climate
stabilize land slopes and regulate water flows mitigation and adaptation strategies, the rate and
(Munang et al. 2013). EBA and ecosystem-based extent of anthropogenic activity contributing to
mitigation (EBM) strategies and approaches can climatic changes will continue to affect biodiversity,
additionally be highly cost–effective options that constrain the capacity of ecosystems to deliver
provide a range of social, economic and cultural essential services, and affect human health both
co-benefits while proactively responding to the directly and in combination with other drivers and
adverse impacts of climate change, safeguarding pressures. These include land-use change, pollution,
biodiversity and contributing to the livelihoods of population growth, urbanization and globalization
local communities (CBD 2009; Doswald and Osti (Campbell et al. 2009; Parmesan and Martens
2011; Goulden et al. 2009). 2009). These demand the adoption of a broad range
of multilevel sustainable-use and conservation
In Central and South America, there are practices (e.g. strengthening protected area
several examples of EBM strategies that networks; ensuring adaptive management through
support the establishment of protected areas, monitoring and evaluation). The full involvement
conservation agreements and community of communities and policy-makers alike is a key
resource management. Resilient crop varieties, determinant of their success (Martínez et al.
climate forecasts and integrated management 2012). Additionally, climate change adaptation
of water resources are also being adopted in the and mitigation strategies cannot be dissociated
agricultural, aquaculture and silviculture sectors from health equity considerations, without which
(IPCC 2014d). Aqua–silviculture systems, which equity gaps are likely to increase with a resounding
integrate mangrove forestry with fish and crab impact on the social determinants of health for the
aquaculture ponds, are commonly used in South- poorest, most vulnerable communities (Costello
East Asia. These systems are more resilient to et al. 2009).
shocks and extreme events, and they also lead to
increased production due to improved ecosystem There is a reservoir of important indigenous
services. While climate change adaptation is traditional knowledge, which is an invaluable
becoming embedded in some planning processes, resource for climate change adaptation and
the implementation of responses remains variable biodiversity conservation in indigenous
and requires strengthening (IPCC 2014d). EBM populations, and increases the effectiveness
and EBA strategies that include communities as of adaptation planning strategies (Field et al.
a central component of planning, address the 2014; Bennett et al. 2014). Indicators of climate
governance and policy context within which they adaptation and resilience should also include
are developed, and build on interdisciplinary nutrition outcomes such as the Dietary Diversity
scientific inquiry, provide valuable opportunities at the Household level (HDDS), including
to address these challenges, and to scale up Women’s Dietary Diversity Score (WDDS) or the
new indicator Minimum Dietary Diversity for

²⁵ Forests provide a carbon reservoir as they contain about 60% of all carbon stored in terrestrial ecosystems (CIFOR 2007),
and they can serve as important buffers for climate adaptation strategies. As deforestation contributes a large proportion
of global carbon emissions, curbing deforestation and investing in reforestation activities are a critical adaptation strategy
(Chaudhary and Aryal 2009).

236 Connecting Global Priorities: Biodiversity and Human Health

Women (MDD-W), which has been suggested and integrative approaches to the analysis of
for consideration as one of the priority nutrition environmental change and health outcomes.
indicators for the post-2015 Sustainable In turn, these must draw not from an isolated
Development Goals (SDGs). analysis of health impacts but also draw on
historical and contemporary insights about the
Conserving natural terrestrial, freshwater and underlying “factors that have determined the
marine ecosystems and restoring degraded structure and distribution of biodiverse systems”
ecosystems (including their genetic and species (Hoberg and Brooks 2015). Holistic strategies for
diversity) are also essential for the overall goals climate change mitigation and adaptation, which
of both the CBD and the UNFCCC. The key role of jointly consider multiple objectives, including
ecosystems in the global carbon cycle, for climate biodiversity conservation and livelihoods, will
change adaptation, for the provision of a wide likely be more effective and sustainable than
range of ecosystem services essential to human stand-alone strategies that focus on any single
health and well-being, and for the broader goals of objective, such as carbon sequestration (Heller
sustainable development, including the MDGs and and Zavaleta 2009).
SDGs that will follow (Haines et al. 2012), make
an ecosystem approach indispensible. Since 2008, Looking ahead, global health leaders are now
WHO has also adopted a very active programme calling for a “planetary health” approach with
to guard human health from the impacts of strengthened focus on threats to human
climate change²⁶ and it recently hosted its first civilizations and, ultimately, human survival,
international conference on related health issues.²⁷ from disturbances in planetary systems (Horton
While somewhat buffered against environmental 2013; Lancet-Rockefeller Foundation Commission
changes by culture and technology, human health on Planetary Health 2015), and an ecosocial
is fundamentally dependent on the continuing understanding of health, which acknowledges
flow of ecosystem services (Corvalán et al. 2005). its ecological, economic and social foundations.
There is a pressing need to formally recognize
Among poor and vulnerable populations in key environmental limits and processes, and
particular, climate change is already affecting the thresholds that we must respect in order
health in myriad ways and, more generally, to maintain the sustainability of our planet
climate change presents increasing future health (CBD 2014; Rockström et al. 2009). The current
threats worldwide (McMichael et al. 2012). reliance on gross domestic product (GDP) as the
Climate change affects health through primary, primary indicator of success has led to perverse
secondary and tertiary mechanisms, including outcomes and has not delivered fair levels of well-
its impacts on biodiversity and ecosystem service being for society or individuals (Fleurbaey and
provision (Butler 2014a), adding urgency to the Blanchet 2013). Contraction and convergence
task of addressing other international health will bring potential health benefits (Stott 2006).
priorities (Haines et al. 2012). The recognition Accounting for benefits to health and well-being
that climate change mitigation strategies can in development decision-making can encourage
have substantial benefits for both health and transitions to more sustainable and equitable
biodiversity conservation presents policy options patterns of resource use and consumption and,
that are potentially both more cost–effective and at the same time, improve population health (Dora
socially attractive than are those that address these et al. 2014). These changes are essential to avoid
priorities independently (Haines et al. 2009). widespread and profound damage to ecosystems,
upon which human survival ultimately depends.
The magnitude and breadth of these impacts
will require large-scale cross-sectoral efforts

²⁶ World Health Assembly resolution 61.19: Climate change and health. Geneva: World Health Organization; 2008. Available
at: http://www.who.int/phe/news/wha/en/index.html.
²⁷ http://www.who.int/globalchange/mediacentre/events/climate-health-conference/en/

Connecting Global Priorities: Biodiversity and Human Health 237

 14. Increasing resilience and disaster
risk reduction: the value of biodiversity
and ecosystem approaches to resistance,
UNDP BANGLADESH / FLICKR

resilience and relief

1. Introduction (epidemics, pest infestations). Combining these
elements, anthropogenic activities – such as road
Increasing evidence suggests that the frequency, construction, deforestation and mining – can
nature and scale of (at least certain types of) cause or exacerbate natural disasters. The impact of
natural disasters is changing: more mid- and these infrastructures, and ecosystem disturbance
small-sized disasters are now occurring more more broadly, may also pose immediate health
often, while increasing urbanization and the threat risks, by contributing to disease emergence or food
of climate change place more focus on the future insecurity, or increasing vulnerability to mental
social, economic, environmental and public health health issues, for example.¹ These are referred to as
impacts of natural disaster events (ADW 2012; “socionatural hazards”, whereby human activities
Guha-Sapir et al. 2013; Smith et al. 2014; Adger overexploit or degrade environmental resources,
et al. 2014). Three of the top 10 risks in terms increasing the magnitude of disasters and/or the
of impact over the next 10 years are identified as frequency with which they occur.
environmental risks – water crises, the failure of
climate change adaptation and loss of biological Disaster situations are associated with significant
diversity (Global Risks Perception Survey 2014). challenges for public health. The most immediate
threat to health may be posed by the disaster
The United Nations International Strategy for event itself; for example, geophysical and extreme
Disaster Reduction (UNISDR) defines a “disaster” weather events can cause significant physical
as a serious disruption of the functioning of a and mental trauma and loss of life (Guha Sapir
community or a society, involving widespread et al. 2014; Du et al. 2010; Wisner et al. 2008),
human, material, economic or environmental while epidemics are by their nature primarily a
losses and impacts, which exceeds the ability of public health concern. Furthermore, disasters
the affected community or society to cope using can exacerbate other public health risk factors,
its own resources (UNISDR 2009). Disaster by altering the natural and physical environment,
events can be natural or anthropogenic in origin, affecting critical infrastructure (e.g. associated with
or be triggered by a combination of these factors. clean water and sanitation or primary health care),
Human-induced disasters can include conflict and and changing human conditions (e.g. through
pollution events, while natural disasters may be
geophysical (earthquakes, landslides, avalanches, ¹ For example, the impact of dams can significantly
volcanic eruptions), climatic (hurricane, tsunami, contribute to the emergence and spread of schistosomiasis,
flooding, drought, storm surge) or biological as described in the chapter on water quality.

238 Connecting Global Priorities: Biodiversity and Human Health

displacement, injury, or loss of social and family events. More small- and medium-sized disasters
support). In some circumstances, this can lead to are also occurring now and the cumulative effects
an increased risk of infectious disease outbreaks of these on the assets – including biodiversity –
(Watson et al. 2007; Kouadio et al. 2012). People and livelihoods of vulnerable populations may,
affected by disasters – either through direct impact in the long term, have the same effects as high-
or perhaps indirectly through loss of employment magnitude events. Understanding the nature of
or social disruption – are often vulnerable to potential disasters is being increasingly recognized
psychological stress and related health conditions, as necessary for informed decision-making.
including depression, anxiety and post-traumatic Biodiversity – particularly its role in underpinning
stress disorder (Neria et al. 2008). Where disaster ecosystem services – can play a crucial role in
events impact on food production systems or disaster risk management before, during and
otherwise reduce the availability of basic foods, after an event by fostering resistance, building
those affected may also be at risk for nutritional resilience and assisting recovery. Expanding on the
deficit (Weingärtner 2005; UN SCN 2002). The need for more integrative approaches discussed
health burden of disasters is likely to increase as throughout this volume, such as the ecosystem,
a result of climate change (Sena et al. 2014; Kein Ecohealth, or One Health approach, this chapter
2008). describes an ecosystem-based approach to disaster
risk reduction (discussed in detail below) and
Recognition of the widespread ecological and examines the ways in which ecosystem services
humanitarian impacts associated with human- can support the ability of communities to manage
induced disasters, including the aftermaths of disaster risk in an integrated and sustainable
conflict and land-use change, has highlighted the manner. The three sections that follow expose the
need for sustainable multistakeholder solutions heterogeneity of disaster events and the responses
(Hanson 2011; Guha-Sapir and D’aoust 2011; of ecosystems to such events, drawing upon an
Leaning and Guha-Sapir 2013; Promper et al. ecosystem-based approach, with support from a
2014). number of relevant case studies.

The changing nature of disasters is likely to result

in greater loss of life, considerable economic costs,
1.1 Overview: resistance, resilience
reduced livelihood opportunities and significant – and recovery
possibly lasting – damage to critical ecosystems In the academic literature related to disaster
such as watersheds or coastal wetlands. However, management, the terms “resistance” and
while disasters can have a detrimental impact on “resilience” are often used interchangeably,
biodiversity and may even result in the collapse although there are some important distinctions
of essential ecosystem services, diverse and well- between them (Green 2008). While resistance
managed environments can help reduce disaster refers to the ability of a system to avoid having
risks and enhance community resilience to both a disaster impact in the first instance, disaster
natural and anthropogenic events. resilience pertains to the ability of a system to
mitigate, recover from, or adjust to, a disaster.
Urban expansion and infrastructure development, Resistance can therefore be thought of as a form of
increasing population pressures, unsustainable proactive resilience, denoting capacity to anticipate
agricultural intensification and climate change, all a disaster and act on this before it can materialize.
of which can be significant drivers of biodiversity
loss and ill-health, are increasing disaster risks “Recovery” pertains to the restoration (and
for many communities. Rapid-onset, previously improvement, where appropriate) of facilities,
infrequent, high-impact disasters, for example, infrastructure and livelihoods in disaster-affected
are now considered the norm, and many locations communities after an event has occurred, often
and communities are experiencing greater including rehabilitation and reconstruction
susceptibility to repeated and prolonged disaster (UNISDR 2009). For a holistic and sustainable

Connecting Global Priorities: Biodiversity and Human Health 239

 disaster response, these activities should 2. Biodiversity and disaster
be integrated with development initiatives, risk reduction: prevention and
combining tangible restoration projects with
capacity building, awareness-raising and policy
mitigation
formulation (WCPT 2014). This section outlines the integral role of
biodiversity in disaster management, with
The identification of standards and metrics for a specific focus on its ability to eliminate or
measuring disaster resilience is one of the many lessen the impacts of certain events. Well-
challenges faced by policy-makers. This concept managed and healthy ecosystems represent
has been examined by a broad range of research an opportunity to reduce disaster risk, which
perspectives. Expanding on the key concepts eschews a total reliance on physical engineering
described above, this chapter adopts a temporal structures, promoting integrated use of certain
perspective, examining the role of biodiversity ecosystems with physical infrastructure, offering
and well-managed ecosystems in disaster risk a sustainable and cost–effective way to reduce
reduction, and exploring the benefits these can disaster exposure, magnitude and frequency. By
offer before, during and after disaster events. conserving and restoring ecosystems, sustainable
This perspective has been adopted because – as natural resource management has the potential to
described throughout this volume – the impacts make a significant contribution to the prevention
of disasters on complex ecosystems and health and mitigation of disasters, addressing existing
can vary considerably through space and time. and emerging risks to foster resistance and build
A socioecological dimension has also received resilience. At the same time, such an approach
considerable attention and it is worth noting that goes a long way towards ensuring that certain
both resilience and vulnerability are also influenced natural resources, including food and medicinal
by social characteristics (see, for example, Cutter et products – both known and not yet discovered –
al. 2008). In coupled socioecological systems, the are potentially available for use by communities
same drivers can result in both social (including who depend on these as a traditional form of
health) and environmental inequities (e.g. Bunch livelihood and food security.
2011). Considering these dimensions is, therefore,
critical to improving public health outcomes The World Risk Report (2012) conceptualizes
and reversing the drivers of negative ecosystem risk as an outcome of the interaction between
change. Section two describes the potential of the likelihood a disaster and the vulnerability
ecosystem-based approaches to prevent disasters of societies, with vulnerability comprising the
in their entirety, or to mitigate their effects should abilities and capacities of people or systems to
this not be possible. Section three adopts a slightly cope with and adapt to the negative impacts of
different approach and examines the complexity disaster events, including health impacts. Thus,
of the links between biodiversity and disasters, risk is defined as a product of disaster exposure and
emphasizing the reciprocity of this relationship. the susceptibility, coping capacities and adaptive
While ecosystems can foster resistance, buffer the capacities of a population. These population
effects of disasters and assist with response and features are determined by the interplay of a
recovery, disasters can cause significant ecosystem range of physical, sociocultural, economic, political
degradation and biodiversity loss, which may and environmental factors in a specific context,
catalyse or exacerbate the risks of further events. indicating the complexity of “risk” as a concept
This is illustrated by the case study on refugees and its perpetual (trans)formation (ADW 2012).
and internally displaced persons (IDPs) described
in section 3. Disaster risk reduction (DRR) is a systematic
approach to identifying, assessing and reducing
the risks of disaster events. Strategies aim to
reduce the likelihood of disaster events, minimize
vulnerabilities and prevent, mitigate and/or

240 Connecting Global Priorities: Biodiversity and Human Health

 enhance preparedness towards the adverse to support the ability of communities to reduce
impacts of disasters (UNISDR 2004). and adapt to risk in an integrated and sustainable
manner. It has been described as one of the few
Conventionally, attempts at DRR have focused approaches that can impact all elements of the
on the protection of people and infrastructure disaster risk equation: reducing exposure and
through zoning and/or using “hard” engineering vulnerabilities, and increasing the resilience of
solutions, such as dams, levees and sea walls. exposed communities and their assets (PEDRR
As described in the chapter on water, these 2013).
infrastructures are often expensive to build and
operate, can generate unforeseen environmental Ecosystem engineering solutions – based on
and social consequences and – in many ecosystem services that use natural and/or
cases – have fallen short in the performance of managed ecosystems – comprise an integral
their protective duties (ProAct 2008; Badola and component of ecosystem-based strategies and have
Hussain 2005; Sudmeier-Rieux and Ash 2009). In become increasingly popular, particularly since the
light of this realization – and the changing nature 2004 Indian ocean tsunami (ProAct 2008). This
of disaster events described above – a search for disaster, in particular, highlighted the potential
alternative means of reducing disaster risk has protective capacities of coastal forests and brought
opened opportunities for increased attention to mangrove rehabilitation and conservation to the
ecosystem-based management approaches. forefront of the environmental agenda in South-
East Asia (Giri et al. 2008). At the global scale,
The ecosystem-based approach to DRR recognizes an increasing number of United Nations (UN)
and seeks to investigate and use the potential of agencies and international nongovernmental
biodiversity and ecosystem goods and services organizations (INGOs) have since expanded their
UNDP BANGLADESH / FLICKR

Connecting Global Priorities: Biodiversity and Human Health 241

 interest in ecosystem-based approaches to DRR 2.1 Disaster prevention: the role of
and plan to further integrate these into their biodiversity in reducing the likelihood
core activities in recognition of the “increasing of disaster events
importance of ecosystem management in adapting
Disaster prevention expresses the concept of and
and responding to climate change impacts and
intention to completely avoid potential adverse
associated disaster risks” (UNEP 2009; World
impacts through action taken in advance (UNISDR
Bank 2009).
2009). It is closely related to the concept of disaster
In the international policy arena, the Hyogo resistance, which suggests the ability of a system to
Framework for Action (HFA) (2005–2015) also evade the onset of a disaster and its impacts, and
acknowledges the role of healthy ecosystems to continue to function at close to normal capacity
and sustainable environmental management in and capability.
reducing disaster risks. Under its fourth Priority
Prevention has only recently become a permanent
for Action – “reduce the underlying risk factors”
feature of modern disaster management
– activities include the “appropriate management
frameworks – accompanying a general shift from
of fragile ecosystems” and “the sustainable use
reactive to proactive disaster responses. Examples
and management of ecosystems... to reduce risks
include the construction of dams or embankments
and vulnerabilities”. Unfortunately, efforts at
that reduce flood risks, and land-use regulations
ecosystem management for DRR have been largely
that prohibit settlement in high-risk zones. In
made on an ad-hoc basis, and a mid-term review of
terms of EbA for disaster prevention, ecosystems
the HFA determined that Priority Four has made
can also deliver benefits. For example, properly
the least progress of the five Priorities for Action
sited wetlands can reduce flood risks through
(UNEP 2009b; van Eeden 2013; PEDRR 2013).
water flow regulation, while certain mixtures of
This is illustrative of a general difficulty vegetation cover can – according to the specific site
encountered in the context of disaster location and characteristics – help act as a form of
management strategies, whereby there is often a ecological engineering, stabilizing steep slopes and
disconnect between the intentions of government preventing or reducing the scale of avalanches, soil
authorities, humanitarian and relief organizations, erosion and gulley formation.
donors and civil society, and the emergence of
Although preventive measures are designed to
practical and appropriate interventions in the
provide permanent protection from disasters,
field. Opportunities to adopt ecosystem-based
it must be recognized that not all disasters can
adaptation (EbA) measures have not been taken
be prevented and, in many cases, their complete
and laudable de jure proclamations extolling the
circumvention is unavoidable. Obviously, where a
benefits of biodiversity and ecosystem services for
disaster may not always be prevented then once
sustainable DRR have not been translated into de
it occurs its impacts need to be mitigated. In
facto actions, with concomitant implications for
the event of a tsunami or volcanic eruption, for
human security. EbA strategies that have been
example, disaster risk should be mitigated to the
implemented have often been prone to failure, due
greatest extent possible.
typically to an absence of local participation, various
financial and technical impediments, and the
recurrent underutilization of scientific knowledge 2.2 Disaster mitigation: the role of
(Quarto 2012; Kathiresan 2008). Notwithstanding biodiversity during a disaster event
these challenges, a number of successful EbA DRR “Mitigation” describes the alleviation or limitation
experiences in recent years attest to the potential of of the adverse impacts of disasters. These impacts
this approach to contribute to disaster prevention often cannot be prevented fully, but their scale or
and mitigation, helping to build the resistance and severity can be substantially lessened by various
resilience of human systems to existing, emerging strategies and actions (UNISDR 2009).
and evolving risks.

242 Connecting Global Priorities: Biodiversity and Human Health

 Case study: The use of vegetation in slope stabilization

In China, arti cial, human-made structures have traditionally been employed to protect communities
and infrastructure from shallow landslides, but these have short lifespans and have in many instances
caused considerable disruption to ecosystems. Ecological engineering involves “the design of
sustainable ecosystems that integrate human society with its natural environment for the bene t of
both” (Stokes et al. 2014). The use of plants as ecological engineers represents a more cost–e ective
and enduring option to combine with civil engineering approaches, with the potential of being self-
sustaining, increasing in e cacy over time, enhancing local biodiversity, and providing a plethora of
ecosystem services that can help address various drivers of livelihood vulnerability.

Several studies have shown that the establishment of certain types of vegetation cover signi cantly
reduces shallow landslides and erosion on steep slopes (>35°) due to the ability of root systems
to modify the biophysical, mechanical and hydrological properties of soil (Stokes et al. 2010;
Reubens et al. 2007; Fattet et al. 2011; Ghestem et al. 2011; Mao et al. 2014). To be e ective,
however, ecological engineering techniques require that the mechanical, chemical and architectural
traits of plant root systems be determined on a site-speci c basis to determine optimum species
combinations and planting con gurations for rehabilitating, protecting and stabilizing degraded
slopes (Stokes et al. 2014).

Certain species are traditionally favoured in slope stabilization – such as vetiver grass in China (Ke
et al. 2003), but monocultures can be a high-risk venture, thus favouring a mixture of di erent plant
functional types for slope stabilization, for example (Stokes et al., 2014; Fattet et al., 2011; Pohl et
al. 2009; Reubens et al. 2007). Polyculture plantations provide a range of root systems for optimum
soil stability. They also foster a heterogeneous environment for enhanced biodiversity and overall
ecosystem functioning, as well as supporting opportunities for income generation and a number of
other socioeconomic co-bene ts (Gouzerh et al. 2013; Shi and Li 1999; Post and Kwon 2000; Cavaillé
et al. 2013).

While ecological engineering usually does not incorporate, but can enhance the e ciency of, human-
made structures, another key distinction between these approaches relates to their e ectiveness
over time and space. From the rst moment of hard engineering installation, no erosion should occur;
however, this ecological engineering relies largely on plant growth, leaving a window of susceptibility
during the early years of restoration of a site when plants are too small to fully contribute to soil
stability (Stokes et al. 2004; 2008).

Mitigation measures encompass, for example, common mitigation efforts, while early warning
engineering techniques, improved environmental systems may be established and building design
policies and educational campaigns, and can be standards integrated into policy at the national
implemented at a range of scales. At the household level.
level, awareness-raising schemes can encourage
an avoidance of unnecessary risks through Mitigation is linked to the concept of disaster
encouraging the preparation of emergency kits or resilience, which describes the ability of a
the procurement of personal insurance. At a larger system, community or society to resist, absorb,
scale, the instalment of gas shut-off valves for accommodate and recover from the effects of a
earthquake events or the construction of houses hazard in a timely and efficient manner, including
on stilts to reduce flooding damage also comprise through the preservation and restoration of its

Connecting Global Priorities: Biodiversity and Human Health 243

 essential basic structures and functions (UNISDR sea level rise. As mentioned above, these diverse
2009). However, resilience does not necessarily ecosystems have also proven able to mitigate the
entail an ability to maintain or return to an impacts of storm surges and tsunamis, enhancing
exact pre-disaster state and a vital component of the resilience of communities along tropical and
many resilient systems is their capacity to adapt subtropical shorelines (Huxham et al. 2010;
to changing conditions. Mangrove forests, for McIvor et al. 2013; Jayasurya 2007).
example, migrate inland, if able, in response to

Case study: Building coastal resilience – bamboo wave barriers in Thailand

ŝI Ʋnd the sea level becoming higher and higher each year. Storms are more frequent and unpredictable.
If the situation continues, we may have nowhere to live.” — Kanit Sookdang

An innovative mangrove restoration project in southern Thailand has used ecological engineering to
mitigate the impacts of coastal storms and erosion. Klong Prasong is a shing village located on Klang
Island in the Krabi river estuary along Thailand s Andaman sea coast. For many years, powerful waves,
strong winds and rising sea levels threatened the village and its inhabitants, eroding the shoreline,
damaging infrastructure and properties, and forcing villagers to relocate to higher land. Local
shermen report that waves have eroded the coastal area by more than 1 km and Kanit Sookdang, a
54-year-old villager from Klong Prasong, has been forced to move house ve times in the past three
decades due to coastal erosion (Sarnsamak 2014; BP 2014).

Representing socionatural disasters, the storms and coastal erosion experienced in Klong Prasong
can be attributed to a complex interplay of natural and anthropogenic factors, including the monsoon
climate, intensive shrimp cultivation and the e ects of climate change. This multifaceted risk
pro le is further complicated by the increasing frequency and severity of coastal erosion and storm
conditions over the past few years, an intensi cation which demonstrates the dynamic nature of
disaster events over time and calls for a new approach to disaster management on Klang Island.

Observing the ine ectiveness of a concrete barrier wall constructed in 2003 – which, despite being
raised in height, failed to protect communities and actually augmented sediment loss and the e ects
of coastal ooding – a community-initiated demonstration project under Raks Thai Foundation s
“Building Coastal Resilience to Reduce Climate Change Impacts in Thailand and Indonesia (BCRCC)”
initiative adopted a true EbA. It constructed a bamboo wave barrier in an attempt to address coastal
erosion and facilitate the re-establishment of mangrove forests (Enright and Nakornchai 2014; Raks
Thai 2014).

It is anticipated that the bamboo wall will reduce wave energy, mitigate erosion and foster the
accumulation of sediment on its landward side in which mangroves can be planted. The structure –
made from bamboo sourced locally in Krabi province – is expected to last approximately seven
years, su cient time to enable mangroves to form a natural bioshield. The dense network of trunks,
branches and aerial roots of mangroves help shelter coastlines from strong winds and generate
a high drag force, which attenuates waves and dissipates their energy across the intertidal zone
(McIvor et al. 2012; Alongi 2008; Feagin et al. 2010; Giri et al. 2008). Mangroves have, in a number of
instances, been observed to signi cantly reduce the impacts of storm events on coastal communities,
reducing economic damages, mitigating biodiversity losses and saving lives (Das and Crépin 2013;
Quartel et al. 2007; Kathiresan and Rajendran 2005; Badola and Hussain 2005).

244 Connecting Global Priorities: Biodiversity and Human Health

 While community members and visitors in Klong Prasong will be directly involved in the planting
process – planting locally raised seedlings helps to build stewardship, awareness and support for
the project – the bamboo barrier will also facilitate natural regeneration, trapping oating mangrove
propagules to yield a forest with a high level of biodiversity. It is widely accepted that multispecies
systems have greater ecological resilience than monospeci c forest stands, and are thus more capable
of mitigating natural disasters. Heterogeneous forests also provide a greater range of opportunities
for livelihood diversi cation, demonstrating that ecological restoration, DRR and socioeconomic
development are mutually reinforcing (MAP 2012; ayakody et al. 2012; Vickers et al. 2012).

In addition to enhancing the resilience of coastal communities to disasters, mangrove forests

generate other bene ts by ltering water, absorbing CO2 and providing a breeding habitat for aquatic
animals (Enright and Kaewmahanin 2012; Sudtongkong and Webb 2008; Barraclough and Finger-
Stich 1996). Accordingly, it is hoped that the re-establishment of mangrove forests along the coast
of Klong Prasong will restore local biodiversity and ecosystem functioning for livelihood support,
improved local food security and enhanced community health and well-being.

Although budget restrictions meant that only a single-layer bamboo barrier was constructed under
the BCRCC project, the demonstration of this innovative approach to disaster management convinced
the Krabi Provincial Administrative O ce to build a more substantial, 500 m long double-layer
bamboo barrier, supported with government investments of 1 750 000 Baht (US 55 000). This
illustrates a new commitment by the government to ecosystem-based DRR approaches (Enright and
Nakornchai 2014).

While it is too early to evaluate the long-term impacts of these bamboo wave barriers, a number
of successes have already become apparent. Only eight months after the bamboo was rst put in
place – in une 2013 – assessments found that 15 cm of sediment had accumulated behind the
structure, with a clearly visible di erence in soil strata height between the seaward and landward
sides. Planted Avicennia marina seedlings had a survival rate of 80–90%, compared with rates of
just 10% when the same species was planted in front of the concrete wall. Signi cant increases
have also been recorded in the biodiversity and population sizes of aquatic species, particularly
molluscs: Musculus senhousia, Donex scortum and Meretrix sp. Local people can now expect to collect
at least 3 kg of Donex scortum each during every collection session – a few hours during the low tide
when the mud ats are exposed – which they had been unable to do in the recent past (Enright and
Nakornchai 2014).

This innovative approach to disaster resilience has also had a positive impact on the mental health
and well-being of community members in Klong Prasong. Village residents reported that they used
to sleep uneasily with the sound of strong waves hitting the concrete wall and a constant fear that
seawater would ood their homes. The construction of the bamboo barrier has increased their sense
of security and allows them to sleep peacefully in the knowledge that they are better protected.

Sources: Enright and Nakornchai 2014; Raks Thai 2014

The above case study demonstrates best practice ecosystems off the coast of Klong Prasong has built
in the use of an EbA for the mitigation of disaster the resilience of coastal communities, restored
risk. The construction of bamboo barriers local biodiversity, and supported the revival of
and concomitant regeneration of mangrove

Connecting Global Priorities: Biodiversity and Human Health 245

 a number of livelihood opportunities for a more 14.9 million people became internally displaced
prosperous present and sustainable future. due to natural disasters, the majority of them
across Asia (UNHCR 2014). Current predictions
Together, the case studies in this section regarding climate change as well as recurrent civil
demonstrate the ways in which well-managed conflicts and cases of political unrest will likely
ecosystems are able to prevent or mitigate the lead to further displacements in the future, forcing
impacts of natural disasters, contributing to DRR people into marginal lands, and urban and peri-
by building resilience to diminish the effects of urban settlements.
exposure, or fostering resistance to avert an event
altogether. They also show that – through the This section describes the complexity of the
rehabilitation and conservation of ecosystems and relationship between displaced populations and
a concomitant enhancement of biodiversity – EbAs biodiversity, which can be seen as simultaneously
afford a range of environmental and socioeconomic symbiotic and destructive. An exploration of the
benefits, which address multiple drivers of dependence of refugees and IDPs on ecosystem
vulnerability, as well as improve the ability of goods and services – during a crisis, in its
communities to avoid, withstand and recover from immediate aftermath and during the longer-term
the impacts of disaster (ProAct 2008). Finally, EbA post-disaster phase – is followed by an examination
measures have been seen to provide a dynamic, of the impacts that humanitarian operations can
adaptable and innovative disaster management have in terms of the overexploitation and rapid
response, which is vital in a world of emerging and degradation of natural resources, exposing an
continually evolving disaster risks (van Slobbe et ironic situation in which those resources upon
al. 2013). which communities may be most reliant are the
ones being degraded or destroyed.
6SHFLƩFFRQVLGHUDWLRQVIRU Although displaced populations are sometimes
internally displaced persons and blamed for causing environmental degradation
refugeesƹ in the areas where they are forced to settle, it
is extremely difficult to distinguish refugee/
Disaster events – whether driven by anthropogenic
IDP impacts from other processes of ecosystem
or natural factors, or a combination of both – are
decline. As such, the contribution of these groups
a major cause of population displacement, either
to biodiversity loss is sometimes overstated, while
within or across national borders. In 2011, some
the important role they can play in ecosystem
conservation and restoration can be understated
² The 1951 Refugee Convention defines a refugee as
someone who “owing to a well-founded fear of being or overlooked.
persecuted for reasons of race, religion, nationality,
membership of a particular social group or political opinion,
3.1 Refugees/IDPs rely on biodiversity/
is outside the country of his nationality” (UNHCR 2014).
Notably, this definition excludes environmental drivers of
ecosystem goods and services
population displacement and refugees may also be forced The survival and longer-term well-being of refugees
to migrate due to natural disasters although, in many cases,
and IDPs – in addition to host communities living
environmental disruptions result in internal migration
rather than relocation to another country (Hyndman
within the vicinity of camps – is often dependent
2009). Unlike refugees, internally displaced persons on particular natural resources, and the availability
(IDPs) have not crossed an international border and and accessibility of certain ecosystem goods and
remain within their home countries, retaining the rights services. In the short term, these may provide
and protection afforded by citizenship under both human immediate assistance for displaced populations
rights and international humanitarian law. The taxonomic
at the onset of a crisis, during the event and in
distinction of these groups serves to mask a number of
shared characteristics, as well as concealing considerable
its direct aftermath. Supporting the realization
internal heterogeneity in terms of backgrounds and of basic needs, for example, building materials
experiences. As such, the term “displaced populations” is for rudimentary shelters are typically sourced
used here to denote both refugees and IDPs (Oucho 2007).

246 Connecting Global Priorities: Biodiversity and Human Health

from local forests, while wild foods and natural – and represent two of the most commonly
medicines may be collected for direct consumption adopted natural resource-based livelihood
or sale. This was observed in 1994, when intense activities in camp settings. Unfortunately, these
ethnic fighting in Rwanda drove an estimated activities place considerable additional pressure on
600 000 refugees into an area surrounding already stressed ecological systems and have led a
Tanzania’s Burigi National Park. In addition to the number of host governments to adopt measures
serious habitat destruction caused by widespread to reduce further environmental degradation, such
tree cutting, the high demand for food that as the implementation of encampment policies
accompanied the arrival of the refugees caused (e.g. Kenya and Tanzania) (UNHCR 2002; 2014b).
wildlife in the park to decline sharply. According to In most instances, however, policies restricting the
a report by TRAFFIC (Jambiya et al. 2007), large movement of displaced populations are poorly
mammal populations declined by 60% between enforced and have failed to conserve natural
1994 and 1997, at the peak of the refugee influx, resources. They have also encouraged the uptake of
and some wildlife populations were reduced to negative coping strategies (such as illicit resource
less than 10% of their former numbers. Buffalo gathering and sale of food rations), inhibited self-
(Synceros caffer) numbers fell from about 2670 to reliance and fostered dependency (Lyytinen 2009;
just 44, the roan antelope (Hippotragus equinus) Ahlsten et al. 2005).
and zebra (Equus quagga) populations declined
from 466 to 15, and 6552 to 606, respectively, More sustainable income-generating opportunities
and the Lichtenstein’s hartebeest (Sigmoceros could incorporate environmental conservation
lichtensteinii) vanished completely. and restoration, and several experiences have
demonstrated the benefits of directly involving
In the longer term, biodiversity can support a range displaced populations in schemes to protect,
of livelihood activities. Displaced populations enhance and sustainably utilize biodiversity and
have been known to utilize wild resources in ecosystem goods and services in and around camp
opportunistic ways – for example, through settings (Lyytinen 2009).
charcoal making and the trading of bushmeat
and firewood – demonstrating a more complex While it is clear that displaced populations draw
relationship than simple passive dependency. upon a range of ecosystem goods and services to
Such activities are often driven by numerous satisfy immediate survival needs and to support
factors, including mounting population pressures, long-term health and well-being, self-reliance
a lack of employment and income-generation and livelihood security, these groups – as well as
opportunities, ineffective law enforcement, food humanitarian efforts to assist them – typically
insecurity and the inability of humanitarian present a dual threat to biodiversity and public
assistance to accommodate dietary and culinary health.
needs and customs (Jambiya et al. 2007). While
resource-based livelihoods have helped displaced 3.2 Humanitarian operations can pose
communities to enhance their resilience to disaster dual threats to biodiversity and human
risks and eschew a dependence on external well-being
organizations, caution must be exercised as the
extraction of certain natural resources can quickly Environmental degradation is inevitable in
wreak havoc on ecosystems if not appropriately refugee/IDP situations. Displaced populations
managed and monitored, as the example from and associated humanitarian operations –
Burigi National Park above illustrates. which are in some instances poorly planned and
coordinated – place considerable pressure on
The collection and sale of firewood and production ecosystem goods and services. Deforestation for
of charcoal are among the few options for income shelter construction and fuelwood, the extraction
generation available to refugees and IDPs – who are and pollution of groundwater and livestock
typically denied the right to formal employment grazing are among the most extensive ecological

Connecting Global Priorities: Biodiversity and Human Health 247

 Case study: Rwandan refugees in Gihembe National Park

In Rwanda s Gihembe camp, agricultural activities have fostered economic self-reliance for refugees
who cultivate mushrooms to enrich their diets and generate income. With support from the American
Refugee Committee (ARC), an association of 50 women living with HIV/AIDS has been established and
supported to pursue commercial agriculture. The women have received extensive training on a range
of topics – including association ethics, marketing, basic accountancy and business development
– and encouraged to employ sustainable land management techniques for the conservation of
ecological resources, minimizing soil and water erosion through terrace construction, trench digging
and the planting of 780 agro-forestry trees (ARC 2014).

In seven months, 3700 kg of mushrooms have been harvested, with 3000 kg sold to camp residents,
host community members and a local mushroom farm company (at around 1000 Rwandan francs
US 2 per kg) and the remaining 700 kg divided between the members of the association for
domestic consumption (Gonzalez 2006).

In addition to providing nutritional bene ts, this project has encouraged money management and a
culture of saving has begun to develop among the women. The association account contains over 1.5
million Rwandan francs (US 2200), a third of which is shared as pro t among members and stored in
xed deposit accounts to accrue interest (ARC 2014). This resource-based income-generating project
has also contributed to ghting the stigma surrounding HIV in the camp. Refugees and members of
the host community who purchase the mushrooms have been made aware that those living with this
disease are still able to work productively and contribute to life in Gihembe, reducing prejudice and
enhancing the quality of life for all those with HIV (ARC 2014).

The agricultural activities in Gihembe refugee camp demonstrate that well-managed ecosystems
are capable of providing a direct source of livelihoods for displaced populations. With active
participation and capacity building, the refugees were able to help themselves, utilizing locally
available natural resources to rebuild and improve their lives in a digni ed and sustainable manner
(UNHCR 2014).

threats engendered by the sudden arrival of some degree on the goods and services provided
large numbers of people. This results in the loss by local ecosystems), but will also impact members
of indigenous plant and animal species and a of host communities.³ The establishment of a
substantial decline in biodiversity (Oucho 2007). refugee/IDP camp and the subsequent influx of
With time, ecosystem degradation may spread thousands of people (potentially from different
beyond the immediate confines of a camp, where ethnic and cultural backgrounds) change the
other disaster response activities might be under environment of host communities in both
way. In north-east Kenya’s Dadaab refugee camp, positive and negative ways. In most cases, initial
for example, the deforestation radius around the kindness gives way to hostility as biodiversity is
camp increased from 5–10 km to 70 km between diminished and resource scarcities arise, inciting
1990 and 2010 (Gitau 2011). tension between the newcomers and host
community members, which can result in conflict
Any additional stress to existing environmental
degradation will not only have significant
implications for displaced populations (whose ³ Host communities comprise the local, regional and
national political and socioeconomic structures within
livelihoods and well-being are likely to depend to
which refugees live (UNHCR 2014).

248 Connecting Global Priorities: Biodiversity and Human Health

 Case study: Pressure on water resources: Syrian refugees in Jordan

ordan is one of the world s most arid countries but, since 2011, potential threats to water and food
security have been exacerbated by the arrival of over 600 000 Syrian refugees. This population in ux
has accelerated groundwater depletion and caused water tables to drop precipitously, increasing
salinization and rendering what little water remains less safe for human consumption.

ordanian households use an estimated 80 L of water per day on average, but communities in which
refugee camps have been established have seen the average supply drop below 30 L per day, with
accompanying declines in sanitation and a rise in disease incidence. As the quality and quantity of
limited water reserves continues to deteriorate, attention has turned towards demand and the poor
water conservation habits of Syrians, who are unaccustomed to living in a water-scarce environment
and are thus prone to wasting water.

Future e orts at water management must be implemented with long-term sustainability in mind in
order to preserve natural resources, support their restoration and maximize public health bene ts.
A holistic approach incorporating water demand management could also include the promotion of
simple and culturally appropriate conservation practices at the household level in order to reduce
water consumption and facilitate the possibility of groundwater replenishment.

Source: Mercy Corps 2014

(UfS 2013). The case studies below illustrate the non-refugee affected areas. Refugees rarely felled
myriad impacts displaced populations can have on trees for fuelwood alone – collecting most of it
biodiversity in their hosting areas. from the ground or as a byproduct of trees felled
for other purposes. The main environmental
While the examples given above illustrate change caused by refugees has been a decline in
the detrimental effects that humanitarian woody biomass.
operations can have on biodiversity, ecosystem
functioning and sustainability, this need not Localized instances of deforestation and
always be the case. It must be recognized that the considerable variation in the extent of woody
environments which displaced populations enter biomass depletion throughout Dedza and Ntcheu
are not necessarily pristine, but are usually already districts – even in areas subjected to similar human
undergoing various processes of degradation and pressures – demonstrate that the simple presence
decline. It is not uncommon, though, for these of refugee communities does not necessarily
groups to be blamed for declining conditions lead to biodiversity loss. This heterogeneity is an
that predate their arrival, particularly where outcome of interactions between various local
environmental baseline data and monitoring are environmental and sociocultural factors, such
unavailable (Oucho 2007). as the presence and enforcement of informal
regulations and established norms of resource
The presence of Mozambican refugees in Malawi’s access (Barnett 2003). The ways in which refugee
Dedza and Ntcheu districts, for example, had little livelihoods interact with the environment are
discernable impact on soil fertility or the depletion complex and diverse, with substantial differences
of many other natural resources (Barnett 2003). often discernable between, and within, specific
Although most Mozambicans made use of tree locations.
products – notably for fuelwood and construction
poles – little overall difference was noted in the Refugees and IDPs can make a significant
rates of forest coverage between refugee and contribution to conservation and rehabilitation

Connecting Global Priorities: Biodiversity and Human Health 249

 efforts. In a number of West African countries, from the fruit they eat and have started a small
for example, the presence of displaced populations nursery near the camp, while the running of a
led to the transfer of skills for sustainable sustainable agriculture and gardening course has
cultivation, plant management and resource- seen the creation of a community garden and
based entrepreneurship between these groups and the introduction of a permaculture project for
host communities, as well as fostering improved additional livelihood opportunities (Stapleton
environmental consciousness and awareness of 2014).
conservation issues (Oucho 2007).
This section has illustrated the complex nature of
As mentioned above, strategies to reduce the relationship between displaced populations,
environmental degradation and restore biodiversity, human security and well-being.
ecosystems offer the potential to provide much- While refugees and IDPs often rely directly on
needed income-generating opportunities in local ecosystem goods and services to meet a
refugee and IDP situations as well as enhance range of short- and long-term needs essential
biodiversity. A number of successful projects to their well-being, the ongoing degradation
demonstrate the benefits of collaborating with and overexploitation of natural resources in and
displaced populations as well as host communities around settlements threaten their ability to fulfil
for effective and contextually appropriate disaster basic daily requirements, partake in sustainable
responses, which reduce the risks associated with livelihood activities and achieve autonomy. There
further resource overexploitation and provide is therefore an urgent need for context-specific and
livelihood support for impacted groups. participatory interventions to reduce the demands
placed upon local ecosystem goods and services
In Dzaleka refugee camp in Malawi, refugees by displaced populations, and to foster the more
have established the “Education and Plantation sustainable extraction and utilization of natural
Strategies Association” (EPSA), which aims to resources. As this chapter has demonstrated,
boost local incomes through the planting of integrative, cross-sectoral approaches, such as the
6000 fruit trees both within and beyond the ecosystem approach, are required and may hold
camp’s limits. EPSA members grow seedlings the key to meeting these challenges.

UNDP BANGLADESH / FLICKR

250 Connecting Global Priorities: Biodiversity and Human Health

STEPHAN BACHENHEIMER / WORLD BANK PHOTO / FLICKR

15. Population, consumption

and the demand for resources;
STEPHAN BACHENHEIMER

pathways to sustainability
1. Introduction chapter 2, in particular). The linkages and the
origins and impacts of the drivers occur at various
The large-scale transformations of ecosystems to spatial scales and have a wide range of implications
meet the needs of growing human populations for human well-being.
have greatly accelerated over the past century,
transforming up to three quarters of the Earth’s This chapter looks at the underlying drivers of
biosphere, and diverting much of its biological change and their current trends. It examines
productivity for human use (Brown 2004; MEA possible future scenarios of change and their
2005; Ellis & Rammankutty 2008; Steffen et implications for biodiversity, human health, and
al 2015). The growing conversion of land for the interactions between them. Looking at future
agriculture, pasture, energy and commercial scenarios can be useful in elucidating potential
development has grown steadily alongside the synergies and tradeoffs in policies for health and
extraction of natural resources, the erosion of biodiversity conservation as well as in examining
landscapes and the unabated loss of the Earth’s the feasibility of meeting health and biodiversity
genetic and species diversity. objectives in the context of broader goals such as
the emerging sustainable development goals.
While many of these developments have benefitted
the lives of millions of people, improving their In recent decades, there has been an increased
access to food, shelter, energy, water and other interest in the implications of environmental
resources, they have often come at the expense change for human health (WHO 2005), often
of human health and the ecosystems upon which with a particular focus on the impacts of climate
we all rely for our survival (MEA 2005). They have change (See Chapter 13). More recently still,
also inevitably altered the nature and functions the importance of biodiversity and its decline
of many of our ecosystems, in turn shaping the for human well-being has been also highlighted
burdens of disease and inequity, across geopolitical (Cardinale et al 2012). In fact, threats to human
boundaries, from local to global scales (Robbins health from climate change and biodiversity
2011). change need to be addressed together, in a
coherent framework. This is necessary not only
The previous chapters describe the multitude of because of the interactions between the impacts
linkages between biodiversity and human health. on human health due to climate change and those
They also note that there are common drivers of due to biodiversity change (see Chapter 13), but
change to biodiversity and human health (see also because consideration needs to be given to

Connecting Global Priorities: Biodiversity and Human Health 251

 the potential tradeoffs and synergies in addressing maternal and child mortality persist, and access
these challenges. to family planning is lowest (UN DESA, 2015).

Addressing the direct and underlying drivers of Population growth may have some positive
biodiversity loss, poverty and ill health, under consequences. For example, some economists
present and future challenges also ultimately have argued that population growth induces
requires behavioural change by individuals, technological innovation, and provides
communities, organizations, industries, development benefits including agricultural
businesses and governments. Understanding, innovation and intensification (e.g. Boserup
awareness and appreciation of the diverse values 1965; Das Gupta 2011). However, population
of biodiversity, ecosystems and the services they expansion also places increased demand on
deliver underpin the combined willingness of healthcare systems and can greatly extenuate
millions of individuals to undertake purposeful pressures on natural resources. In particular, rapid
actions to address these drivers of change (see population growth in high fertility countries can
Chapter 16). Greater awareness of the values of create a range of economic, social, health and
biodiversity and ecosystem services also allows environmental challenges as well as for governance
individuals and governments to assess more (lagging investments in health, education, and
accurately the trade-offs of their policies and infrastructure). (Brown 20014; Bongaarts 2013;
decisions (CBD, 2013). Gerland et al 2015)

Among the most robust empirical findings in the

2. Current Trends and Alternatives literature on fertility transitions are that higher
rates of contraceptive use and female education are
1.1 Population pressures
associated with faster fertility decline (Hirschman
The increase in the exploitation of natural 1994; Sen 1999). These suggest that the projected
resources since the 20th century is in part rapid population growth could be moderated by
attributable to a rapid and sustained increase in greater investments in family planning programs
the global population.. The world population, now to satisfy the unmet need for contraception
7.2 billion people, will likely increase to between (Petersen et al 2013), as well as investments in
9.2 billion and 9.9 billion in 2050 and between 9.6 girls’ education.
billion and 12.3 billion in 2100 (80% probability
levels). Much of the increase is expected to happen Greater investment in the education of girls and
in Africa, in part due to higher fertility rates and women, improved access to and awareness of
a recent slowdown in the pace of fertility decline birth control and family planning would not only
(Gerland et al. 2014). While population is expected improve human health and well-being directly, it
to decline in some regions, notably in Europe, the would also help slow and reverse trends among
overall global population is expected to increase, countries with the highest projected growth
on average, by over 10% through to 2030, with the rates and concomitant pressures on ecosystems
largest population growth occurring in low and (Speidel et al. 2007; Sachs 2008; Population and
low-to-middle income countries (UN-DESA 2015). Environment 2007). However, in many cases,
The greatest population density has also been economic development and healthcare systems
projected to occur across areas that are already have not kept apace with the growing needs of
densely populated, including coastal regions in the fastest-growing populations, particularly
which communities are facing sea level rise and in low-income countries already struggling to
other threats posed by climate change (The Earth expand healthcare services to women and girls
Institute, 2006). The highest birth rates and largest (The Lancet 2012). In regions with the highest
increase in number of women of reproductive age projected population growth rates, notably Sub-
are expected in Africa, where the highest rates of Saharan Africa, there remains a largely unmet
need for access to contraception, a reduction of

252 Connecting Global Priorities: Biodiversity and Human Health

unwanted pregnancies, and the implementation According to a recent study 1.3 billion people
of family planning policies (Ezeh et al. 2012). worldwide do not have access to an electric grid
(IEA 2013), including over three quarters of the
population (or 600 million people) in Africa alone
3. Consumption – the demand for
(IEA 2011). This leads to an estimated 600 000
food and energy preventable yearly deaths from indoor fumes
Global demand for food, energy, water, shelter (UNEP 2015a). According to recent UN estimates,
and healthcare has risen dramatically over the the burning of fossil fuels for lighting accounts for
past 100 years, and this trend is likely to continue, 90 million tonnes of CO2 annually (UNEP 2015b),
leading to a new set of interrelated conservation, and an additional 270,000 tons of black carbon
public health and development challenges emitted as a result of kerosene lamps for lighting
(Eg.: Tillman and Clark 2014; Neff et al. 2011; (UNEP 2015a). Without adequate measures, the
Costello et al. 2009). The resulting pressures on number of people without access to an electric
natural ecosystems, including biodiversity loss, grid in Africa is projected to increase to 700 000
may not only lead to increased competition for by 2030, further extenuating pressures of climate
food, water, energy and land, affect economies, change on ecosystems and public health (UNEP
and bring us closer to “tipping points” (Leadley et 2015a). Thus efforts to reduce the use of emissions
al 2010, 2014; See also Chapter 2); they will also from fossil fuels must be accompanied with efforts
have major implications for global public health, to provide modern energy for all.
with disproportionate impacts on the poor and
vulnerable. A well-nourished global population expected
to exceed 9 billion by 2050 would require an
While population growth contributes to this estimated increase in food production ranging
increased demand, its impact is dwarfed by the between 70% and 100%, with a corresponding
effects of rising consumption by more prosperous rise in demand for processed foods, meat, dairy
members of the global community. The “ecological and fish as populations become more urbanized
footprint” provides an estimate of the per capita (Godfray et al. 2010; Royal Society of London
impact of consumption on biodiversity and 2009). Tilman and Clark (2014) note that dietary
ecological systems. It is measured in “global trends towards diets higher in refined sugars,
hectares”, with the earth able to support the refined fats, oils and meats, could lead to land
current population with just under two global clearing for agriculture and an 80% increase in
hectares per person. Most countries in Africa associated greenhouse gas emissions. Such dietary
have per capita footprints well within this value, trends would also increase the burden of disease
while the per capita footprint in Western Europe is from type II diabetes, coronary heart diseases
about and in North America about (Wackernagel, and other chronic non-communicable diseases.
1994; Global Footprint Network, 2015). However, as noted in Chapter 6, alternative diets
(such as the Mediterranean diet), if widely adopted,
With respect to greenhouse gas emissions, would greatly reduce impacts on biodiversity and
Satterthwaite (2009) notes that significant climate change and also improve health outcomes.
proportion of the world’s urban (and rural)
populations have consumption levels that are Water resources are projected to come
so low that they contribute little or nothing to under increased pressure, both as a result of
such emissions. He concludes: “if the lifetime increased pollution and demand. In developed
contribution to GHG emissions of a person added and developing countries alike, water stress
to the world’s population varies by a factor of more hinders economic growth and threatens food
than 1,000 depending on the circumstances into production systems and food security (Bogardi
which they are born and their life choices, it is et al. 2012; Viala 2008; Brown 2004). As the
misleading to see population growth as the driver chapter on freshwater indicates, this resource
of climate change”. is consumptively used for agriculture, as well as

Connecting Global Priorities: Biodiversity and Human Health 253

 domestic use, and, increasingly, by the industrial 4. Global trends to 2050 and
sector (Schwarzenbach et al. 2006), often to the pathways to sustainability
detriment of the most vulnerable populations who
have least access to health care, energy supplies Increasingly, scenarios of biodiversity change are
and other essential services. The freshwater crisis being used to explore (Pereira et al. 2010). Most
mirrors those related to other ecosystem services, scenarios indicate that biodiversity will continue
including the impact of sustained air pollution, to decline over the 21st century. However, the
and the decline of ‘soil based’ ecosystem services range of projected changes is much broader than
which affect crop yields and land productivity (see most studies suggest, partly because there are
e.g. Barrios 2007). major opportunities to intervene through better
policies (Pereira et al. 2010).
Addressing increased pressures on natural
resources, while also ensuring that the basic needs Recently, scenarios are also being used to explore
of all for food and modern energy are met, will alternative pathways for achieving globally
necessarily need to greater emphasis on equality agreed goals. For example PBL-the Netherlands
of access to and use of these natural resources. Assessment Agency has developed scenarios to
In fact, empirical research shows that more equal elucidate pathways to achieve the 2050 Vision of
societies are also associated with better health the Strategic Plan for Biodiversity 2011–2020,
outcomes, among other factors of human well- while also meeting other globally agreed goals
being (Wilkinson and Pickett 2009). (PBL 2012). These scenarios have been updated
and extended for GBO-4 (see box) (CBD 2014;
Kok, Alkemade et al (2014)).

Box 1: Global Biodiversity Outlook-4: A mid term assessment of progress towards

the Aichi Biodiversity Targets

In 2014, the Conference of the Parties to the Convention on Biological Diversity assessed progress
in the implementation of the Strategic Plan for Biodiversity 2011–2020 and its Aichi Biodiversity
Targets. (See Chapter I, box 1, on the basis of an evaluation contained in the fourth edition of the
Global Biodiversity Outlook (GBO-4; see also Tittensor et al 2014). The assessment shows that
signi cant progress towards meeting the components of the majority of the Aichi targets. However,
in most cases, this progress will not be su cient to achieve the targets set for 2020 and additional
action is required. The evaluation was based on multiple lines of evidence including global
assessments extrapolated trends in 55 indicators to 2020 and 2050, including response indicators
and indicators based on projections on the state of biodiversity. The conclusions are that while
responses to biodiversity loss are increasing (i.e countries are taking action), the large majority
of projections of the state of biodiversity to 2020 and 2050 show a signi cant deterioration and
pressures on biodiversity continue to increase.

The Outlook also identi es actions that would help to accelerate progress and concludes that
attaining most of the Aichi Biodiversity Targets will require implementation of a package of
actions typically including: legal and policy frameworks; socioeconomic incentives aligned to such
frameworks; public and stakeholder engagement; monitoring and enforcement. Coherence of policies
across sectors and the corresponding government ministries is necessary to deliver an e ective
package of actions.

254 Connecting Global Priorities: Biodiversity and Human Health

 Business-as-usual scenarios were contrasted Under ‘business as usual’ scenarios, pressures of
against plausible alternative scenarios to 2050 increased per-capita consumption and population
that would simultaneously curb biodiversity loss, growth, energy-intensive agricultural production
mitigate climate change, alleviate poverty and, that is both water and fossil fuel-intensive,
in so doing, contribute to maintaining essential unsustainable harvest, overconsumption,
ecosystem services that sustain human health (see indiscriminate and unregulated large-scale
Figure 1). exploitation of terrestrial and marine resources,
the erosion of genetic diversity; pervasive use of
Drawing on the findings of the Global Biodiversity pesticides, nitrogen fertilizers in food production
Outlook report described in the preceding section, systems and antibiotics, deforestation, illegal trade,
the scenarios in Figure 1 suggest that there are perverse economic incentives, marginalization
multiple plausible pathways to simultaneously and alienation of poor and vulnerable populations,
achieve the intersecting goals of maximizing and lack of awareness and education on the values
biodiversity, human health, and development of biodiversity and ecosystem services, will all
outcomes. Under these alternative scenarios, combine to exert untenable pressures on the
several biodiversity indicators reflecting the health biosphere and human populations alike. These
of our ecosystems and the life-supporting services pressures have been abundantly demonstrated
that they deliver would also be improved. (see throughout this volume. Fortunately, sustainable
Figure 2). alternatives have also been proposed and
evaluated.

ǡǤǢǰǭǠɻ

A B
.

Proportion in
Population Size Red List Index Species Richness Mean Species
Abundance
Proportion in averaged Values in Values in under Levels in averaged across the
across three response scenarios business as usual three responses scenarios

C D
, ,

, ,
tonnes per year

, ,
Gt CO equivalent

, ,

, ,

, ,

, ,

, ,

Current levels Food production in

Levels in under business as usual Food production in under business as usual

Levels in averaged across the response scenarios Food production in averaged across the three response scenarios

Connecting Global Priorities: Biodiversity and Human Health 255

 Common elements of the pathways identified in (see also chapters on agricultural biodiversity and
the preceding section include: nutrition);

• Reducing greenhouse gas emissions from • Reducing nutrient and pesticide pollution and
energy and industry (see also chapter on climate water use (see also chapters on freshwater and air
change); quality and impacts of pharmaceuticals on the
environment);
• Increasing agricultural productivity and
containing agricultural expansion to prevent • Promoting sustainable harvest, use and trade
further biodiversity loss and to avoid excessive of resources used for medicines (see also chapter
greenhouse gas emissions from conversion of on traditional medicine).
natural habitats (see also chapter on agricultural
biodiversity); As the scenarios in Figure 2 and practical
experience demonstrate, it is possible to achieve
• Restoring degraded land, protecting critical these goals while achieving food security,
habitats and resources (see also chapter on protecting biodiversity, curtailing climate change
freshwater); and attaining other goals for human development.

• Managing biodiversity in agricultural Improvements in energy production, transmission,

landscapes end-use and resource use efficiency, are needed,
along with a transition toward the decarbonization
• Reducing post harvest losses in agriculture and of energy supplies (Neff et al. 2011; Peñuelas
food waste by retailers and consumers as well as 2010; Horton 2007). As noted above, this must
moderating the increase in meat consumption be accompanied by improved access to modern
energy for all. Trends associated with globalized

ǡǤǢǰǭǠɼ

Target
%

Restore abandoned lands

Reduce nitrogen emmissions

%
Mitigate climate change
Baseline
Reduce nature fragmentation
Reduce infrastructure expansion

Expand protected areas

%
Reduce consumption and waste

Increase agricultural productivity

Global Decentralised Consumption

Technology Solutions Change
%

256 Connecting Global Priorities: Biodiversity and Human Health

industrial food production systems that are 5. Conclusion
highly reliant on petroleum for the development
As we embark toward a new sustainable
of pesticides, industrial agriculture, and the
development agenda in 2015, the identification
transportation of food, can only be reversed
and prioritization of strategies that jointly deliver
through the development of a robust package of
environmental (including biodiversity) and socio-
economic measures and policies which includes
economic (including health and development)
taxes on carbon and economic policies that
co-benefits will be both a key challenge and
mitigate the perverse impacts of energy policies
opportunity. Interlinked efforts to reduce the
(Horton 2007; Flora 2010). Pollan (2008) argues
ecological footprint of development, including
that reform of agricultural systems is needed to
stressors on biodiversity, energy demand,
meet health, food safety and energy challenges.
and health services provision, will be strategic
The important role of public health in enabling priorities.
a smooth transition toward more proactive,
Population growth, and prevailing consumption
sustainable and equitable social and policy
and production patterns are but part of these
transitions toward less fossil-fuel dependent
challenges, however: population movement, for
and resilient food production systems also
example, also causes environmental stress. Conflict
cannot be overstated (Neff et al. 2011). At the
prevention can help reduce the environmental
national level, these changes will need to be
impact of large congregations of displaced
complemented by increased equality in access
persons in refugee camps (Burkle 2010; see also
to and use of energy and other natural resources
chapter 14 in this volume). Similarly careful
and in access to healthcare and the provision of
environmental impact assessment can mitigate
related infrastructural innovation. For example,
the effect of communities displaced by large-scale
using indoor wood-burning stoves to increase food
development projects. The ecological footprint of
security (or for heating) is counterproductive as
city growth and urban pollution, and associated
exposure to indoor air pollution is responsible for
health impacts described in previous chapters
a staggering number of preventable deaths¹ and
can be limited by long-term urban planning. In
illnesses each year.
all these cases a mixture of conservation, public
Many of the routine human behaviours that health and social sciences, demography, and
together define the functioning of the global policy planning is needed to avoid the worst-case
economy will need to be altered if these goals scenarios wherein resource scarcity, ecosystem
are to be realized, requiring transformational degradation, biodiversity loss, human conflict,
change at the at the global, national and and climate change combine to present the
personal levels (Horton, 2007; Schwartz 2011). perfect storm of multiple, simultaneous, ongoing
Managing, and benefiting from, the interlinkages humanitarian crises. As further described in the
between biodiversity, ecosystems services and following chapter, the architects of coherent
human health increasingly demands broad-scale strategic policies integrating the biodiversity and
interventions that effectively and sustainably health nexus must harness these opportunities
influence human behaviour (Freya et al. 2010; and reflect these imperatives for the health and
Fulton et al. 2011; The Lancet 2015; see also well-being of present and future generations.
Chapter 16).

¹ Based on World Health Organization estimates, in 2012, approximately 4.3 million premature deaths were attributable to
household air pollution.

Connecting Global Priorities: Biodiversity and Human Health 257

 16. Integrating health and
biodiversity: strategies, tools
and further research
1. Introduction organized by the CBD Secretariat and the World
Health Organization through an ongoing series
The various interlinkages between biodiversity of workshops (Romanelli et al, 2014b; Box 1), the
and human health have been surveyed in the chapter outlines some objectives for such strategies
preceding chapters of this volume. Table 1 provides and provides a list of preliminary list of priority
a summary of the some of these interlinkages interventions at country level. The chapter then
and how the health sector might respond. As considers a number of tools and approaches that
has been demonstrated throughout this volume, could support such strategies, including common
biodiversity and ecosystems should be viewed metrics and approaches, methods and indicators
as part of the overall public health management for monitoring progress, and tools and approaches
landscape, and a vital resource for promoting for economic valuation. Building on the analysis in
public health and healthy lifestyles, in the Chapter 15, the chapter also considers approaches
prevention of disease – both communicable and for promoting behavioural change.
noncommunicable. (chapters 5, 6, 7, 8, 12). A
careful identification and assessment of common A discussion of needs for further research on the
drivers (chapter 2) includes land use change interlinkages between health and biodiversity is
(chapters 5, 7, 15), invasive species (chapters 3, also provided.
7), over-exploitation of resources (chapters 9,
11, 15), habitat loss (chapter 7), climate change Finally, the chapter discusses the integration of
(chapter 13), and the unintended consequences of biodiversity-health linkages in the post-2015
human activity (chapters 4, 5, 6, 7, 8, 9, 10), which sustainable development agenda.
can range from antibiotic resistance (chapter 5,
8, 9, 10), to endocrine disruption (chapter 3)
to air pollution (4) and climate change; each of
2. Strategic objectives for the
them further compounded by urbanizing and integration of biodiversity and
population pressures (chapters 5, 6, 15) human health
The linkages between biodiversity and human
This final chapter considers some possible
health presents a broad range of opportunities
strategies and tools for promoting the integration
for jointly protecting health and biodiversity,
of biodiversity and health objectives, especially in
and for advancing human well-being. More
policies, programmes and practices at national
specifically, health and biodiversity strategies
level. Building upon consultations among countries

258 Connecting Global Priorities: Biodiversity and Human Health

Table 1 : Some key biodiversity-health linkages

Biodiversity and Health Topic Health Sector Opportunity

Water Direct responsibility:
• Water quantity • Integrate ecosystem management considerations
into health policy
• Water quality
Indirect responsibility:
• Water supply
• Promote protection of ecosystems that supply
water and promote sustainable water use
Food and nutrition Direct responsibility:
• Species, varieties and breeds including • Recognize and promote dietary diversity, food
domesticated and wild components cultures and their contribution to good nutrition
• Diversity of diet • Recognize synergies between human health and
sustainable use of biodiversity (e.g. moderate
• Ecology of production systems
consumption of meat)
• Total demand on resources
Indirect responsibility:
• Sustainability of o take, harvesting and trade of
• Promote sustainable production harvesting and
species used for food
conservation of agrobiodiversity
• Changing status of species used for food
Diseases Direct responsibility:
• Disease source and regulation services • Integrate ecosystem management considerations
into health policy
• Ecosystem integrity and diversity
Indirect responsibility:
• Promote ecosystem integrity
Medicine Direct responsibility:
• Traditional medicines • Recognize contribution of genetic resources and
traditional knowledge to medicine
• Drug development (genetic resources and
traditional knowledge) Indirect responsibility:
• Chemical/ pharmaceutical accumulation in • Protect genetic resources and traditional
ecosystems knowledge
• Sustainability of o take/harvesting and trade of • Ensure bene t sharing
medicinal species
• Changing status of species used for medicine
Physical, mental and cultural dimensions of health Direct responsibility:
• Physical and mental health • Integrate value of nature into health policy
• Cultural/spiritual enrichment Indirect responsibility:
• Promote protection of values, species and
ecosystems
Adaptation to climate change Indirect responsibility:
• Ecosystem resilience • Promote ecosystem resilience and conservation of
genetic resources
• Genetic resources ( options for adaptation)
• Decrease vulnerability of people reliant on
• Shifting reliance to biodiversity with climate
important food and medicinal species which are
change shocks
likely to be impacted by climate change

Connecting Global Priorities: Biodiversity and Human Health 259

 could be developed with the aim of ensuring for the conservation and sustainable use of
that the biodiversity and health linkages are biodiversity as well as the fair and equitable
widely recognized, valued, and reflected in sharing of benefits;
national public health and biodiversity strategies,
and in the programs, plans, and strategies of (c) Managing ecosystems to reduce the risks of
other relevant sectors, with the involvement infectious diseases, including zoonotic and
of local communities. The implementation of vector-borne diseases, for example by avoiding
such strategies could be a joint responsibility ecosystem degradation, preventing invasive
of ministries of health, environment, and alien species, and limiting or controlling
other relevant ministries responsible for the human-wildlife contact;
implementation of environmental health
programs and national biodiversity strategies (d) Addressing drivers of environmental change
and action plans. Such strategies would need to (deforestation and other ecosystem loss and
be tailored to the needs and priorities of particular degradation and chemical pollution) that harm
countries. both biodiversity and human health, including
direct health impacts and those mediated by
Such strategies might include the following biodiversity loss;
objectives (this volume; Romanelli et al. 2014b):
(e) Promoting lifestyles that might contribute
(b) Promoting the health benefits provided by jointly to positive health and biodiversity
biodiversity for food security and nutrition, outcomes (e.g.: protecting traditional foods
water supply, and other ecosystem services, and food cultures, promoting dietary diversity,
pharmaceuticals and traditional medicines, etc.)
mental health and physical and cultural
well-being. In turn, this provides a rationale

Box 1: Workshops on the interlinkages between biodiversity and human health

In 2012, the WHO and the CBD embarked on an unprecedented joint collaborative endeavour aimed
at engaging the health and biodiversity sectors worldwide, with a particular focus on developing
countries, where concerted action is most urgently needed, in order to build capacity, and promote
action to jointly protect biodiversity and promote human health in the context of sustainable
development. The initial series of regional capacity-building workshops jointly convened by these
organizations, in collaboration with national and regional country partners, were held for the Americas
in Manaus, Brazil in September 2012 and for Africa in Maputo, Mozambique in April 2013. Country
representatives from the biodiversity and health sectors from a combined total of some 50 countries,
and a number of relevant organizations, regional experts and representatives of indigenous and local
communities, gathered to survey some of the critical linkages at the biodiversity-health nexus and
their relevance to the Strategic Plan and its Aichi Biodiversity Targets and to discuss the need to further
mainstream biodiversity in public health strategies and to incorporate public health considerations in
biodiversity strategies. Participants agreed upon an initial broad set of conclusions which have been
further revised and adapted in light of the issues identi ed throughout various chapters of this state of
knowledge review, in the broader context of the implementation of the Strategic Plan for Biodiversity
2011–2020 and the Post-2015 development agenda. These conclusions are re ected in sections 2
and 3 of this chapter as a broad framework for the integration of the biodiversity-health considerations
in local, national and regional strategies (see also Romanelli et al. 2014b) .

260 Connecting Global Priorities: Biodiversity and Human Health

(f) Addressing the unintended negative impacts outcomes cannot be overstated (PEDRR 2013).
of health interventions on biodiversity (e.g.: For example, the chapters on disaster risk reduction
antibiotic resistance, contamination from and climate change demonstrate the need for a
pharmaceuticals), incorporating ecosystem proactive approach to risk management by outlining
concerns into public health policies, and examples from a growing portfolio of ecosystem-
based adaptation and mitigation measures.
(g) Addressing the unintended negative impacts “Enhancing disaster preparedness for effective
of biodiversity interventions on health (e.g.: response” comprises the fourth priority under the
effect of protected areas or hunting bans on newly concluded Sendai Framework for Disaster
access to food, medicinal plants, etc.). Risk Reduction (2015–2030); well-managed
ecosystems and the myriad of services they can
Promoting and maximizing the health benefits provide will undoubtedly play an important role
provided by biodiversity for food security and in achieving this target and removing, or at least
nutrition, water supply, and other ecosystem reducing, the effects of natural disaster events
services, pharmaceuticals and traditional on human life. The health status of populations
medicines, mental health and physical and cultural exposed to extreme events is equally central to the
well-being provide a strong rationale for the overall success of the Sendai Framework, placing
conservation and sustainable use of biodiversity the health sector at the centre of prevention and
and the fair and equitable sharing of benefits. mitigation strategies. The call for additional public
Lifestyles (such as diets based on low-fat, diverse and private investment alone, which is the third
and nutritious foods), practices and actions (such priority of the Sendai Framework, while essential,
as integrated land-use planning to maximize will not be sufficient to strengthen health systems
health benefits) will require educating, engaging or improve health outcomes.
and mobilizing the public and the health sector
alike, including professional health associations as Monitoring, evaluating and forecasting progress
potential, powerful advocates for the sustainable toward the achievement of national, regional and
management of ecosystems. It will also require global targets at regular intervals against evidence-
mobilizing organizations and individuals who based indicators, including threshold values for
can articulate the linkage and the enormous value critical ecosystem services, such as the availability
proposition investments in sustainable ecosystem and access to food, water and medicines is critical
management provide to the social and economic as further discussed section 5 of this chapter.
health of communities.

In the sections that follow, some tools to achieve 3. Priority interventions for the
these outcomes and additional areas for further integration of biodiversity and
research are identified. These are not intended to be human health
comprehensive, but rather illustrative of the need
Romanelli and others (2014b) identified as of
to further strengthen interdisciplinary knowledge
priority interventions to facilitate the integration
at the intersection of biodiversity and health.
of biodiversity-health linkages in relevant polices,
A key element is adopting integrative approaches programmes and practices at the national level.
such as the “One Health” approach or other As they noted, the implementation of these
approaches that consider connections between interventions will be largely influenced by
human, animal, and plant diseases and promotes individual country institutional and financial
cross-disciplinary synergies for health and capacities, and shaped by competing demands
biodiversity (see section 4 of this chapter). In faced by health and environment agencies,
this context, the importance of preventive and with often limited resources. In that light, they
precautionary strategies for the management suggest that a pragmatic approach is needed,
of sustainable ecosystems to optimize health focusing first on those activities which require
little initial investment and which will gradually

Connecting Global Priorities: Biodiversity and Human Health 261

 develop partnerships and capacities to deliver (e) Disseminate and share lessons learned,
more efficiently on the shared agendas of health knowledge, and national experiences related to
and conservation actors. These would likely biodiversity–health linkages among countries and
include improved cross-sectoral collaboration with international, national, and local partners
mechanisms, the sharing of existing data and to facilitate the development of tools aimed
information, and the pooling of resources, where at integrating biodiversity in health strategies
feasible. This would help to move beyond the and reflecting public health considerations in
confines of habitual institutional silos in which biodiversity strategies
health and environmental policies are often
developed, so interventions are no longer viewed (f) Carry out awareness raising activities and
as added burdens imposed by one sector on the develop education programs on the importance
other, but rather as important opportunities of health–biodiversity linkages at various levels,
for collaboration toward improved health and so as to enhance support for policies and their
conservation outcomes. implementation

The priority interventions identified include. (g) Promote further applied research on
biodiversity–health linkages to identify country-
(a) Encourage the development of new and existing specific health risks, notably through disease
tools such as environmental impact assessments, organisms or ill-health triggers that result from
strategic environmental assessments, risk ecosystem degradation and address local health
assessments, and health impact assessments that adaptation needs and solutions. Research should
consider health-biodiversity linkages to manage also contribute to strengthening inter-country
future risks and safeguard ecosystem functioning and regional research collaboration to address
while ensuring that social costs, including health knowledge gaps and to incorporate social and
impacts, associated with new measures and cultural perspectives as well as traditional and
strategies do not outweigh potential benefits religious values that serve to promote health and
protect biodiversity
(b) Strengthen core national capacities that enable
health systems to prepare for and effectively (h) Facilitate implementation of integrated
respond to public health threats resulting from essential public health and biodiversity-related
ecosystem degradation and undertake cooperative interventions for the management of both
actions toward capacity-building that promote short and long-term health risks resulting from
the training of professionals in the health and biodiversity loss and unsustainable practices;
biodiversity sectors, as well as indigenous and
local communities (i) Facilitate implementation of integrated
environment and health surveillance to support
(c) Promote research, development, and timely and evidence-based decisions for the
cooperation in traditional medicine in compliance effective identification and management of short
with national priorities and international and long-term risks to human health posed by
legal instruments, including those concerning ecosystem degradation and biodiversity loss by
traditional knowledge and the rights of indigenous forecasting and preventing increases in related
peoples, as appropriate ill-health and disease

(d) Promote the exchange of information, (j) Strengthen and operationalize the health
experiences, and best practices to support the components of disaster-risk reduction plans
development of national and regional biodiversity to prevent casualties resulting from the health
and health strategies, and integrated tools of consequences of ecosystem degradation
territorial planning
(k) Strengthen international and regional
partnerships, joint work programs, and

262 Connecting Global Priorities: Biodiversity and Human Health

intersectoral collaboration on biodiversity–health Complementary conservation approaches include
linkages. landscape and seascape change modelling,
vulnerability and adaptation assessments,
integrated health and environmental assessments
4. Towards the development of
and ecosystem service analyses. Valuation
common metrics and approaches approaches, when being used in conjunction with,
The integration of biodiversity and human or being based on, tools and methods that further
health can be facilitated by the use of common contribute to our understanding of ecosystem
metrics and frameworks. Conventional measures functioning and human health linkages, can also
of health are often too limited in focus to be useful tools for the assessment of benefits and
adequately encompass the multiple health trade-offs of different policy scenarios.
benefits from biodiversity (Corvalan et al. 2005).
Notwithstanding the broad WHO definition of Measuring the health effects of ecosystem change
health described in Chapter 2 of this volume, by considering established “exposure” threshold
traditional measures of health, such as disability values can help to highlight biodiversity-health-
adjusted life years (DALYs) and burden of disease, development linkages. Mechanisms linking
tend to have a more narrow focus on morbidity, ecosystem change to health effects are varied.
mortality, and disability, and fail to capture the For many sub-fields, exposure thresholds or
full breadth of the complex linkages between standards have been scientifically established that
biodiversity and health, including social and serve as trigger points for taking action to avoid
determinants and cultural underpinnings (E.g. or minimize disease or disability. For example,
Talbot and Verrinder 2009; see also the chapters air quality standards exist for particle pollution,
on mental health and traditional medicine in this WHO has established minimum quantities of per
volume). A more holistic approach is necessary. capita water required to meet basic needs, and
thresholds for food security define the quantity of
Examples of such tools on the human health food required to meet individual daily nutritional
side include environmental hazard or risk factor needs. Measuring the health effects of ecosystem
analyses, tools aimed at the identification (and change relative to established threshold values
reduction) of health disparities and inequities, highlights how such change constitutes exposure –
identifying environmental and socio-economic an important principle linking cause and disease
determinants of disease, and conducting or other health effects – and encourages action if
health impact assessments. Complementary thresholds are exceeded.
conservation approaches include landscape
and seascape change modelling, vulnerability Given the complexity and heterogeneity
and adaptation assessments, integrated health of the tools available to assess health and
and environmental assessments and ecosystem biodiversity linkages, complementary cross-
service analyses. Valuation approaches, when sectoral approaches require the development of
being used in conjunction with, or being based a common evidence base across the health and
on, tools and methods that further contribute to conservation sectors. These can extend from the
our understanding of ecosystem functioning and development of standardized measures in the
human health linkages, can also be useful tools integration of systematic assessment processes
for the assessment of benefits and trade-offs of (including environmental impact assessments,
different policy scenarios. Examples of such tools strategic environmental assessments, health
on the human health side include environmental impact assessments and risk or strategic
hazard or risk factor analyses, tools aimed at the assessments), to more systematic reviews of
identification (and reduction) of health disparities research findings, standardized data collection
and inequities, identifying environmental forms and computerized modelling programs,
and socio-economic determinants of disease, and the systemic consideration of multiple health
and conducting health impact assessments. impacts in policy evaluation and assessment. The

Connecting Global Priorities: Biodiversity and Human Health 263

 integration of these tools in the development of a and avoid the much greater damage and costs of
common framework should consider the health- disease outbreaks (see also chapter 7).
biodiversity linkages – including those described
throughout this volume  – to manage future Progress toward the development of a common
risks and safeguard ecosystem functioning while framework will thus require more systematic
ensuring that social costs, associated with new collaboration across disciplines and sectors, with
measures and strategies, do not outweigh potential greater attention being paid to “translating” the
benefits. The development of precautionary meaning of key metrics to increase their shared
policies and safe minimum standards that place a relevance for the health and biodiversity sectors.
value on ecosystem services to health, and make Similarly, frameworks provide a conceptual
positive use of linkages between biodiversity and structure to build on for research, demonstration
health is critical to this endeavour. These should projects, policy and other purposes. Embracing a
be considered prior to any analysis of trade-offs. common framework that aims to maximize the
health of ecosystems and humans both could
In practical terms, for example, policy-makers help the different disciplines and sectors work
and researchers could prioritize measures such more collaboratively. As introduced in Chapter 2
as integrated disease surveillance in wildlife, of this volume, the conceptual framework of the
livestock and human populations, as a cost- Intergovernmental science-policy Platform on
effective measure to promote early detection Biodiversity and Ecosystem Services (IPBES),
building upon that articulated in the Millennium

ǡǤǢǰǭǠɻ The IPBES Conceptual Framework

Source: Diaz et al 2015a.

264 Connecting Global Priorities: Biodiversity and Human Health

Ecosystem Assessment, is a framework that links 5: Keeping tabs: The need for
biodiversity to human well-being, considering also monitoring and accountability for
institutions and drivers of change (See Figure 1).
evidence-based indicators at the
Fig.1 In the central panel, boxes and arrows intersection of biodiversity and
denote the elements of nature and society that health
are at the main focus of the IPBES. In each of
Identifying ecosystems critical for the delivery
the boxes, the headlines in black are inclusive
of human health benefits and evaluating key
categories that should be intelligible and relevant
socio-economic variables that affect access to
to all stakeholders involved in IPBES and embrace
and delivery of associated goods and services to
the categories of western science (in green) and
communities, particularly vulnerable populations,
equivalent or similar categories according to
is an instrumental step towards the identification
other knowledge systems (in blue). The blue and
of appropriate policy measures and strategies.
green categories mentioned here are illustrative.
However, the ongoing objective evaluation of
Solid arrows in the main panel denote influence
those strategies once measures are in place, is
between elements; the dotted arrows denote links
equally essential.
that are acknowledged as important, but are not
the main focus of the Platform. The thick, coloured Monitoring, evaluating and forecasting progress
arrows below and to the right of the central toward the achievement of national, regional and
panel indicate that the interactions between global targets at regular intervals against evidence-
the elements change over time (horizontal based indicators, including threshold values for
bottom arrow) and occur at various scales in critical ecosystem services, such as the availability
space (vertical arrow). Interactions across scales, and access to food, water and medicines will
including cross-scale mismatches, occur often. The be essential to the effective implementation
vertical lines to the right of the spatial scale arrow of strategies. To be effective, monitoring and
indicate that, although IPBES assessments will evaluation will require considerable strengthening
be at the supranational – subregional to global – through more innovative and integrated
geographical scales (scope), they will in part build approaches. These could include, for example,
on properties and relationships acting at finer – the development of robust, cross-cutting
national and subnational  – scales (resolution, indicators that jointly address human health and
in the sense of minimum discernible unit). The environmental considerations (see, for example,
resolution line does not extend all the way to the Dora et al. 2014; Pelletier et al. 2014). Further
global level because, due to the heterogeneous guidance for the establishment of national
and spatially aggregated nature of biodiversity, development plans that simultaneously encourage
even the broadest global assessments will be cross-sectoral partnerships and stakeholder
most useful if they retain finer resolution. This engagement are also critical to strengthening and
figure is a simplified version of that adopted encouraging more innovative monitoring and
by the Second Plenary of IPBES; it retains all evaluation approaches.
its essential elements but some of the detailed
wording explaining each of the elements has Each of the elements identified above must
been eliminated within the boxes to improve be supported by the development of robust
readability. A full description of all elements and indicators. Many indicators used in biodiversity
linkages in the conceptual framework, together conservation and environmental management can
with examples, can be found in Diaz et al. (2015b). prove useful to health impact assessments, either
to help in the identification of contributing factors
to existing health problems, or areas where health
risks or opportunities may arise.

Connecting Global Priorities: Biodiversity and Human Health 265

 Drawing on the findings discussed throughout presented as complementary information, thus
this volume, these indicators may include contributing to the overall calculation.
parameters of water quality; the extent, quality
and distribution of important habitats; wildlife Valuation approaches linking ecosystem
population movements; animal and plant health functioning and health that support decisions
status; and various indicators of biodiversity loss. about resource allocation may appeal to a variety
Similarly, in some circumstances the indicators of stakeholders, including many of those in the
used by the health community (nutritional public health and conservation sectors. Many tools
status and availability, births, deaths, morbidity, for monetary valuation of ecosystem services have
occurrence of specific diseases, etc.) may help to been developed in recent decades (for a recent
bring specific ecological issues into focus or help review see e.g. Brouwer et al. 2013; for different
identify areas in which conservation measures approaches see also see also Gómez-Baggethun
need to be assessed, strengthened or revised. The et al. 2014; Nelson et al. 2009; Brauman et al.
same holds true for the development sector, since 2007; Costanza et al 2006; Nunes et al. 2001).
the delivery of ecosystem services are supported The Economics of Ecosystems and Biodiversity
by biodiversity. Inter-disciplinary partnerships (TEEB), a global multidisciplinary initiative that
to identify existing indicators which can be used seeks to mainstream the value of biodiversity
directly or modified to address cross-cutting issues and ecosystem services, has been particularly
are an important element of capacity building for successful in drawing attention to the global
the ecosystem approach, and help to promote economic benefits associated with biodiversity
co-operation. Examples of cross-cutting indicators conservation and the growing financial ecological
which might be considered are provided in Table 2 and human burden associated with its loss (http://
below. www.teebweb.org) (MacDonald and Corson 2012).

People rely on a range of ecosystem services to

6. Assessing the economic value sustain livelihoods, health, and well-being, of
of biodiversity and health: which only a subset can be reflected in economic
EHQHƩWVDQGOLPLWDWLRQV evaluations in monetary terms; still fewer can be
addressed through market-based instruments.
Providing estimated economic values for an
The Economics of Ecosystems and Biodiversity
ecosystem service can be useful for internalizing
(TEEB) follows a tiered approach in analyzing
that value and guiding decision-making and more
and structuring valuation, including: societal
integrated policy analysis. If used effectively, and
recognition of values; demonstration value in
in conjunction with other tools, some valuation
economic terms where possible; and in some cases,
approaches can help us reconsider our relationship
using market-based mechanisms to capture value.
with the natural environment, alerting us to the
The TEEB initiative calls for the internalization
consequences of our choices and behaviour for the
and assessment of values of biodiversity and
environment and human health. Translating the
ecosystem services where it can practically
value of natural resources and costs associated
and appropriately be carried out, based on the
with conservation into economic terms can
recognition that it is unacceptable “…to permit
promote more equitable, effective and efficient
the continued absence of value to seep further into
conservation practices, help to identify more
human consciousness and behaviour, as an effective
efficient means of delivering ecosystem services,
‘zero’ price, thus continuing the distortions that drive
identify more cost-effective alternatives, and
false trade-offs and the self-destructiveness that has
allow for a more thorough assessment of trade-
traditionally marked our relationship with nature”
offs (TEEB 2010). Significantly, some aspects of
(TEEB 2010:12).
ecosystem functioning such as ecological resilience
cannot be fully captured in quantitative valuations. The approach also acknowledges several of the
However, in most cases, economic values can be limitations, risks and complexities involved in

266 Connecting Global Priorities: Biodiversity and Human Health

Table 2: Examples of cross-cutting indicatorsƸ
Issue Cross-cutting indicators
Water and air quality • Biological/health hazards of source water from di erent sectors (e.g. agriculture; mining; energy
development)
• Chemical integrity of source water (e.g. pesticides, endocrine disrupting compounds, and harmful
algal blooms (cyanotoxins).
• Shifts in lychen species (as an indicator for air quality)
Food security, • Nutritional status (e.g. type and prevalence of nutrient de ciencies)
nutrition, and
• Food species diversity
noncommunicable
diseases • Status of unmanaged agrobiodiversity (e.g. pollinators, pests, predators)
• Time spent / distance travelled accessing foods
• Income and dietary intake from traditional foods, including wild foods
• Land used for producing traditional foods
• Prevalence of malnutrition / diet-related non-communicable disease
• Food yields from various resources (e.g. crops, sh/aquaculture, hunting)
• Outbreaks of food-borne disease
• Land use change (e.g. % area, pace of change, intensi cation)
• Use of agrobiodiversity in healthcare interventions (e.g. intervention type, species used)
Infectious diseases • Areas of intact habitat in high risk areas
• Status of wildlife populations (distribution, movement, abundance, diversity, conservation status)
• Outbreaks of zoonotic, water-borne, vector-borne and food-borne disease (frequency,
distribution, morbidity, mortality)
• Outbreaks of human / wildlife / livestock / plant disease
• Water availability, vulnerability and quality
• Land use change (e.g. % area, pace of change, intensi cation)
• Outbreaks of infectious human/wildlife/livestock disease
Medicinal resources • Use of biodiversity for primary medicinal resources (e.g. % of total medicinal use, % income
derived from sale of traditional medicines)
• Status of key species and related habitats
• indigenous population indicators – movements, density, births, morbidity and mortality
Disaster risk and • Areas of intact habitat in high risk areas
climate change
• Encroachment and degradation (e.g. wetland reclamation, deforestation, urban sprawl)
• Population density in high risk areas
• Dependence of population on local ecosystems for food / medicine / income (e.g. % of total
population, income derived from ecosystems etc)
• Area of land experiencing erosion, deforestation, drought, deserti cation
• Frequency and severity of disasters
• Population displaced by disasters, and degree / pace of return
• Prevalence of disease after disasters
• Land use change (% area, pace of change, intensi cation)
• Indicators of climate adaptation and mitigation measures implemented by other sectors on
biodiversity and human health

¹ Adapted from COHAB Initiative, unpublished.

Connecting Global Priorities: Biodiversity and Human Health 267

 economic valuation, covers different types of value and trade-offs. The development of frameworks of
appreciation, and includes various categories of this kind involve synthesizing the abundant but
response at the level of public policies, voluntary often scattered body of literature that analyses non-
mechanisms and markets (Box 1). monetary values of biodiversity, and articulating
it into ecosystem service concepts, methods, and
Capturing the full range of values associated classifications (Gómez-Baggethun and Muradian
with biodiversity loss, including socio-cultural 2015; Kelemen et al. 2014; Christie et al. 2012;
dimensions, requires that economic valuation tools Gimona and van der Horst 2007). TEEB is clearly
are complemented with non-monetary valuation a useful framework that has been put to widespread
methods and planning tools based on various (cross- use around the globe, but further strengthening of
sectoral) criteria that help to differentiate benefits the health dimensions of valuation are also needed.

Box 1: The TEEB approach

Recognizing Value: Recognizing value in ecosystems, landscapes, species and other aspects of
biodiversity is a feature of all human societies, and is sometimes su cient to ensure conservation
and sustainable use. This may be the case especially where the spiritual or cultural values of nature
are strong. For example, protected areas such as national parks have historically been established
in response to a sense of collective heritage or patrimony, a perception of shared cultural or social
value being placed on treasured landscapes, charismatic species or natural wonders. Protective
legislation or voluntary agreements can be appropriate responses where biodiversity values are
generally recognized and accepted. In such circumstances, monetary valuation of biodiversity and
ecosystem services may be unnecessary, or even counterproductive if it is seen as contrary to
cultural norms or fails to re ect a plurality of values.

Demonstrating Value: Demonstrating value in economic terms is sometimes useful for policymakers
and others, in reaching decisions that consider the full costs and bene ts of a proposed use of
an ecosystem, rather than only costs or values that enter markets in the form of private goods.
Economic valuations of natural areas are a case in point. Examples include calculating the costs and
bene ts of conserving the ecosystem services provided by wetlands in treating human wastes and
controlling oods, compared to the cost of providing the same services by building water treatment
facilities or concrete ood defences. Valuation is best applied for assessing the consequences of
changes resulting from alternative management options, rather than attempting to estimate the
total value of ecosystems. Most valuation studies do not assess the full range of ecosystem services
and not all biodiversity values can be reliably estimated using existing methods. The identi cation
of all signi cant changes in ecosystem services is a necessary rst step even if all of them are not
monetized.

Capturing Value: This nal tier involves the introduction of mechanisms that incorporate the values
of ecosystems into decision-making, through incentives and price signals. This can include payments
for ecosystem services, reforming environmentally harmful subsidies, introducing tax breaks for
conservation, or creating new markets for sustainably produced goods and ecosystem services. It
needs to come along with reinforcing rights over natural resources and liability for environmental
damage. The challenge for decision makers is to assess when market-based solutions to biodiversity
loss are likely to be culturally acceptable, as well as e ective, e cient and equitable.

Source: TEEB, 2010

268 Connecting Global Priorities: Biodiversity and Human Health

7. Shaping behaviour and iii) Addressing the significant gap in knowledge
engaging communities for on what works, how and why, in order to
develop evidence-based best practices that can
transformational change be scaled-up for sustainability.
Human behaviour is central to the biodiversity-
human health nexus: our actions, as producers Tackling these and other aspects of human
and consumers of energy, natural resources and behaviour change can have far-reaching
manufactured products, are prime determinants implications for poverty alleviation, human health
of both the ability to conserve biodiversity and and biodiversity conservation (Allegrante 2015;
to promote human health. Therefore, managing, Barrett et al. 2011). Each of these is relevant to
and benefiting from, the interlinkages between building a culture of health that is in line with social
biodiversity, ecosystems services and human and environmental objectives, including those
health increasingly demands broad-scale embedded in the Strategic Plan for Biodiversity
interventions that effectively and sustainably 2011–2020 and its Aichi biodiversity targets, and
influence human behaviour (Freya et al. 2010; the emerging sustainable development goals.
Fulton et al. 2011; The Lancet 2015).
Understanding the drivers of human behaviour
The social sciences can assist us to motivate requires moving beyond rational individualistic
choices consistent with health and biodiversity behaviour models in order to appreciate the
objectives and to develop new approaches through, complexities of daily life, social and economic
inter alia, better understanding of behavioural incentives for change, and actual processes of
change, production and consumption patterns, change (Hargreaves 2011; Pons-Vigués et al.
policy development, and the use of non-market 2014). Social, cultural and psychological factors
tools (CBD 2013a). Accordingly, the development interact in complex ways with broader economic,
of work on values, institutions and behaviour is political and environmental processes (Marmot et
needed (CBD 2013b; Duraiappah et al 2014).² It al. 2008; Waylen et al. 2010). Designing effective
has been argued that intervention efforts that also and sustainable behaviour change interventions
seek to modify the physical, social, political, and also demands that we account for the perceptions,
economic environments in which people live and needs, capacities, heterogeneity and constraints
make health and environment related decisions of communities. Engaging with human behaviour
can jointly deliver health, environmental and change also involves understanding complexity at
social benefits (e.g. Allegrande 2015 and references different scales, which requires multi-disciplinary
therein; Pons-Vigués et al. 2014).³ Core elements approaches. In addition to the need to further
to promote behaviour change on a global scale strengthen the scientific base of a broad range
include: of issues at the intersect of biodiversity and
health, there is also a need for policymakers
i) Understanding the drivers of human and practitioners to draw deeply from the social
behaviour and the role of micro- and macro- sciences (psychology, anthropology, sociology,
level processes (including political, social, political science and other fields) in order to
environmental and economic institutions and inform strategies (Glanz and Bishop 2010).
structures) in mediating positive change; Moreover, the traditional values of indigenous
and local communities can sometimes provide
ii) Recognizing that influencing human behaviour critical foundations for positive behaviour change;
can take many forms but that strategies should recognizing these values and working with these
be tailored to specific contexts and issues; and groups to develop more sustainable production

² UNEP/CBD/SBSTTA/17/INF/1
³ The effectiveness of such approaches in addressing ethical considerations or reducing health disparities has also been
questioned (Lieberman et al. 2013).

Connecting Global Priorities: Biodiversity and Human Health 269

 and consumption patterns is essential (Kuhnlein excludes sufficient recognition of related structural
et al. 2013).⁴ barriers (political, social and environmental) and
of efforts to address them (Lieberman et al. 2013;
In addition, the importance of behavioural change Khun and Manderson, 2007). Strategies for the
in the private and business sectors is also critical conservation and sustainable use of biodiversity,
to achieving truly sustainable development, as including through the CBD, commonly focus
many of the goals and targets at the biodiversity on promoting changes in awareness, with the
and human health nexus require encouraging the assumption that changes in these indicators will
private sector to adopt more sustainable practices precede behaviour change. Unfortunately, as noted
(e.g. supply chain management). by Verissimo (2013), this assumption is generally
wrong (McKenzie-Mohr et al. 2011). The same can
With reference to any particular set of objectives, be said of interventions in the health sector which
behaviour change includes efforts (such as often focus on “downstream” drivers of health
modifying institutional or social structures) (Freudenberg et al. 2015; WHO 2008; Marmot
to reduce behaviours that are negative to the et al. 2008; Freudenberg et al. 2015) rather than
objectives, promote behaviours that are positive, “upstream” drivers such as biodiversity loss (WHO
and increase structural determinants so as to 2012) and individual behaviour modification
foster “nurturing environments” (Biglan et al. strategies rather than modifying the social,
2012). Interventions can be very broadly divided political, economic and physical environments in
into top-down and bottom-up approaches. These which people live (Golden and Earp 2012; Pons-
can take many forms and make use of different Vigués et al. 2014).
strategies, ranging from media campaigns,
promoting the adoption of specific technologies, There are a variety of innovative techniques that
fostering compliance and/or community dialogue can be used to move beyond didactic methods in
on regulatory policies and legislative reforms, order to engage with community participation,
strengthening community action, building local skills development and the addressing of broader
resilience, and many others (Gaventa and Barrett social determinants (Trickett et al. 2011), such
2012). Whatever the approach, it is important that as developing or reformulating technologies
interventions be tailored to local, social, cultural, as agents of behaviour change (Newson et al.
economic, political and environmental contexts 2013), social marketing (McKenzie-Mohr et al.
in order that strategies consider local constraints, 2011), school-based programmes that combine
values and incentives for change (Wakefield et education and environmental interventions (De
al. 2010; Netto et al. 2010). However, it is not Bourdeaudhuij et al. 2011), and social mobilization
enough that behaviour change programmes be (Pretty et al. 2002). These examples show the
culturally-acceptable; they also need to be based need for interventions to engage in innovation,
on a compelling rationale for change (see Panker- embracing both complexity, and long-term
Brick et al. (2006) for malaria prevention; Moon visions of change, which in turn rely on sufficient
and Cocklin (2013) for biodiversity conservation; resource-mobilization.
Sunderlin (2006) for forest conservation; Lewis et
al. (2011) for sustainable agriculture; Newson et The health sector can provide useful experience
al. (2013) for nutrition; and Vaughan et al. (2013) in this regard. Social marketing has been widely
for safe drinking water). implemented in the health sector in countries
with promising results in addressing issues such
Many large-scale programmes for behavioural as obesity and smoking (French et al. 2009;
change are often poorly implemented and rely Shin et al. 2015; Gielen and Green 2015). Social
solely on passive information dissemination that marketing consists of a suite of research and

⁴ For example, Kuhnlein et al. (2013) discuss how the Ainu people in the Saru River region, Japan, approached behaviour
change. In chapter 14 of that same volume detailed approaches and methods for behaviour change among indigenous
peoples are also discussed.

270 Connecting Global Priorities: Biodiversity and Human Health

execution techniques; this is the application of c. What are the linkages between biodiversity
marketing concepts and techniques, informed (including biodiversity in the food production
by the psychology of persuasion and influence system), dietary diversity and health? Is there
to create, communicate and deliver values to a relationship between dietary biodiversity
influence behaviour and benefit the target and the composition and diversity of the
audience and society (Kotler & Lee 2011). It also human microbiome? What are good indicators
involves the development of non-traditional of dietary biodiversity? What are the linkages
partnerships. For example, as Shin and colleagues between biodiversity in environment, the
(2015) demonstrate, developing unique cross- human microbiome and health?
sectoral partnerships by combining health sector
information with point-of-purchase strategies d. Beyond microbial influences on the immune
can also encourage positive behaviours that system, what are the actual mechanisms by
jointly promote healthy foods and make them which exposure to biodiverse environments
more accessible, including among low-income influence health outcomes? What are the
populations which can, in turn, contribute to a implications for the design of buildings and
reduction in obesity rates. cities and access to “natural environments”?
What are the implications for the treatment of
some non-communicable diseases? What are
8. Research needs the cumulative health impacts of ecosystem
As the various chapters in this volume have alteration? Who stands to benefit?
demonstrated, scientific data and information
from multiple sources and disciplines are not only e. Beyond provisioning services, which
fundamental to our understanding of biodiversity- components of coastal and marine ecosystems
health linkages but to the identification of more lead to positive human health outcomes?
integrated public health, conservation and Does exposure to marine biodiversity have
development strategies. While this knowledge measurable health benefits?
is increasing rapidly, many data gaps persist and
much more sustained cross-disciplinary research f. How can biodiversity monitoring be better
is needed to evaluate the full-breadth of these integrated with or more accessible to the
complexities across geographical and temporal public health and conservation communities?
scales (for recent discussion on existing research
These and many other questions merit further
gaps see also, for example, Myers et al. 2013;
attention from the scientific community in
Sandifer et al. 2015).
order for science to more meaningfully inform
Further research is needed to elucidate some of policy and decision-making. Ensuring that this
the potential knowledge gaps on linkages between knowledge can also be accessed and shared by
biodiversity and human health. For example, key decision-makers and practitioners, including
questions include: among and between low- and middle-income
countries, is not only instrumental to their wide-
a. What are the relationships between scale implementation but to the operationalization
biodiversity, biodiversity change and infectious of our shared commitment to achieve sustainable
diseases? Specifically, what are the effects of development objectives (Sachs 2012).
species diversity, disturbance and human-
wildlife contacts? What are the best metrics The knowledge in question must not be confined
by which to measure exposure? to scientific data nor any single discipline, as
multiple sources of information are critical to
b. What role does functional diversity play? How understanding the direct threats to and underlying
might it modulate health outcomes? What are drivers of ill health and biodiversity loss. For
the implications for spatial planning? example, further research is needed to assess the
current proportion of species used for medicinal

Connecting Global Priorities: Biodiversity and Human Health 271

 and food purposes; qualitative data is also needed affecting food security and nutrition, the provision of and
to determine the proportion of this reliance on access to water and the health of the rural poor and of people
natural resources that is based on needs and that worldwide, including present and future generations…”
which is based on individual preferences. This (UN, The Future We Want, 2012).
research can in turn be critical to developing sound
strategies aimed at sustainable use, management The United Nations Conference on Sustainable
and trade of biological resources essential to Development (UNCSD, Rio+20), in its outcome
human health and well-being. document, “The future we want”, agreed to
establish a process to develop sustainable
Considering the regional heterogeneity of the development goals (SDGs) as a key part of the
disease burden, and the variation of interactions United Nations development agenda beyond
between variables at different scales, analyses of 2015. Human health, biodiversity and ecosystems
local burdens of disease (including the eventual were all prominently featured in the outcome
implementation of sustainable development goals document which devoted numerous paragraphs
and targets in the post-2015 period) should be to calls for a comprehensive framework for a
complemented by strategies that also take local healthy, sustainable and more equitable future
variability into account (Murray et al. 2012). (UN, 2012). The need to eradicate poverty and to
Findings from the natural sciences should be further mainstream sustainable development at
complemented by work from numerous other all levels was recognized from the outset as was
disciplines, including the social sciences. The “integrating economic, social and environmental
latter are especially relevant to behavioural aspects and recognizing their interlinkages, so
change discussed in the previous section. as to achieve sustainable development in all its
Analyses should also draw from local knowledge dimensions” (UN 2012: paragraph 3).
ensuring, insofar as possible, full and effective
participation of local and community-level The SDGs are intended to build upon the
stakeholders. This routinized participation will Millennium Development Goals (MDGs),
not only contribute to strengthening and/or which were an expression of the international
validating scientific knowledge, but also increase community’s commitment to global development,
opportunities for mutual learning, transparency, bringing social dimensions such as environment,
coherence and collaboration. By its very definition, poverty, hunger, disease, education, and gender
mainstreaming (biodiversity considerations) equity to the forefront of the global policy agenda.
implies that the integration of biodiversity in The MDGs and their associates 2015 targets were
relevant public and global health policies and largely successful in giving new prominence to
strategies will require the involvement of various global public health issues affecting poor and
stakeholders, at multiple scales. vulnerable populations (Sachs 2012; Smith and
Taylor 2013). The health-related MDGs have
contributed to reinvigorating several multilateral
9. Integrating biodiversity and health institutions (although global engagement
health into the sustainable could be much more effective and coordinated);
development agenda galvanized collective action in the fight against
HIV-AIDS, contributing to the expansion of
“We reaffirm the intrinsic value of biological diversity, as
coverage with antiretroviral drugs (despite a large –
well as the ecological, genetic, social, economic, scientific,
and ongoing- access gap); contributed to an overall
educational, cultural, recreational and aesthetic values
reduction of deaths from malaria, tuberculosis and
of biological diversity and its critical role in maintaining
some other infectious diseases; contributed to an
ecosystems that provide essential services, which are
increase in overall access to immunizations in
critical foundations for sustainable development and
developing countries and reduced child mortality
human well-being. We recognize the severity of the global
(Carlsson and Nordström, 2012). The MDG
loss of biodiversity and the degradation of ecosystems
framework included the biodiversity target to
and emphasize that these undermine global development,

272 Connecting Global Priorities: Biodiversity and Human Health

“reduce biodiversity loss, achieving, by 2010, a Indeed, the sustainable development framework
significant reduction in the rate of loss, 5 under must not only acknowledge the role of biodiversity
Goal 7 “ensuring environmental sustainability”. for its contribution to development, but also
The target originated from the “2010 biodiversity provide the enabling conditions for its conservation
target”, adopted, in 2002, by the Conference of the and sustainable use by promoting transformational
Parties to the Convention on Biological Diversity change in economies and societies. This not only
and also by the World Summit on Sustainable requires improving governance, considerably
Development, as part of the Johannesburg Plan strengthening institutional and cross-sectoral
of Implementation. collaboration at multiple scales, and coordinating
global responses, it also demands behavioural
While biodiversity and environmental change and building human capabilities through
sustainability more generally, were included in access to education and health care (CBD 2013b).
the MDG framework, in the implementation of
the framework, the importance of biodiversity for Within the SDG process, unique opportunities
the achievement of the other MDGs (including the to advance the parallel goals of improving health
high-profile goals on poverty, food, and health) was and other social dimensions of sustainable
not sufficiently recognized. Despite many actions development can be maximized by harnessing
in support of biodiversity, the 2010 biodiversity opportunities that deliver joint benefits, such
target was not fully met because the actions were as measures and policies at the intersection of
not taken on sufficient scale and because the nutrition, urban health, and noncommunicable
underlying drivers of loss were not addressed diseases (see chapter 6).
significantly. In the post-2015 development
agenda, biodiversity needs to be better integrated In line with the rationale and methods proposed
into broader development objectives (CBD 2013a). by Dora and colleagues (2014), progress toward
intersecting goals could be measured against
In line with the mandate from Rio+20, United a robust set of target indicators that evaluate
Nations General Assembly established an Open health-related-risks modulated by biodiversity-
Working Group on Sustainable Development related measures. For example, target indicators
Goals and tasked it to prepare a proposal for the could be developed to evaluate progress of actions
SDGs. The Group has proposed 17 goals (see taken based on sustainable food production and
Table 3). The SDGs are due to be finalized and agriculture polices (see chapter 5) that could not
adopted by the United Nations General Assembly only contribute to biodiversity protection and
in September 2015. ecosystem resilience but also improve human
nutrition (under SDG goal 2), and contribute to
While one of the proposed goals is focussed reducing the burden of noncommunicable diseases
specifically on human health (Table 3) others also (under SDG goal 3). The SDG framework should
address important and closely-related components additionally provide for the enabling conditions
of human well-being including the eradication of for human health and for the conservation
poverty, food security and nutrition, availability and sustainable use of biodiversity, and for the
of water and sanitation, and access to modern underlying drivers of biodiversity loss and ill health
energy. Biodiversity is related to each of these to be addressed (Chapter 2). This further implies
components and these intersections have been Goals for improved governance, and institutions,
demonstrated at length throughout this volume. at appropriate scales (from local to global), for
Biodiversity is addressed explicitly in two of the management of risks and the negotiation of
the proposed goals and in several sub-targets trade-offs among stakeholder groups, where they
including those related to food and water. The are necessary.
proposed goals also recognize the importance of
sustainable consumption and production, as well As national policies and strategies continue to
as the importance of gender equality and equity. develop, the ongoing evaluation of synergistic and

Connecting Global Priorities: Biodiversity and Human Health 273

 Table 3Ƽ: Summary of the sustainable development goals and targets proposed by the
open working group on sustainable development goals, and how biodiversity, and ele-
PHQWVRIWKH6WUDWHJLF3ODQIRU%LRGLYHUVLW\ŘDUHDGGUHVVHGE\WKHP

Biodiversity addressed in targets

The proposed sustainable development goals
(SDGs) Directly Indirectly
End poverty in all its forms everywhere Targets 1.4; 1.5; 1.a; 1.b
End hunger, achieve food security and improved Targets 2.4; 2.5 Targets 2.1; 2.3; 2.a; 2.b
nutrition, and promote sustainable agriculture
Ensure healthy lives and promote well-being for all Targets 3.3; 3.4; 3.8; 3.9; 3.b;
at all ages 3.d
Ensure inclusive and equitable quality education Targets 4.5; 4.7
and promote life-long learning opportunities for all
Achieve gender equality and empower all women Targets 5.1; 5.5; 5.a; 5.c
and girls
Ensure availability and sustainable management of Target 6.6 Targets 6.1; 6.3; 6.4; 6.5; 6.a,
water and sanitation for all 6.b
Ensure access to a ordable, reliable, sustainable, Target 7.a
and modern energy for all
Promote sustained, inclusive and sustainable Target 8.4 Targets 8.2; 8.3; 8.5; 8.9
economic growth, full and productive employment
and decent work for all
Build resilient infrastructure, promote inclusive and Targets 9.1; 9.4; 9.a; 9.b
sustainable industrialization and foster innovation
Reduce inequality within and among countries Targets 10.2–10.4; 10.a; 10.b
Make cities and human settlements inclusive, safe, Targets 11.4; 11.7; Targets 11.1; 11.3; 11.5;
resilient and sustainable 11.a 11.6; 11.b; 11.c
Ensure sustainable consumption and production Targets 12.2; 12.4; Targets 12.1; 12.5; 12.7;
patterns 12.8 12.a; 12.b
Take urgent action to combat climate change and its Targets 13.1–13.3; 13.a; 13.b
impacts
Conserve and sustainably use the oceans, seas and Targets 14.1–14.6; Targets 14.7; 14.a; 14.b
marine resources for sustainable development 14.c
Protect, restore and promote sustainable use of Targets 15.1–15.9;
terrestrial ecosystems, sustainably manage forests, 15.a-15.c
combat deserti cation, and halt and reverse land
degradation and halt biodiversity loss
Promote peaceful and inclusive societies for Targets 16.3; 16.4; 16.6;
sustainable development, provide access to justice 16.7; 16.8; 16.10; 16a; 16.b
for all and build e ective, accountable and inclusive
institutions at all levels
Strengthen the means of implementation and Targets 17.2–17.4;
revitalize the global partnership for sustainable 17.6-17.11; 17.14–17.19
development

⁵ From Progress report on the process of integrating biodiversity into the post-2015 framework for sustainable development
(UNEP/CBD/COP/12/15)

274 Connecting Global Priorities: Biodiversity and Human Health

antagonistic effects of complementary sustainable to human-microbial interactions), positive,
development goals and targets will be essential. negative and neutral links are quite likely to occur
This includes sustainable development goals and simultaneously. An enhanced understanding of
targets addressing health, food and freshwater health–biodiversity relationships will allow for
security, climate change and biodiversity loss. the adjustment of interventions in both sectors,
Consistent evaluations of the long-term impacts with a view to promoting human well-being over
of trade-offs are also needed. For example, the the long-term.
short-term gains from intensive and unsustainable
agricultural production must be weighed against Integrating linkages at the biodiversity–health
costs to longer-term nutritional security; the nexus in public health, conservation and
impacts of unsustainable agricultural practices sustainability strategies will contribute not only
that may exacerbate climatic pressures may also to improved health and biodiversity outcomes
lead to greater food insecurity, particularly among but also to poverty alleviation, disaster-risk
poor and vulnerable populations, by negatively reduction, and sustainable development more
influencing food availability, accessibility, broadly in line with the goals of the emerging post-
utilization and sustainability. 2015 development agenda (Horwitz et al. 2012;
Langlois et al. 2012; Romanelli, 2014b). Both the
As with other global policy developments, SDGs and the objectives of the CBD Strategic
the SDGs present many opportunities for the Plan 2011–2020 will require adequate levels of
realization of many of the key messages that resource commitment, citizen action, professional
derive from this State of Knowledge Review. It will development, capacity building, and other factors,
be up to the biodiversity conservation and human but what is most needed overall is a fundamental
health communities to help shepherd related shift in how western societies tend to view nature
national policies in the most rewarding directions. as separate from human values and needs.

Conclusion This volume has identified numerous linkages

between human health, ecosystem services,
Health is our most basic human right and one and biodiversity. While there remain serious
of the most important indicators of sustainable gaps in knowledge and the need for deep policy
development. At the same time, as the chapters innovations persists, we can look with cautious
throughout this volume have shown, the optimism toward the near future as our scientific
conservation and sustainable use of biodiversity knowledge base increases and our understanding
is imperative for the continued functioning of of these complex linkages unfolds. In turn,
ecosystems at all scales, and for the delivery political pressure to move toward sophisticated,
of ecosystem services that are essential for integrated policy design will only increase as public
human health. There are many opportunities awareness and anxiety over the immense costs of
for synergistic approaches that promote both inaction grows. In this light, connecting the global
biodiversity conservation and the health of priorities of biodiversity and health is not only
humans. In some cases there must be trade-offs prudent; it is a form of long-term insurance for
among these objectives. Indeed, because of the community resilience and the well-being of future
complexity of interactions among the components generations.
of biodiversity at various tropical levels (including
parasites and symbionts), and across ecosystems
at various scales (from the planetary-scale biomes

Connecting Global Priorities: Biodiversity and Human Health 275

 References
Chapter 1 and 2 Convention on Biological Diversity, Secretariat (CBD), (2014).
Global Biodiversity Outlook, fourth edition.
Andersson, E., Barthel, S., Borgström, S., Colding, J.,
CBD, Secretariat. (2012). Cities and Biodiversity Outlook.
Elmqvist, T., Folke, C., & Gren, Å. (2014). Reconnecting
Montreal, 64 p.
cities to the biosphere: Stewardship of green infrastructure
and urban ecosystem services. Ambio, 43(4), 445–453. CBD, Secretariat, (2010). Global Biodiversity Outlook, third
edition.
Artner, A. & Siebert, R. (2006). The role of the social
sciences for biodiversity and ecosystem management. Chapin III, F. S., Carpenter, S. R., Kofinas, G. P., Folke, C.,
Published in Jahrbuch der österreichischen Gesellschaft Abel, N., Clark, W. C., ... and Swanson, F. J. (2010). Ecosystem
für Agrarökonomie, 15, 129–141. Austrian Society for stewardship: sustainability strategies for a rapidly changing
agricultural economics. Available online: www.boku.ac.at/ planet. Trends in Ecology and Evolution, 25(4), 241–249.
oega
Chapin III, F. S., Zavaleta, E. S., Eviner, V. T., Naylor, R. L.,
Balmford, A., and Bond, W. (2005). Trends in the state of Vitousek, P. M., Reynolds, H. L., et al. (2000). Consequences
nature and their implications for human well-being. Ecology of changing biodiversity. Nature, 405(6783), 234–242.
Letters, 8(11), 1218–1234.
Chaves, L. F., Hamer, G. L., Walker, E. D., Brown, W. M.,
Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J. S., Ruiz, M. O., & Kitron, U. D. (2011). Climatic variability and
Nakashizuka, T., Raffaelli, D., and Schmid, B. (2006). landscape heterogeneity impact urban mosquito diversity and
Quantifying the evidence for biodiversity effects on ecosystem vector abundance and infection. Ecosphere, 2(6), art70
functioning and services. Ecology letters, 9(10), 1146–1156.
Chivian, E. and Bernstein, A. (Eds.) (2008). Sustaining life:
Balvanera, P., Siddique, I., Dee, L., Paquette, A., Isbell, How human health depends on biodiversity. New York: Oxford
F., Gonzalez, A., et al. (2014). Linking Biodiversity and University Press.
Ecosystem Services: Current Uncertainties and the Necessary
Crutzen, P. J. (2002). Geology of mankind. Nature, 415(6867),
Next Steps. BioScience, 64(1), 49–57.
23–23.
Barnosky, A. D., Hadly, E. A., Bascompte, J., Berlow, E. L.,
Daszak, P., Zambrana-Torrelio, C., Bogich, T. L., Fernandez,
Brown, J. H., Fortelius, M., et al. (2012). Approaching a state
M., Epstein, J. H., Murray, K. A., and Hamilton, H. (2013).
shift in Earth/’s biosphere. Nature, 486(7401), 52–58.
Interdisciplinary approaches to understanding disease
Bonds, M. H., Dobson, A. P., and Keenan, D. C. (2012). emergence: The past, present, and future drivers of Nipah
Disease ecology, biodiversity, and the latitudinal gradient in virus emergence. Proceedings of the National Academy of
income. PLoS biology, 10(12), e1001456. Sciences, 110: 3681–3688.
Butchart, S. H., Walpole, M., Collen, B., van Strien, A., Dearborn, D. C., & Kark, S. (2010). Motivations for conserving
Scharlemann, J. P., Almond, R. E., et al. (2010). Global urban biodiversity. Conservation biology, 24(2), 432–440.
biodiversity: indicators of recent declines. Science, 328(5982),
Díaz, S., Demissew, S., Joly, C., Lonsdale, W. M., &
1164–1168.
Larigauderie, A. (2015). A Rosetta Stone for nature’s benefits
Campbell, A., Kapos, V., Scharlemann, J. P.W., Bubb, P., to people. PLoS biology, 13(1).
Chenery, A., Coad, L., Dickson, B., Doswald, N., Khan, M.
Díaz, S., Demissew, S., Carabias, J., Joly, C., Lonsdale,
S. I., Kershaw, F. and Rashid, M. (2009). Review of the
M., Ash, N., Larigauderie, A., Adhikari, J.R., Ariko, S.,
Literature on the Links between Biodiversity and Climate
Baldi, A. Bartuska, A., et al. (2015). The IPBES Conceptual
Change: Impacts, Adaptation and Mitigation. Secretariat of
Framework – connecting nature and people. Current Opinion
the Convention on Biological Diversity, Montreal. Technical
in Environmental Sustainability, 14, 1–16.
Series No. 42, 124 pages.
Duraiappah, A.K. & Rogers, D. 2011. The Intergovernmental
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U.,
Platform on Biodiversity and Ecosystem Services:
Perrings, C., Venail, P., et al. (2012). Biodiversity loss and its
opportunities for the social sciences. Innovation-the
impact on humanity. Nature, 486 (7401), 59–67.
European Journal of Social Science Research, 24, (3) 217–224
Carpenter, S. R., Mooney, H. A., Agard, J., Capistrano, D., available from: ISI:000299230500002
DeFries, R. S., Díaz, S., et al. (2009). Science for managing
Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson,
ecosystem services: Beyond the Millennium Ecosystem
J., Walker, B., and Norberg, J. (2003). Response diversity,
Assessment. Proceedings of the National Academy of Sciences,
ecosystem change, and resilience. Frontiers in Ecology and the
106(5), 1305–1312.
Environment, 1(9), 488–494.
Castaneda, I., Aguilar, C., & Rand, A. (2012). Measurement
Falkowski P.G., Fenchel T. & Delong E.F. (2008). – The
and Reporting: Important Elements of Gender Mainstreaming
microbial engines that drive Earth’s biogeochemical cycles.
in Environmental Policies. Cornell JL & Pub. Pol’y, 22, 667.
Science, 320 (5879), 1034–1039.

276 Connecting Global Priorities: Biodiversity and Human Health

Folke, C. (2006). Resilience: the emergence of a perspective Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime,
for social–ecological systems analyses. Global environmental J. P., Hector, A., ... and Wardle, D. A. (2001). Biodiversity
change, 16(3), 253–267. and ecosystem functioning: current knowledge and future
challenges. Science, 294(5543), 804–808.
Gilbert, K., Hulst, N., & Rientjes, S. (2006). Social Science and
Biodiversity Why is it important? A Guide for Policy Makers. Lovasi, G. S., Quinn, J. W., Neckerman, K. M., Perzanowski,
European Centre for Nature Conservation. M. S., and Rundle, A. (2008). Children living in areas with
more street trees have lower prevalence of asthma. Journal of
Gutiérrez, N. L., Hilborn, R., & Defeo, O. (2011). Leadership,
Epidemiology and Community health, 62(7), 647–649.
social capital and incentives promote successful fisheries.
Nature, 470(7334), 386–389. Mace, G. M., Norris, K., and Fitter, A. H. (2012). Biodiversity
and ecosystem services: a multilayered relationship. Trends in
Gutierrez-Montes, I., Emery, M., & Fernandez-Baca, E.
ecology and evolution, 27(1), 19–26.
(2012). Why gender matters to ecological management
and poverty reduction. In Integrating Ecology and Poverty Mace, G. M., Reyers, B., Alkemade, R., Biggs, R., Chapin III, F.
Reduction (pp. 39–59). Springer New York. S., Cornell, S. E., Diaz, S., Jennings, S., Leadley, P., Mumby.,
et al. (2014). Approaches to defining a planetary boundary
Hahn, M.B., Gangnon, R.E., Barcellos, C., Asner, G.P., & Patz,
for biodiversity. Global Environmental Change, 28, 289–297.
J.A. (2014). Influence of Deforestation, Logging, and Fire on
Malaria in the Brazilian Amazon. Plos One, 9, (1) available Maclaurin, J., and Sterelny, K. (2008). What is biodiversity?.
from: ISI:000329460800085 University of Chicago Press.
Haines, A., Alleyne, G., Kickbusch, I., & Dora, C. (2012). Maes, J., Paracchini, M. L., Zulian, G., Dunbar, M. B., and
From the Earth Summit to Rio+ 20: integration of health and Alkemade, R. (2012). Synergies and trade-offs between
sustainable development. The Lancet, 379(9832), 2189–2197. ecosystem service supply, biodiversity, and habitat
conservation status in Europe. Biological conservation, 155,
Haines-Young, R., and Potschin, M. (2010). The links between
1–12.
biodiversity, ecosystem services and human well-being.
Ecosystem Ecology: a new synthesis, 110–139. Manfre, C., & Rubin, D. (2012). Integrating gender into
forestry research: A guide for CIFOR scientists and
Hooper, D. U., Adair, E. C., Cardinale, B. J., Byrnes, J. E.,
programme administrators. CIFOR.
Hungate, B. A., Matulich, K. et al. (2012). A global synthesis
reveals biodiversity loss as a major driver of ecosystem McCann, K. (2007). Protecting biostructure. Nature, 446
change. Nature, 486(7401), 105–108. (7131), 29–29.
Hooper, D. U., Chapin Iii, F. S., Ewel, J. J., Hector, A., McDonald, R.I., Kareiva P. and Forman, R.T.T. (2008). The
Inchausti, P., Lavorel, S., ... and Wardle, D. A. (2005). Effects of implications of current and future urbanization for global
biodiversity on ecosystem functioning: a consensus of current protected areas and biodiversity conservation. Biological
knowledge. Ecological monographs, 75(1), 3–35. Conservation 141: 1695–1703.
Hough, R.L., Biodiversity and human health: evidence McMichael, A. J., and Beaglehole, R. (2000). The changing
for causality?, (2014). Biodiversity Conservation (2014) global context of public health. The Lancet, 356(9228),
23:267–288. 495–499.
Jiang, L., Pu, Z., and Nemergut, D. R. (2008). On the Mikkelson, G.M., Gonzalez, A., & Peterson, G.D. (2007).
importance of the negative selection effect for the relationship Economic Inequality Predicts Biodiversity Loss. Plos One, 2,
between biodiversity and ecosystem functioning. Oikos, (5) available from: ISI:000207445900004
117(4), 488–493.
Millennium Ecosystem Assessment (MA) (2005a):
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, Ecosystems and human well- being: synthesis, Island Press,
D., Gittleman, J. L., and Daszak, P. (2008). Global trends in Washington DC, USA, 2005.
emerging infectious diseases. Nature, 451(7181), 990–993.
Millennium Ecosystem Assessment (2005a): Ecosystems
Kremen, C. (2005). Managing ecosystem services: what do and human well-being: biodiversity synthesis. Island Press,
we need to know about their ecology?. Ecology letters, 8(5), Washington DC, USA, 2005.
468–479.
Mitchell, R., and Popham, F. (2008). Effect of exposure to
Laporta, G.Z., de Prado, P.I.K.L., Kraenkel, R.A., Coutinho, natural environment on health inequalities: an observational
R.M., & Sallum, M.A.M. 2013. Biodiversity Can Help Prevent population study. The Lancet, 372(9650), 1655–1660.
Malaria Outbreaks in Tropical Forests. Plos Neglected Tropical
Mora, C. & Zapata, F. A. (2013), “Anthropogenic footprints on
Diseases, 7, (3) available from: ISI:000316943800052
biodiversity,” In The Balance of Nature and Human Impact, K.
Leadley, P., Proença, V., Fernández-Manjarrés, J., Pereira, H. Rohde, ed., Cambridge: Cambridge University Press.
M., Alkemade, R., Biggs, et al. (2014). Interacting regional-
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G., & Worm,
scale regime shifts for biodiversity and ecosystem services.
B. (2011). How many species are there on Earth and in the
BioScience, biu093.
ocean?. PLoS biology, 9(8), e1001127.
Levy, S. (2013). The Lyme Disease Debate Host Biodiversity
and Human Disease Risk. Environmental Health Perspectives,
121, (4) A120-A125.

Connecting Global Priorities: Biodiversity and Human Health 277

 Mori, A. S., Furukawa, T., and Sasaki, T. (2013). Response Sarkar, S., and Margules, C. (2002). Operationalizing
diversity determines the resilience of ecosystems to biodiversity for conservation planning. Journal of biosciences,
environmental change. Biological Reviews, 88(2), 349–364. 27(4), 299–308.
Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford, Schwartz, M. W., Brigham, C. A., Hoeksema, J. D., Lyons,
K. H., Ricketts, T. H., et al. (2013). Human health impacts of K. G., Mills, M. H., and Van Mantgem, P. J. (2000). Linking
ecosystem alteration. Proceedings of the National Academy of biodiversity to ecosystem function: implications for
Sciences, 110(47), 18753–18760. conservation ecology. Oecologia, 122(3), 297–305.
Naeem, S., and Wright, J. P. (2003). Disentangling biodiversity Seto, K. C., Fragkias, M., Güneralp, B., and Reilly, M. K.
effects on ecosystem functioning: deriving solutions to a (2011). A meta-analysis of global urban land expansion. PloS
seemingly insurmountable problem. Ecology letters, 6(6), one, 6(8), e23777.
567–579.
Smit, B., and Wandel, J. (2006). Adaptation, adaptive
Nelson, E., Mendoza, G., Regetz, J., Polasky, S., Tallis, H., capacity and vulnerability. Global environmental change, 16(3),
Cameron, D., et al. (2009). Modeling multiple ecosystem 282–292.
services, biodiversity conservation, commodity production,
Spangenberg, J. H., and Settele, J. (2010). Precisely incorrect?
and tradeoffs at landscape scales. Frontiers in Ecology and
Monetising the value of ecosystem services. Ecological
the Environment, 7(1), 4–11.
Complexity, 7(3), 327–337.
Ostfeld, R.S. & Keesing, F. 2000. Biodiversity and disease
Steffen, W., Richardson, K., Rockström, J., Cornell, S. E.,
risk: The case of Lyme disease. Conservation Biology, 14, (3)
Fetzer, I., Bennett, E. M. et al. (2015). Planetary boundaries:
722–728.
Guiding human development on a changing planet. Science,
Postel, S. L., and Thompson, B. H. (2005). Watershed 1259855.
protection: Capturing the benefits of nature’s water supply
Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O., & Ludwig,
services. In Natural Resources Forum (Vol. 29, No. 2, pp.
C. (2015). The trajectory of the Anthropocene: The Great
98–108). Blackwell Publishing, Ltd.
Acceleration. The Anthropocene Review, 2053019614564785.
Raudsepp-Hearne, C., Peterson, G. D., Tengö, M., Bennett,
Taylor, L. H., Latham, S. M., and Mark, E. J. (2001).
E. M., Holland, T., Benessaiah, K., ... and Pfeifer, L. (2010).
Risk factors for human disease emergence. Philosophical
Untangling the environmentalist’s paradox: Why is human
Transactions of the Royal Society of London. Series B: Biological
well-being increasing as ecosystem services degrade?.
Sciences, 356(1411), 983–989.
BioScience, 60(8), 576–589.
The Economics of Ecosystems and Biodiversity study (TEEB),
Reiss, J., Bridle, J. R., Montoya, J. M., & Woodward, G. (2009).
(2010). The Economics of Ecosystems and Biodiversity:
Emerging horizons in biodiversity and ecosystem functioning
Ecological and Economic Foundation. Earthscan, Cambridge.
research. Trends in ecology & evolution, 24(9), 505–514.
Thompson, I., Mackey, B., McNulty, S., and Mosseler, A.
Reiss, J., Bailey, R. A., Cássio, F., Woodward, G., & Pascoal,
(2009). Forest resilience, biodiversity, and climate change.
C. (2010). Assessing the contribution of micro-organisms
In A synthesis of the biodiversity/resilience/stability relationship
and macrofauna to biodiversity-ecosystem functioning
in forest ecosystems. Secretariat of the Convention on Biological
relationships in freshwater microcosms. Advances in
Diversity, Montreal. Technical Series (Vol. 43).
Ecological Research, 43, 151–176.
Thompson, R. M., Brose, U., Dunne, J. A., Hall Jr, R. O.,
Rockström, J., Steffen, W., Noone, K., Persson, Å., Chapin,
Hladyz, S., Kitching, R. L., et al. (2012). Food webs: reconciling
F. S., Lambin, E. F,. et al. (2009). A safe operating space for
the structure and function of biodiversity. Trends in ecology
humanity. Nature, 461(7263), 472–475.
and evolution, 27(12), 689–697.
Romanelli, C., Cooper, H. D., de Souza Diaz, B.F (2014a) The
Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and
integration of biodiversity into One Health. Revue Scientifique
Siemann, E. (1997). The influence of functional diversity and
et Technique 33(2): 487–496.
composition on ecosystem processes. Science, 277(5330),
Romanelli, C., Corvalan, C., Cooper, H. D., Manga, L., Maiero, 1300–1302.
M., and Campbell-Lendrum, D. (2014b). From Manaus to
Tittensor, D. P., Walpole, M., Hill, S. L., Boyce, D. G., Britten,
Maputo: Toward a Public Health and Biodiversity Framework.
G. L., Burgess, N. D., ... & Visconti, P. (2014). A mid-term
EcoHealth, 11(3), 292–299.
analysis of progress toward international biodiversity targets.
Sala, O.E., Meyerson, L.A. and Parmesan, C. (2012 ) Science, 346(6206), 241–244.
Biodiversity Change and Human Health: From Ecosystem
United Nations Human Settlements Programme
Services to Spread of disease. SCOPE/DIVERSiTAS
(UN-Habitat) (2013) State Of The World’s Cities 2012/2013:
Sandifer, P. A., Sutton-Grier, A. E., & Ward, B. P. (2015). Prosperity of Cities. Routledge. Available from:
Exploring connections among nature, biodiversity, ecosystem
UNDP (2005). UN Millennium Project  – Investing in
services, and human health and well-being: Opportunities
Development: A Practical Plan to Achieve the Millennium
to enhance health and biodiversity conservation. Ecosystem
Development Goals. London: Earthscan; 2005.
Services, 12, 1–15.
UNESCO 2013. World Social Science Report: Changing
Global Environments.

278 Connecting Global Priorities: Biodiversity and Human Health

United Nations Task Team on Social Dimensions of Climate Chapter 3
Change 2011. The social dimensions of climate change: A
discussion draft. Albright, T., T. Moorhouse, J. McNabb. 2004. “The Rise and
Fall of Water Hyacinth in Lake Victoria and the Kagera River
United Nations, Department of Economic and Social Affairs Basin, 1989–2001. Journal of Aquatic Plant Management
(UN/DESA) Population Division, (2013). World Population 42:73.
Prospects: The 2012 Revision, Press Release. 13 June 2013:
“World Population to reach 9.6 billion by 2050 with most Ashbolt, N.J., 2004. Microbial contamination of drinking
growth in developing regions, especially Africa”. Available water and disease outcomes in developing regions. Toxicology
at: http://esa.un.org/wpp/Documentation/publications.htm 198.

Walker, B., Holling, C. S., Carpenter, S. R., & Kinzig, A. (2004). Balmford A. and Bond W. (2005) Trends in the state of nature
Resilience, adaptability and transformability in social-- and their implications for human well-being. Ecology Letters,
ecological systems. Ecology and society, 9(2), 5. 8, 1218–1234.

Walter, H.S. 2003. Contested nature: Promoting international Barros FAF. 1990. Ciência e tecnologia no processo de
biodiversity with social justice in the twenty-first century. desenvolvimento da região Amazônica. Brasília: CNPq, 548p.
Geographical Review, 93, (2) 275–277 available from: Batker, D., Torre, I., Costanza, R., Swedeen, P., Day, J.,
ISI:000222838000010 Boumans, R., Bagstad, K. (2010). Gaining Ground: Wetlands,
Ward Thompson, C., Roe, J., Aspinall, P., Mitchell, R., Clow, A., Hurricanes, and the Economy: The Value of Restoring
and Miller, D. (2012). More green space is linked to less stress the Mississippi River Delta. Tacoma, Washington: Earth
in deprived communities: Evidence from salivary cortisol Economics.
patterns. Landscape and Urban Planning, 105(3), 221–229. Bednar, A. J., Garbarino, J. R., Ranville, J. F., and T. R.
World Health Organization (WHO) (2015). World health Wildeman (2002). Presence of organoarsenicals used in
statistics 2015. http://www.who.int/gho/publications/ cotton production in agricultural water and soil of the
world_health_statistics/2015/en/; ISBN 978 92 4 156488 5 southern United States. Journal of agricultural and food
chemistry, 50(25), 7340–7344.
WHO, (2014), Biodiversity. Available at: http://www.who.int/
globalchange/ecosystems/biodiversity/en/ Benedict, M. Q., R. S. Levine. (2007). Spread of the Tiger:
Global Risk of Invasion by the Mosquito Aedes albopictus.
WHO (2011). Gender, climate change and health Geneva, The American Naturalist, 7(1), 76–85.
World Health Organization.
Binelli, A., Magni, S., Soave, C., Marazzi, F., Zuccato,
World Health Organization (WHO) (2012). Our Planet, Our E., Castiglioni et al. (2014). The biofiltration process
Health, Our Future. Human Health and the Rio Conventions. by the bivalve D. polymorpha for the removal of some
Discussion paper. Geneva: World Health Organization. pharmaceuticals and drugs of abuse from civil wastewaters.
http://www.who.int/globalchange/publications/reports/ Ecological Engineering, 71, 710–721.
health_rioconventions.pdf.
Blumenfeld, S., Lu, C., Christophersen, T. and Coates, D.
WHO (2010). Hidden cities: unmasking and overcoming (2009). Water, Wetlands and Forests. A Review of Ecological,
health inequities in urban settings. Technical Report. Centre Economic and Policy Linkages. Secretariat of the Convention
for Health Development, and United Nations Human on Biological Diversity and Secretariat of the Ramsar
Settlements Programme Un-habitat. Convention on Wetlands, Montreal and Gland. CBD Technical
WHO (2008). Closing the gap in a generation: Health equity Series No. 47.
through action on the social determinants of health, Geneva. Bruijnzeel, L. A. (2004). 18 Tropical montane cloud forest:
WHO 2005. Ecosystems and human well-being: health a unique hydrological case. Forests, Water and People in the
synthesis: a report of the Millennium Ecosystem Assessment. Humid Tropics: Past, Present and Future Hydrological Research
Carlos Corvalan, Simon Hales, Anthony McMichael et al. for Integrated Land and Water Management, 462.
Geneva, World Health Organization. Brüsch, W. and B. Nilsson (1993). Nitrate transformation
Woolley, H. (2003). Urban open spaces. Taylor and Francis. and water movement in a wetland area. Hydrobiologia, 251:
103–111.
Woolley, H., Rose, S., Carmona, M. and Freeman, J. (2004)
The Value of Public Space, How High Quality Parks and Public Bullock A., Acreman, M.C. (2003) The role of wetlands in
Spaces Create Economic, Social and Environmental Value. the hydrological cycle. Hydrology and Earth System Sciences.
London: CABE Space. 7,3: 75–86.

Zhou, J., Deng, Y., Luo, F., He, Z., and Yang, Y. (2011). Buss, D. F.; Carlisle, D. M.; Chon, T. -S.; Culp, J.; Harding, J.
Phylogenetic molecular ecological network of soil microbial S.; Keizer-Vlek, H. E.; Robinson, W. A.; Strachan, S.; Thirion,
communities in response to elevated CO2. MBio, 2(4). C. & Hughes, R. M. (2015). Stream biomonitoring using
macroinvertebrates around the globe: a comparison of large-
scale programs. Environmental Monitoring and Assessment,
187: 1–21

Connecting Global Priorities: Biodiversity and Human Health 279

 Caliman, F. A., & Gavrilescu, M. (2009). Pharmaceuticals, Convention on Biological Diversity (CBD), Secretariat.
personal care products and endocrine disrupting agents in (2012). Report of the expert group on maintaining the ability
the environment–a review. CLEAN–Soil, Air, Water, 37(4– of biodiversity to continue to support the water cycle. UNEP/
5): 277–303. CBD/COP/11/INF/2
Cardinale, B.J. 2011. “Biodiversity Improves Water Quality Coetzee, J. A., Jones, R. W., & Hill, M. P. (2014). Water
Through Niche Partitioning.” Nature 472: 86–89. hyacinth, Eichhornia crassipes (Pontederiaceae), reduces
benthic macroinvertebrate diversity in a protected subtropical
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U.,
lake in South Africa. Biodiversity and conservation, 23(5),
Perrings, C., Venail, P., ... & Naeem, S. (2012). Biodiversity
1319–1330.
loss and its impact on humanity. Nature, 486(7401), 59–67.
Coetzee, J. A., & Hill, M. P. (2012). The role of eutrophication
Carmichael, W. W. (2001). Health effects of toxin-producing
in the biological control of water hyacinth, Eichhornia
cyanobacteria:“The CyanoHABs”. Human and ecological risk
crassipes, in South Africa. BioControl, 57(2), 247–261.
assessment: An International Journal, 7(5) 1393–1407.
Cosgrove, W. J., & Rijsberman, F. R. (2014). World water
Carpenter, S. R., Stanley, E. H., & Vander Zanden, M. J. (2011).
vision: making water everybody’s business. Routledge.
State of the world’s freshwater ecosystems: physical, chemical,
and biological changes. Annual Review of Environment and Costanza, R., d’Arge, R., de Groot, R., Farberk, S., Grasso,
Resources, 36, 75–99. M., Hannon, B., Limburg, K. Naeem, S. O’Neill, R.V. Paruelo,
J. Raskin, R.G. Sutton, P. and van den Belt, M. (1997). The
Carr, G. M., and Neary, J. P. (2008). Water quality for
value of the world’s ecosystem services and natural capital.
ecosystem and human health. UNEP/Earthprint.
Nature 387: 253–260.
Cattaneo, M. G., Yafuso, C., Schmidt, C., Huang, C. Y.,
Dale, P. and Knight, J. (2008). Wetlands and mosquitoes: a
Rahman, M., Olson, C., ... and Carriere, Y. (2006). Farm-scale
review. Wetlands Ecology and Management, 16(4), 255–276.
evaluation of the impacts of transgenic cotton on biodiversity,
pesticide use, and yield. Proceedings of the National Academy Dale, P. and Connelly, R. (2012). Wetlands and human
of Sciences, 103(20), 7571–7576. health: an overview. Wetlands Ecology and Management, 20(3),
165–171.
Cazenave, J., Wunderlin, D. A., de los Angeles Bistoni, M.,
Amé, M. V., Krause, E., Pflugmacher, S., & Wiegand, C. Daniel, R.B. and J.W. Gilliam (1996). Sediment and chemical
(2005). Uptake, tissue distribution and accumulation of load reduction by grass and riparian filters. Soil Sci. Soc. Am.
microcystin-RR in Corydoras paleatus, Jenynsia multidentata J., 60, pp. 246–251.
and Odontesthes bonariensis: A field and laboratory study.
DEFRA. 2007. The protection of waters against pollution from
Aquatic Toxicology, 75, 178–190.
agriculture: consultation on implementation of the Nitrates
Chapagain, A., Hoekstra, A., Savenije, H., Goutam, R. (2006) Directive in England. London: DEFRA Publications. Available
The water footprint of cotton consumption: an assessment at: http://archive.defra.gov.uk/environment/quality/water/
of the impact of worldwide cotton products on the water waterquality/diffuse/nitrate/documents/consultation-
resources of the cotton producing countries. Ecological supportdocs/consultation.pdf. Accessed on 14 August 2014.
Economics 60(1):186–203.
DEFRA, (2004). Making space for water: Taking forward a
Charles, H. Dukes, J.S. (2007) Impacts of invasive species on new Government strategy for flood and coastal erosion risk
ecosystem services. In: Nentwig, W; ed. Biological invasions. management in England. In: First Government Response
Ecol. Studies 193. New York: Springer; pp. 217–337. to the Autumn 2004 Making Space for Water Consultation
Exercise.
Chen, J., He, D., & Cui, S. (2003). The response of river
water quality and quantity to the development of irrigated De Moor, F. C. (1994). Aspects of the life history of Simulium
agriculture in the last 4 decades in the Yellow River Basin, chutteri and S. bovis (Diptera; Simuliidae) in relation to
China. Water Resources Research, 39(3). changing environmental conditions in South African rivers.
Verhandlungen Internationale Vereinigung Limnologie 25,
Chorus, I., & Bartram, J. (1999). Toxic cyanobacteria in water:
1817–1821.
A guide to their public health consequences, monitoring and
management. Published on behalf of UNESCO, WHO and Diaz, R. J. (2001). Overview of hypoxia around the world.
UNEP by Spon Press. Journal of environmental quality, 30(2), 275–281.
Coates, C., and Smith, M. (2012). Chapter 11: Natural Diaz, R.J. and R. Rosenberg (2008). Spreading dead zones
infrastructure solutions for water security. In R. Ardakanian& and consequences for marine ecosystems. Science, 321(5891),
D. Jaeger (Eds.), Water and the green economy (1 ed., Vol. 1, 926–929.
pp. 167–181). Bonn, Germany: UNW-DPC.
Döll, P., & Siebert, S. (2002). Global modeling of irrigation
Cohen, AN; Carlton, JT. (1998) Accelerating invasion rate in water requirements. Water Resources Research, 38(4), 8–1.
a highly invaded estuary. Science 279(5350):555–558.
Convention on Biological Diversity (CBD), Secretariat. (2014).
Global Biodiversity Outlook. Secretariat of the Convention on
Biological Diversity.

280 Connecting Global Priorities: Biodiversity and Human Health

Drace, K.; Kiefer, A. M.; Veiga, M. M.; Williams, M. K.; Floyd, T; Williams, J. (2004) Impact of green crab (Carcinus
Ascari, B.; Knapper, K. A.; Logan, K. M.; Breslin, V. M.; maenas L.) predation on a population of soft-shell clams (Mya
Skidmore, A.; Bolt, D. A.; Geist, G.; Reidy, L. & Cizdziel, J. arenaria L.) in the southern Gulf of St. Lawrence. J of Shellfish
V. (2012). Mercury-free, small-scale artisanal gold mining in Res 23(2):457–462.
Mozambique: utilization of magnets to isolate gold at clean
Frei, A., Armstrong, R., Clark, M., Serreze, M. (2002) Catskill
tech mine. Journal of Cleaner Production, 32: 88–95.
Mountain Water Resources: Vulnerability, Hydroclimatology,
Dudgeon, D., Arthington, A. H., Gessner, M. O., Kawabata, and Climate Change Sensitivity. Annals of the Association of
Z. I., Knowler, D. J., Lévêque, C., ... & Sullivan, C. A. (2006). American Geographers 92(2):203–224.
Freshwater biodiversity: importance, threats, status and
Freitas de Magalhães, V., Moraes Soares, R., & Azevedo,
conservation challenges. Biological reviews, 81(2), 163–182.
S. M. (2001). Microcystin contamination in fish from the
Ellis, E.C, Goldewijk K.K, Siebert, S, Lightma, D, Ramankutty, Jacarepaguá Lagoon (Rio de Janeiro, Brazil): ecological
N, (2010). Anthropogenic transformation of the biomes, implication and human health risk. Toxicon, 39(7),
1700–2000, Global Ecology and Biogeography, 19, 589–606. 1077–1085.
European Environment Agency (EEA). (2005). Source Fuller, K., Shear, H. and Wittig, J. (1995). Great Lakes Atlas.
apportionment of nitrogen and phosphorus inputs into Great Lakes National Program Office, U.S. Environmental
the aquatic environment. EEA Report, 7 Office for Official Protection Agency, 3rd Edition. Chicago, Ill. (USA).
Publications of the European Communities: Luxembourg.
Gardner, R. C., Barchiesi, S., Beltrame, C., Finlayson, C. M.,
ISBN 92–9167–777–9. 48 pp.
Galewski, T., Harrison, I., ... & Walpole, M. (2015). State of the
EPA (2008) U.S. Environmental Protection Agency. Effects of World’s Wetlands and Their Services to People: A Compilation
climate change for aquatic invasive species and implications for of Recent Analyses.
management and research. National Center for Environmental
Gerba, C. P., & Smith, J. E. (2005). Sources of pathogenic
Assessment, Washington, DC; EPA/600/R-08/014. Available
microorganisms and their fate during land application of
from the National Technical Information Service, Springfield,
wastes. Journal of Environmental Quality, 34(1), 42–48.
VA, and online at http://www.epa.gov/ncea.
Glandon, R.F., McNabb, P.C. and T. Batterson (1981). A
Erlanger, Tobias E., et al. “The Attributable Fraction
comparison of rain related phosphorous and nitrogen loading
of the Lymphatic Filariasis Burden to Water Resource
from urban, wetland and agricultural sources. Water Res., 15,
Development and Management.” Report prepared for the
pp. 881–892
WHO commissioned study Burden of water-related vector-
borne diseases: An analysis of the fraction attributable Glantz, M.H. (1998). Creeping environmental problems in
to components of water resources development and the Aral Sea basin. In Kobori, I. And M.H. Glantz (Eds.),
management. Central Eurasian Water Crisis: Caspian, Aral and Dead Seas,
United Nations University Press, New York (1998).
Ervin, J., Sekhran, N., Dinu, A., Gidda, S., Vergeichik, M.,
& Mee, J. (2010). Protected Areas for the 21st Century: Glenn, E. P., Lee, C., Felger, R., & Zengel, S. (1996). Effects
Lessons from UNDP/GEF’s Portfolio. In New York: United of water management on the wetlands of the Colorado River
Nations Development Programme and Montreal: Convention on delta, Mexico. Conservation Biology, 10(4), 1175–1186.
Biological Diversity.
Goldschmidt, T., Witte, F., & Wanink, J. (1993). Cascading
European Topic Centre on Water (2010). Climate Change effects of the introduced Nile perch on the detritivorous/
Impacts on Water Quality and Biodiversity: Background Report phytoplanktivorous species in the sublittoral areas of Lake
for EEA European Environment State and Outlook. Prague. Victoria. Conservation Biology, 7(3), 686–700.
Evers, B. N., Madsen, H., McKaye, K. M., & Stauffer Jr, J. Hacon S, Azevedo F. 2006. Plano de ação regional para
R. (2006). The schistosome intermediate host, Bulinus prevenção e controle da contaminação por mercúrio nos
nyassanus, is a ‘preferred’ food for the cichlid fish, Ecossistemas Amazônicos. Brasilia – DF – OTCA. p 8–46.
Trematocranus placodon, at Cape Maclear, Lake Malawi.
Hallegraeff, G.M. (1998). “Transport of toxic dinoflagellates
Annals of tropical medicine and parasitology, 100(1), 75–85.
via ships’ ballast water: Bioeconomic risk assessment and
Fenwick, A. (2006). Waterborne infectious diseases – could efficacy of possible ballast water management strategies”.
they be consigned to history?. Science, 313(5790), 1077–1081. Marine Ecology Progress Series 168: 297–309
Fearnside PM. 1999. Social Impacts of Brazil’s Tucuruí Dam. Hamilton, L. S. (1995). Mountain cloud forest conservation
Environmental Management 24(4): 485–495. and research: a synopsis. Mountain Research and Development,
259–266.
Fisher J. and Acreman C. (2004). Wetland nutrient removal: a
review of the evidence. Hydrology and earth System Sciences, Hanna, D. E., Solomon, C. T., Poste, A. E., Buck, D. G., &
8 (4). 673–685. Chapman, L. J. (2014). A review of mercury concentrations
in freshwater fishes of Africa: Patterns and predictors.
Fleming, L.E., McDonough, N., Austen, M. Mee, L., Moore,
Environmental Toxicology and Chemistry.
M., Hess, P., … Smalley, A., Oceans and Human Health: A
rising tide of challenges and opportunities for Europe, Marine
Environmental Research, Volume 99, August 2014, Pages
16–19.

Connecting Global Priorities: Biodiversity and Human Health 281

 Heuer, H., Krögerrecklenfort, E., Wellington, E. M. H., Millennium Ecosystem Assessment (MA). (2005b). Mountain
Egan, S., Elsas, J. V., Overbeek, L., ... & Smalla, K. (2002). Systems: Millennium Ecosystem Assessment- Chapter 24.
Gentamicin resistance genes in environmental bacteria: Ecosystems and Human Well-being: Current State and
prevalence and transfer. FEMS Microbiology ecology, 42(2), Trends. Island Press, Washington, DC.
289–302.
Marchand, C., Fernandez, J. M., Moreton, B., Landi, L.,
Hey, D., Kostel, J., Crumpton, W., Mitsch, W., Scott, B. (2012). Lallier-Vergès, E., & The partitioning of transitional metals
The roles and benefits of wetlands in managing reactive (Fe, Mn, Ni, Cr) in mangrove sediments downstream of a
nitrogen. Journal of Soil and Water Conservation, 67(2), ferralitized ultramafic watershed (New Caledonia). Chemical
(47A- 54A). Geology, 300–301(0), 70–80.
Horwitz, P., Finlayson, M. and Weinstein, P. (2012). Mazepova, G.F. (1998). The role of copepods in the Baikal
Healthy wetlands, healthy people: a review of wetlands ecosystem.Journal of Marine Systems, 15 (1–4), 113–120.
and human health interactions. Ramsar Technical Report
McGeoch, Melodie A, S. H. M. Butchart, D. Spear, E. Marais,
No. 6. Secretariat of the Ramsar Convention on Wetlands,
E. J. Kleynhans, A. Symes, J. Chanson and M. Hoffmann.
Gland, Switzerland, & World Health Organization, Geneva,
2010 “Global indicators of biological invasion: species
Switzerland.
numbers, biodiversity impact and policy responses.” Diversity
Hotez, P. J., & Kamath, A. (2009). Neglected tropical diseases and Distributions 16: 95–108.
in sub-Saharan Africa: review of their prevalence, distribution,
McNeely, J. A. (2001). An introduction to human dimensions
and disease burden. PLoS neglected tropical diseases, 3(8).
of invasive alien species. The Great Reshuffling: Human
Ibelings B.W. and Chorus, I. (2007). Accumulation of Dimensions of Invasive Alien Species. IUCN Publishers, Gland,
cyanobacterial toxins in freshwater ‘‘seafood’’ and its Switzerland, 5–22.
consequences for public health: A review. Environmental
Micklin, P. (2007). The Aral sea disaster. Annu. Rev. Earth
Pollution 150: 177- 192.
Planet. Sci., 35, 47–72.
IWMI. (2007). Water for Food, Water for Life: A
Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford,
Comprehensive Assessment of Water Management in
K. H., Ricketts, T. H., Turner, W.R., and Osofsky, S. A. (2013).
Agriculture; Molden, D. Ed.; Earthscan and IWMI: London
Human health impacts of ecosystem alteration. Proceedings
2007.
of the National Academy of Sciences, 110(47), 18753–18760.
Keesing. F., Holt R. D. and Ostfeld R. S. (2006). Effects of
Myers, S. S., & Patz, J. A. (2009). Emerging Threats to Human
species diversity on disease risk. Ecology Letters 9: 485–498.
Health from Global Environmental Change. Annu. Rev.
Kemper, N. (2008). Veterinary antibiotics in the aquatic and Environ. Resour, 34, 223–52.
terrestrial environment. Ecological indicators, 8(1), 1–13.
Molyneux, D., Ostfeld R.S., Bernstein, A., and Chivian, E.
Kou, Y., Lu, X., Zhang, Z., Song, X., Cao, X. (2012). Nitrogen (2008). Ecosystem disturbance, biodiversity loss, and human
retention and purification efficiency for typical wetlands infectious disease. In Sustaining Life: How Human Health
in West Jilin: effects based on microcosm experiment and Depends on Biodiversity, ed. E Chivian, A Bernstein, pp. 287–
phosphorus increase. Journal of Food, Agriculture and 323. Oxford/ New York: Oxford Univ. Press.
Environment, 10 (2), 1035–1039.
Nakamura, K., Nakayama, H., Hideshima, Y., Ishida, T.,
Lapworth, D. J., Baran, N., Stuart, M. E., & Ward, R. S. (2012). Ogikibo, J. and S. Moriwaki (2001). Drainage flows in grass
Emerging organic contaminants in groundwater: a review of and forest slope lands. Proceedings of the JSIRDE Annual
sources, fate and occurrence. Environmental pollution, 163, Meeting, pp. 44–45.
287–303.
Naiman, R. J., & Décamps, H. (1997). The ecology of
Lee, K.H., Isenhart, T.M. and R.C. Schultz (2003). Sediment interfaces: riparian zones. Annual review of Ecology and
and nutrient removal in an established multi-species riparian Systematics, 621–658.
buffer. Journal of Soil and Water Conservation, 58(1), 1–8.
Newell, R.I.E. (2004). Ecosystem influences of natural
Lobell, D. B., Cassman, K. G., & Field, C. B. (2009). Crop and cultivated populations of suspension-feeding bivalve
yield gaps: their importance, magnitudes, and causes. Annual molluscs: a review. Journal of Shellfish Research, 23: 51–61.
Review of Environment and Resources, 34(1), 179.
N’Goran, E. K., Diabate, S., Utzinger, J., & Sellin, B.
LoGiudice, K. Ostfeld, R.S., Schmidt, K.A. and Keesing, F. (1997). Changes in human schistosomiasis levels after the
(2003). The ecology of infectious disease: effects of host construction of two large hydroelectric dams in central Côte
diversity and community composition on Lyme disease risk. d’Ivoire. Bulletin of the World Health Organisation, 75(6),
Proc. Natl. Acad. Sci. 100: 567–571. 541–545.
Millennium Ecosystem Assessment (MA). (2005a). Norman, R., Bowers, R. G., Begon, M., & Hudson, P. J. (1999).
Ecosystems and Human Well-being: Biodiversity Synthesis. Persistence of tick-borne virus in the presence of multiple host
World Resources Institute, Washington, DC. species: tick reservoirs and parasite mediated competition.
Journal of Theoretical Biology, 200(1), 111–118.

282 Connecting Global Priorities: Biodiversity and Human Health

Oliver, D.M., Heathwaite, L., Haygarth, P.M. and C.D. Clegg Prüss-Üstün A, Kay D, Fewtrell L, Bartram J, 2004. Unsafe
(2005). Transfer of Escherichia coli to water from drained and water, sanitation and hygiene. In Comparative Quantification
undrained grassland after grazing. Journal of Environmental of Health Risks: The Global and Regional Burden of Disease
Quality, 34 (2005), pp. 918–925. Attributable to Selected Major Risk Factors. Volumes 1 and
2. Ezzati, M, et al., eds. Geneva: World Health Organization.
Ostfeld R.S. and Keesing, F. (2000). The function of
biodiversity in the ecology of vector-borne zoonotic diseases. Pysek, P., and D. Richardson. (2010) Invasive species,
Can. J. Zool. 78: 2061–2078. environmental change and management, and health. Annual
Review of Environmental and Resources 35:25–55.
Ostroumov, S. A. (2005). On Some Issues of Maintaining
Water Quality and Self-Purification. Water Resources, 32: Ragosta, G., Evensen, C., Atwill, E. R., Walker, M., Ticktin,
305–313. T., Asquith, A., & Tate, K. W. (2010). Causal connections
between water quality and land use in a rural tropical island
Ostroumov, S. A. (2006). Biomachinery for maintaining
watershed. EcoHealth, 7(1), 105–113.
water quality and natural water self-purification in marine
and estuarine systems: elements of a qualitative theory. Resh, V. H. (2010). Vector-borne diseases of freshwater
International Journal of Oceans and Oceanography, 1: habitats. Lake Ecosystem Ecology: A Global Perspective, 403.
111–118.
Ricciardi, A. (2006) Patterns of invasion in the Laurentian
Palmer, M. A. and Febria, C. M. (2012). The heartbeat of Great Lakes in relation to changes in vector activity. Divers
ecosystems. Science, 336(6087), 1393–1394. Distrib 12(4):425–433.
Pan Africa Chemistry Network. (PACN). (2010). Africa’s Ronderos M.M., Greco, N.M., & Spinelli G.R. (2003).
Water Quality. Diversity of biting midges of the genus Culicoides Latreille
(Diptera: Ceratopogonidae) in the area of the Yacyreta Dam
Pan-American Health Organization (PAHO), (2012). Health
Lake between Argentina and Paraguay. Memórias do Instituto
in the Americas.Washington D.C: Pan American Health
Oswaldo Cruz 98 (1):19 – 24.
Organization.
Rudolf, V.H. & Antonovics J. (2005). Species coexistence and
Passos, C. J., & Mergler, D. (2008). Human mercury exposure
pathogens with frequency-dependent transmission. Am.
and adverse health effects in the Amazon: a review. Cadernos
Nat.166: 112–118.
de Saúde Pública, 24, s503-s520.
Russi D., ten Brink P., Farmer A., Badura T., Coates D., Förster
Patz, J. A., Daszak, P., Tabor, G. M., Aguirre, A. A., Pearl,
J., Kumar R. and Davidson N. (2012) The Economics of
M., Epstein, J., ... & Working Group on Land Use Change
Ecosystems and Biodiversity for Water and Wetlands. Final
Disease Emergence. (2004). Unhealthy landscapes: policy
Consultation Draft.
recommendations on land use change and infectious disease
emergence. Environmental health perspectives, 112(10), 1092. Santos, L. H., Araújo, A. N., Fachini, A., Pena, A.,
Delerue-Matos, C., & Montenegro, M. C. B. S. M. (2010).
Pejchar, L., & Mooney, H. A. (2009). Invasive species,
Ecotoxicological aspects related to the presence of
ecosystem services and human well-being. Trends in ecology
pharmaceuticals in the aquatic environment. Journal of
& evolution, 24(9), 497–504.
Hazardous Materials, 175(1–3), 45–95.
Pereira, L.S., Cordery, I. and I. Iacovides (2002). Coping
Schwarzenbach, R. P., Egli, T., Hofstetter, T. B., Von Gunten,
with water scarcity. International Hydrological Programme
U., & Wehrli, B. (2010). Global water pollution and human
UNESCO, Paris.
health. Annual Review of Environment and Resources, 35,
Porvari, P. (1995). Mercury levels in fish in Tucuruí 109–136.
hydroelectric reservoir and in River Moju in Amazonia, in
Schwarzenbach, R. P., Escher, B. I., Fenner, K., Hofstetter,
the state of Pará, Brazil. The Science of the Total Environment
T. B., Johnson, C. A., Von Gunten, U., & Wehrli, B. (2006).
175: 109–117.
The challenge of micropollutants in aquatic systems. Science,
Prüss-Ustün, A., Bartram, J., Clasen, T., Colford, J. M., 313(5790), 1072–1077.
Cumming, O., Curtis, V., ... & Cairncross, S. (2014). Burden of
Shaw, G., & Lam, P. (2007). Health aspects of freshwater
disease from inadequate water, sanitation and hygiene in low-
cyanobacterial toxins. Water Science & Technology: Water
and middle-income settings: a retrospective analysis of data
Supply, 7(2), 193–203.
from 145 countries. Tropical Medicine & International Health.
Shaw, G. R., Moore, D. P., & Garnett, C. (2003). Eutrophication
Prüss-Üstün A., Bos, R., Gore, F. & Bartram, J. 2008. Safer
and Algal Blooms. Environmental and Ecological Chemistry,
water, better health: costs, benefits and sustainability of
1–21.
interventions to protect and promote health. World Health
Organization, Geneva. Shiklomanov, I. A., (Ed.), Assessment of Water Resources and
Water Availability in the World, Comprehensive Assessment
Prüss-Üstün, A., & Corvalán, C. (2006). Preventing disease
of the Freshwater Resources of the World, Stockholm
through healthy environments. Geneva: World Health
Environment Institute, Stockholm, 1997.
Organization.
Simberloff D., Parker I.M., Windle P.N. 2005 “Introduced
species policy, management, and future research needs.”
Frontiers in Ecology and the Environment 3: 12–20.

Connecting Global Priorities: Biodiversity and Human Health 283

 Smith V.H., Schindler D.W. 2009. Eutrophication science: UNIDO (1996). Advisory Assistance on Avoidance Mercury
where do we go from here? Trends in Ecology and Evolution 24 Pollution from Artisanal Gold Mining Operations in State
(4): 201–207. DOI: 10.1016/j.tree.2008.11.009 http://www. of Bolivar, Venezuela. Prepared by M.M. Veiga, contract SI/
sciencedirect.com/science/article/pii/S016953470900041X VEN/94/801/11–51. 147 pp.
(30 July 2014).
United States Environmental Protection Agency (US EPA),
Soth, J., Grasser, C. and R. Salerno (1999). The Impact (2003). Guidelines establishing test Procedures for the
of Cotton on Fresh Water Resources and Ecosystems: A Analysis of Pollutants, Analytical Methods for Biological
Preliminary Analysis. WWF, Gland, Switzerland. Pollutants in Ambient Water (Final Rule, U.S. Federal
Register- 40 CFR Part 136 Vol. 68, No.139).
Soto D & Mena G. 1999. Filter feeding by the freshwater
mussel, Diplodon chilensis, as a biocontrol of salmon farming Uyigue, E. (2005). Dams and livelihood: the problems of
eutrophication. Aquaculture 171: 65–81. parasitic diseases in communities hosting dams in Nigeria.
In International Water Management Institute Conference
Southgate V, Wijk H, Wright C. 1976. Schistosomiasis in Loum,
Papers (No. h041154).
Cameroun: Schistosoma haematobium, S. intercalatum, and
their natural hybrid. Z. Parasitenkd. 49:149–59 Van Buskirk, J. and Ostfeld R.S. (1995). Controlling Lyme
disease risk by modifying the density and species composition
Stearns, B. P., & Stearns, S. C. (2010). Still Watching, from the
of tick hosts. Ecol. Appl. 5: 1133–1140.
Edge of Extinction. BioScience, 60(2), 141–146.
Veiga, M. M., Angeloci-Santos, G., Meech, J. A. (2014) Review
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006)
of barriers to reduce mercury use in artisanal gold mining. The
Schistosomiasis and water resources development: systematic
Extractive Industries and Society, 1: 351–361.
review, meta-analysis, and estimates of people at risk. Lancet
Infect Dis 6(7): 411–425. 10.1016/S1473–3099(06)70521–7. Veiga M. M. (1997). Introducing New Technologies for
Abatement of Global Mercury Pollution in Latin America –
Stoett, P. J. (2012). Global Ecopolitics: Crisis, Governance, and
Rio de Janeiro: UNIDO/UBC/CETEM/CNPq, 94pp.
Justice. University of Toronto Press.
Veiga M. M, Meech J. Á. and Oñates, N. (1994). Mercury
Sylvester F, Dorado J, Boltovskoy D, Juárez A & Cataldo D.
Pollution from Deforestation. Nature 368: 816–817.
2005. Filtration rates of the invasive pest bivalve Limnoperna
fortunei as a function of Size and Temperature. Hydrobiologia Viviroli, D., R. Weingartner, and B. Messerli. 2003. Assessing
534: 71–80. the hydrological significance of the world’s mountains.
Mountain Research and Development 23 1:32–40.
Tennstedt, T., Szczepanowski, R., Braun, S., Pühler, A. and
Schlüter, A. (2003). Occurrence of integron-associated Woltermade, C.J. (2000). Ability of restored wetlands
resistance gene cassetes located on antibiotic resistance to reduce nitrogen and phosphorus concentrations in
plasmids isolated from a wastewater treatment plant. FEMS agricultural drainage water. Journal of Soil and Water
Microbiol Ecol 45: 239–252. Conservation, 55(3), 303–309.
Tundisi, J.G., Tundisi. T.M. and Rocha (2002). Ecossistemas WHO (2013) Global health observatory-data repository
de água interiores, p. 153–170. In: Rebouças AC & Braga [Online]. http://apps.who.int/ghodata/files/84/ghodata.
B (eds). Águas doces do Brasil. Caital ecológico, uso e html.
conservaçção. São Paulo, Escrituras, 2ª edição, 704 pp.
WHO (2010a). Progress on Sanitation and Drinking-Water:
United Nations Environment Programme (UNEP) (2013). 2010 Update. WHO Press, World Health Organization, 20
Global Mercury Assessment 2013: Sources, Emissions, Avenue Appia, 1211 Geneva 27, Switzerland.
Releases and Environmental Transport. Division of
WHO (2010b). Water for Health: WHO Guidelines for
Technology, Industry and Economics (DTIE), Geneva,
Drinking-Water Quality. Geneva.
pp. 44. http:// www.unep.org/PDF/PressReleases/
GlobalMercuryAssessment2013.pdf (Accessed 4 September, WHO, (2004). Waterborne Zoonoses: Identification, Causes,
2013). and Control/ Edited by J.A. Cotruvo, A. Dufour, G. Rees, J.
Bartram, R. Carr, D.O. Cliver, G.F. Craun, R. Fayer and V.P.J.
UNEP (2012). Measuring Progress: Environmental Goals
Gannon
& Gaps. United Nations Environment Programme (UNEP),
Nairobi: http://unep.org/geo/pdfs/geo5/Measuring_ WHO (2003a). Quantifying selected major risks to health.
progress.pdf (Accessed August 14, 2014). The World Health Report 2002. World Health Organization,
Geneva (Chapter 4).
UNEP, UNICEF & WHO (2002). United Nations Environment
Programme, United Nations Children´s Fund and World WHO (2003b). Emerging Issues in Water and Infectious
Health Organization. Children in the New Millennium: Disease. World Health Organization, Geneva.
Environmental Impact on Health. Republic of Malta: 141 pp.
WHO (1999). Toxic Cyanobacteria in Water: A guide to their
UNESCO, 2009. World Water Assessment Programme. The public health consequences, monitoring and management/
United Nations World Water Development Report 3: Water Chorus, I. and Bartram, J. (Eds).
in a Changing World. Paris: UNESCO, and London: Earthscan.
WHO and UNICEF (2012). Progress on Drinking Water and
Sanitation: 2012 Update. United States: WHO/UNICEF Joint
Monitoring Programme for Water Supply and Sanitation.

284 Connecting Global Priorities: Biodiversity and Human Health

WWF. (2012). Living Planet Report 2012. WWF International, Cao, T., M. Wang, et al. (2009). “Air quality for metals and
Gland, Switzerland. sulfur in Shanghai, China, determined with moss bags.”
Environmental Pollution 157(4): 1270–1278.
Yongsi, H. B. N. (2010). Suffering for water, suffering from
water: access to drinking-water and associated health risks in Cape, J. N., L. J. van der Eerden, et al. (2009). “Evidence for
Cameroon. Journal of health, population, and nutrition, 28(5), changing the critical level for ammonia.” Environmental
424. Pollution 157(3): 1033–1037.
Zakhary, K. (1997). Factors affecting the prevalence of Cardelino C.A., Chameides W.L. (1990). Natural
schistosomiasis in the Volta region of Ghana. McGill Journal hydrocarbons, urbanization, and urban ozone. Journal of
of Medicine, 3, 93–101. Geophysical Research. 95(D9):13,971–13,979.
Zhang, X. X., Zhang, T., & Fang, H. H. (2009). Antibiotic Cariñanosa P, Casares-Porcela M, et al. (2014). Estimating the
resistance genes in water environment. Applied microbiology allergenic potential of urban green spaces: A case-study in
and biotechnology, 82(3), 397–414. Granada, Spain. Landscape and Urban Planning 123; 134–144
Zettler, E., T. Mincer, and Amaral-Zettler, L. (2013) Life Castro Ribeiro, M., P. Pinho, et al. (2014). “Associations
in the Plastisphere: Microbial Communities on Plastic between outdoor air quality and birth weight: a geostatistical
Marine Debris. Environmental Science and Technology sequential simulation approach in Coastal Alentejo, Portugal.”
47(13):7137–7146. Stochastic Environmental Research and Risk Assessment 28(3):
527–540.
Chapter 4 Cavanagh J.E., Zawar-Reza P., et al. (2009). Spatial
attenuation of ambient particulate matter air pollution within
Aničić, M., M. Tomašević, et al. (2009). “Monitoring of trace an urbanised native forest patch. Urban Forestry and Urban
element atmospheric deposition using dry and wet moss Greening 8:21–30.
bags: Accumulation capacity versus exposure time.” Journal
of Hazardous Materials 171(1–3): 182–188. Chang, C. Li, M., Chang, S. (2007). A preliminary study on
the cool-island intensity of Taipei city parks. Landscape and
Augusto, S., C. Máguas, et al. (2013). “Guidelines for Urban Planning 80, 386–395.
biomonitoring persistent organic pollutants (POPs), using
lichens and aquatic mosses – A review.” Environmental Costello, L.R., Jones, K.S. (1994). WUCOLS: Water Use
Pollution 180(0): 330–338. Classification of Landscape Species – A guide to the water
needs of landscape plants. Half Moon Bay, CA: University
Augusto, S., C. Maguas, et al. (2010). “Lichens as an of California Cooperative Extension, San Mateo and San
integrating tool for monitoring PAH atmospheric deposition: Francisco Counties. 90 p.
a comparison with soil, air and pine needles.” Environmental
Pollution 158(2): 483–489. Costonis, A.C. (1976). Criteria for evaluating air pollution
injury to forest trees. Oslo, Norway: IUFRO Congress.
Augusto, S., M. J. Pereira, et al. (2012). “Assessing human
exposure to polycyclic aromatic hydrocarbons (PAH) in a Dasch J.M. (1987). Measurement of dry deposition to
petrochemical region utilizing data from environmental surfaces in deciduous and pine canopies. Environmental
biomonitors.” J Toxicol Environ Health A 75(13–15): Pollution 44:261–277.
819–830.
Fann N., Lamson A.D., et al. (2012). Estimating the National
Barbour, M.G, Burk, J.H., et al.(1980). Terrestrial plant Public Health Burden Associated with Exposure to Ambient
ecology, 1st edn. Benjamin/Cummings, Menlo Park, CA. PM2.5 and Ozone. Risk Analysis 32:81–95.
Black, V.J. (1985). SO2 effects on stomatal behavior. In: Gadsdon, S. R., J. R. Dagley, et al. (2010). “Relationships
Winner W.E., Mooney, H.A. and Goldstein R.A. eds. Sulfur between lichen community composition and concentrations
dioxide and vegetation. Stanford, CA: Stanford University of NO2 and NH3.” Environmental Pollution 158(8):
Press: 96–117. 2553–2560.
Brauer, M. (2010). “How Much, How Long, What, and Where.” Garsed, S.G. (1985). SO2 uptake and transport. In: Winner W.
Proceedings of the American Thoracic Society 7(2): 111–115. E., Mooney, H. A. and Goldstein R.A. eds. Sulfur dioxide and
vegetation. Stanford, CA: Stanford University Press: 75–95.
Bytnerowicz A., Fenn M.E., et al. (1999). Wet and dry
pollutant deposition to the mixed conifer forest. In: Oxidant Geiser, L. H., S. E. Jovan, et al. (2010). “Lichen-based critical
Air Pollution Impacts in the Montane Forests of Southern loads for atmospheric nitrogen deposition in Western Oregon
California: A Case Study of the San Bernardino Mountains and Washington Forests, USA.” Environmental Pollution
(Eds. Miller PR & McBride JR) Springer-Verlag. New York. 158(7): 2412–2421.
pp. 235–269.
Geron, C.D., Guenther, A.B., et al. (1994). An improved model
Calfapietra, C., Mugnozza, G.S., et al. (2008). Isoprene for estimating emissions of volatile organic compounds
emission rates under elevated CO2 and O3 in two field-grown from forests in the eastern United States. J. Geophys. Res.
aspen clones differing in their sensitivity to O3 . New Phytol. 99(D6):12,773–12,791.
179:55–61
Gromke C., Ruck B. (2009). On the impact of trees on
dispersion processes of traffic emissions in street canyons.
Boundary-Layer Meteorology 131(1):19−34.

Connecting Global Priorities: Biodiversity and Human Health 285

 Guenther, A. (2002). The contribution of reactive carbon Luley, C.J., Bond, J. (2002). A plan to integrate management
emissions from vegetation to the carbon balance of terrestrial of urban trees into air quality planning. Report to Northeast
ecosystems. Chemosphere 49: 837–844. State Foresters Association. Davey Resource Group, Kent,
OH. 73 p.
Haigh, M.J. (1980). Ruderal communities in English cities.
Urban Ecology 4, 329–338. Markert, B., U. Herpin, et al. (1996). “A comparison of heavy
metal deposition in selected Eastern European countries
Harmens, H., L. Foan, et al. (2013). “Terrestrial mosses
using the moss monitoring method, with special emphasis
as biomonitors of atmospheric POPs pollution: A review.”
on the ‘Black Triangle’.” Science of the Total Environment
Environmental Pollution 173(0): 245–254.
193(2): 85–100.
Hawksworth, D. L. and F. Rose (1970). “Qualitative Scale for
McPherson, E.G. and J.R. Simpson. (2000). Carbon dioxide
estimating Sulphur Dioxide Air Pollution in England and
reductions through urban forestry: guidelines for professional
Wales using Epiphytic Lichens.” Nature 227(5254): 145–148.
and volunteer tree planters. PSW GTR-171. Albany, CA:
Heisler, G.M. (1986). Energy savings with trees. Journal of USDA Forest Service, Pacific Southwest Research Station
Arboriculture 12(5):113-125.
Muehlenbach, V. (1969). Along the railroad tracks. Missouri
Heisler, G.M. (1990). Mean wind speed below building Botanical Garden Bulletin 57 (30), 10–18.
height in residential neighborhoods with diffreent tree
National Academy of Sciences. (1977a). Effects of nitrogen
densities. American Society of Heating, Refrigerating, and
oxides on vegetation. In: Nitrogen Oxides. Washington, DC:
Air Conditioning Engineers (ASHRAE) Transactions 96 (1),
National Academy of Sciences:147–158.
1389–1396.
National Academy of Sciences. (1977b). Ozone and other
Heisler, G.H., Walton, J., et al. (2007). Empirical modeling and
photochemical oxidants. Washington, DC: National Academy
mapping of below-canopy air temperatures in Baltimore, MD
of Sciences. 789 pp.
and vicinity. In: Proceedings of Seventh Urban Environment
Symposium, sponsored by American Meteorological Society, National Acid Precipitation Assessment Program (NAPAP).
San Diego, CA. (1991). 1990 integrated assessment report. Washington, DC:
National Acid Precipitation Assessment Program. 520 pp.
Hope, D., Gries, C., et al. (2003). Socioeconomics drive urban
plant diversity. PNAS 100(15); 8788–8792. Nowak, D.J. (1994). Air pollution removal by Chicago’s urban
forest. In: McPherson, E.G, D.J. Nowak and R.A. Rowntree.
Iverson, L.R., Prasad, A.M. (2001). Potential changes in
Chicago’s Urban Forest Ecosystem: Results of the Chicago
tree species richness and forest community types following
Urban Forest Climate Project. USDA Forest Service General
climate change. Ecosystems 4, 186–199.
Technical Report NE-186. pp. 63–81.
Jovan, S., J. Riddell, et al. (2012). “Eutrophic lichens respond
Nowak, D.J. (2010). Urban biodiversity and climate change.
to multiple forms of N: implications for critical levels
In: Urban Biodiversity and Design. Muller, N., Werner, P. and
and critical loads research.” Ecological Applications 22(7):
Kelcey, J.G. (eds). Wiley-Blackwell Publishing. Hoboken, NJ.
1910–1922.
p. 101–117.
Kunzig AP, Warren P, et al. (2005). The effects of human
Nowak, D.J., Rowntree R.A., et al. (1996). Measuring and
socioeconomic status and cultural characteristics on urban
analyzing urban tree cover. Landscape and Urban Planning
patterns of biodiversity. Ecology and Society 10 (1): 23. [online]
36, 49–57.
ttp://www.ecologyandsociety.org/vol10/iss1/art23
Nowak, D.J., Civerolo K.L., et al. (2000). A modeling study of
Lefohn A.S., Lawrence J.A., et al, (1988). A comparison of
the impact of urban trees on ozone. Atmospheric Environment
indices that describe the relationship between exposure
34:1610–1613.
to ozone and reduction in the yield of agricultural crops.
Atmospheric Environment. 22:1229–1240. Nowak D.J., Noble, et al. (2001). Assessing the US urban
forest resource. Journal of Forestry 99 (3), 37–42.
Lerdau, M., Slobodkin, L. (2002) Trace gas emissions and
species dependent ecosystem services. TRENDS in Ecology & Nowak, D.J., Crane, D.E., et al. (2002). Brooklyn’s Urban
Evolution 17(7):309–312. Forest. USDA Forest Service Gen. Tech. Rep. NE-290. 107 p.
Linzon, S.N. (1978). Effects of airborne sulfur pollutants on Nowak D.J., Crane D.E., et al. (2006). Air pollution removal by
plants. In: Nriagu, J. O. ed. Sulfur in the environment: Part II: urban trees and shrubs in the United States. Urban Forestry
ecological impacts. New York: John Wiley and Sons:109–162. and Urban Greening 4:115–123.
Little, P. (1977). Deposition of 2.75, 5.0, and 8.5 mm particles Nowak, D.J., R.E. Hoehn, et al. (2008). A ground-based
to plant and soil surfaces. Environ. Pollut. 12:293–305. method of assessing urban forest structure and ecosystem
services. Arboriculture and Urban Forestry. 34(6): 347–358
Liu, X.-Y., H.-Y. Xiao, et al. (2011). “Physiological and isotopic
signals in epilithic mosses for indicating anthropogenic Nowak, D.J., Greenfield, E.J. (2012). Tree and impervious
sulfur on the urban–rural scale.” Ecological Indicators 11(5): cover in the United States. Landscape and Urban Planning
1245–1250. 107: 21– 30.

286 Connecting Global Priorities: Biodiversity and Human Health

Nowak D.J., Hirabayashi S., et al. (2013). Modeled PM2.5 Shafer, S.R., Heagle, A.S. (1989). Growth responses of field-
removal by trees in ten U.S. cities and associated health grown loblolly pine to chronic doses of ozone during multiple
effects. Environmental Pollution 178:395–402. growing seasons. Canadian Journal of Forestry 19: 821–831.
Nowak, D.J. Hirabayashi, S., et al. (2014). Tree and forest Smith, W.H. (1984). Pollutant uptake by plants. In: Treshow,
effects on air quality and human health in the United States. M. ed. Air pollution and plant life. New York: John Wiley and
Environmental Pollution 193:119–129. Sons: 417–450.
Numata, M. (1977). The impact of urbanization on vegetation Smith, W.H. (1990). Air pollution and forests. New York:
in Japan. In: Miyawaki, A. & Tuxen, R. (eds.) Vegetation Springer-Verlag. 618 p.
Science and Environmental Protection. Maruzen Co. Ltd.
Smith, A.E., Levenson, J.B. (1980). A Screening Procedure
Tokyo.
for the Impacts of Air Pollution Sources on Plants, Soils and
Nylander, W. (1866). Les lichens du jardin du Luxembourg Animals. EPA 450 / 2–81–078 US Environmental Protection
Bull. Soc. Bot. Fr. 13: 364–371. Agency. Research Triangle Park, NC. 124 p.
Office of Technology Assessment. (1989). Catching our Taha, H. (1996). Modeling impacts of increased urban
breath: next steps for reducing urban ozone. OTA-O-412. vegetation on ozone air quality in the South Coast Air Basin.
Washington, DC: Office of Technology Assessment. Atmos. Environ. 30(20):3423–3430.
Ogren, T.L. (2000). Allergy-Free Gardening. Ten Speed Press, Tingey, D.T., Turner, D.P., et al. (1991). Factors controlling
Berkeley, CA. the emissions of monoterpenes and other volatile organic
compounds. In: Sharkey, T.D., Holland, E.A., Mooney, H.A.
Pettyjohn M.E., Levetin, E. (1997). A comparative biochemical
eds. Trace gas emissions by plants. New York: Academic Press:
study of conifer pollen allergens. Aerobiologia 13; 259 -267
93–119.
Pope, C.A., Burnett, R.T., et al. (2002). Lung cancer,
Tiwary, A., Sinnett, D., et al. (2009). An integrated tool to
cardiopulmonary mortality, and long-term exposure to fine
assess the role of new plantings in PM10 capture and the
particulate air pollution. Journal of the American Medical
human health benefits: A case study in London. Environ.
Association 287(9):1132–1141.
Pollution 157: 2645–2653.
Powe, N.A.,Willis, K.G. (2004). Mortality and morbidity
Townsend, A.M. (1974). Sorption of ozone by nine shade
benefits of air pollution (SO2 and PM10) absorption
tree species. Journal of American Horticultural Science. 99(3):
attributable to woodland in Britain. J. Environ. Manage. 70:
206–208.
119–128.
U.S. Environmental Protection Agency. (1991). Non-road
Rennenberg, H. (1991). The significance of higher plants
engine and vehicle emission study-report. Report No. EPA
in the emission of sulfur compounds from terrestrial
460/3–91–02. U.S. Environmental Protection Agency, Office
ecosystems. In: Sharkey, T.D., Holland, E.A., Mooney, H.A.
of Mobile Services, Ann Arbor, MI.
eds. Trace gas emissions by plants. New York: Academic Press:
217–260. U.S. Environmental Protection Agency. (2010). Our nation’s
air: status and trends through 2008. EPA-454 / R-09–002.
Riddell, J., T. H. Nash Iii, et al. (2008). “The effect of HNO3
Office of Air Quality Planning and Standards. Triangle Park,
gas on the lichen Ramalina menziesii.” Flora – Morphology,
NC. 49 p.
Distribution, Functional Ecology of Plants 203(1): 47–54.
U.S. Environmental Protection Agency. (2014). Visibility.
Riddell, J., P. E. Padgett, et al. (2012). “Physiological responses
http://www.epa.gov/visibility/what.html [last accessed July
of lichens to factorial fumigations with nitric acid and ozone.”
2014]
Environmental Pollution 170(0): 202–210.
Vos, P.E.J., Maiheu, B., et al. (2013). Improving local air
Root, H. T., L. H. Geiser, et al. (2013). “A simple tool for
quality in cities: To tree or not to tree? Environmental Pollution
estimating throughfall nitrogen deposition in forests of
183: 113–122.
western North America using lichens.” Forest Ecology and
Management 306(0): 1–8. Wania, A., Bruse, M., et al. (2012). Analysing the influence
of different street vegetation on traffic-induced particle
Salmond, J.A., Williams, D.E., et al. (2013). The influence
dispersion using microscale simulations. Journal of
of vegetation on the horizontal and vertical distribution of
Environmental Management 94: 91–101.
pollutants in a street canyon. Science of the Total Environment
443: 287–298. Wolterbeek, B. (2002). “Biomonitoring of trace element
air pollution: principles, possibilities and perspectives.”
Schjoerring, J.K. (1991). Ammonia emission from the foliage
Environmental Pollution 120(1): 11–21.
of growing plants. In:Sharkey, T.D., Holland, E.A., Mooney,
H.A. eds. Trace gas emissions by plants. New York: Academic World Health Organisation (WHO), (2014). Burden of
Press: 267–292. disease from the joint effects of Household and Ambient Air
Pollution for 2012. WHO, Geneva. http://www.who.int/phe/
Seaward, M.R.D. (2002). Lichens as Monitors of
health_topics/outdoorair/databases/AP_jointeffect_BoD_
Radioelements. Monitoring with Lichens  – Monitoring
results_March2014.pdf (last accessed July 2014)
Lichens. P. Nimis, C. Scheidegger and P. Wolseley, Springer
Netherlands. 7: 85–96.

Connecting Global Priorities: Biodiversity and Human Health 287

 World Health Organisation (WHO), (2014a). 7 million Bassil KL, Vakil C, Sanborn M, Cole DC, Kaur JS, Kerr
premature deaths annually linked to air pollution. Press KJ. 2007. Cancer health effects of pesticides: systematic
release, 25th March 2014. http://www.who.int/mediacentre/ review. Can Fam Physician 53 (10): 1704–11. PMC 2231435.
news/releases/2014/air-pollution/en/ (last accessed July PMID  17934034. http://www.ncbi.nlm.nih.gov/pmc/
2014) articles/PMC2231435/ (24 July 2014).
World Health Organisation (WHO), (2014b). Household air Bebber DP, Ramotowski MAT, Gurr SJ. 2013. Crop pests
pollution and health. WHO Fact Sheet No. 292; March 2014. and pathogens move polewards in a warming world. Nature
http://www.who.int/mediacentre/factsheets/fs292/en/ (last Climate Change 3: 985–988.
accessed July 2014)
Benton Jones J.Jr. 2012. Inorganic Chemical Fertilizers and
Their Properties. In: Plant Nutrition and Soil Fertility Manual.
Chapter 5 Second Edition CRC Press. ISBN 978–1-4398–1609–7. eBook
ISBN 978–1-4398–1610–3.
Abate, T. A. van Huis, J.K.O. Ampof. 2000. Pest management
strategies in traditional agriculture: An African Perspective. Bharucha, Z. and Pretty, J. (2010) The roles and values of
wild foods in agricultural systems. Phil. Trans. R. Soc. B 365:
Abawi, G. S. and T. L. Widmer (2000). Impact of soil health 2913–2926
management practices on soilborne pathogens, nematodes
and root diseases of vegetable crops. Applied Soil Ecology, Bianchi, F.J.J.A., Booij, C.J.H. and T. Tscharntke (2006).
15(1), 37–47. Sustainable pest regulation in agricultural landscapes: a
review on landscape composition, biodiversity and natural
Adoukonou-Sagbadja H, Dansi A, Vodouhè R, Akpagana K pest control. Proceedings of the Royal Society B: Biological
(2006) Indigenous knowledge and traditional conservation Sciences, 273(1595), 1715–1727.
of fonio millet (Digitaria exilis, Digitaria iburua) in Togo.
Biodiversity and Conservation 15(8):2379–2395. Bita, C.E and t. Gerats (2013) Plant tolerance to high
temperature in a changing environment: scientific
Alavanja M.C.R. 2009. Pesticides Use and Exposure Extensive fundamentals and production of heat stress-tolerant crops.
Worldwide. Rev Environ Health. 24(4): 303–309. Available at: Frontiers in Plant Science, 4(237).
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2946087/
pdf/nihms-232681.pdf Bolognesi C. Genotoxicity of pesticides: a review of human
biomonitoring studies. Mutation Res. 2003;543:251–72.
Alexandratos, N. and J. Bruinsma (2012) World Agriculture http://www.ncbi.nlm.nih.gov/pubmed/12787816
Towards 2030/2050: The 2012 Revision. No 12–03, Rome
Food and Agriculture Organization Boshoff, W.H.P., Pretorius, Z.A. and Niekerk (2002).
Establishment, distribution and pathogenicity of Puccini
Altieri, M.A. and L.C. Merrick, 1987. In situ conservation of striiformis f. sp. tritici in South Africa. Plant Disease,
crop genetic resources through maintenance of traditional 86:485–492
farming systems. Economic Botany 41(1): 86--96.
Brush, S.B., 1999. Genes in the Field: On-Farm Conservation
Angelsen, A., Jagger, P., Babigumira, R., Belcher, B., Hogarth, of Crop Diversity. IPGRI/IDRC/Lewis, 288p.
NJ., Bauch, S., Borner, J., Smith-Hall, C., and Wunder, S.
(2014) Environmental income and rural livelihoods: a global Bunting and Ahmed (2014) Climate change and adaptation
comparative analysis. World Development. and prawn-fish-rice agroecosystems, Landscapes Blog
for People, Food and Nature http://blog.ecoagriculture.
Ashman, T.-L., Knight, T.M., Steets, J.A., Amarasekare, P., org/2014/07/14/climate-change-adaptation-and-prawn-
Burd, M., Campbell, D.R. et al. (2004). Pollen limitation of fish-rice-agroecosystems/
plant reproduction: ecological and evolutionary causes and
consequences. Ecology, 85, 2408–2421. Calderone, N.W. (2012). Insect pollinated crops, insect
pollinators and US agriculture: Trend analysis of aggregate
Barabasz W., Albińska D., Jaśkowska M., Lipiec J. 2002. data for the period 1992–2009. PLoS One, 7(5), e37235.
Biological Effects of Mineral Nitrogen Fertilization on Soil
Microorganisms. Polish Journal of Environmental Studies 11 Carr, J.A., Outhwaite, W.E., Goodman, G.L., Oldfield,
(3): 193–198. http://www.pjoes.com/pdf/11.3/193–198.pdf T.E.E. and Foden, W.B. 2013. Vital but vulnerable: Climate
change vulnerability and human use of wildlife in Africa’s
Baranski M., Dominika Srednicka-Tober, Nikolaos Volakakis, Albertine Rift. Occasional Paper of the IUCN Species
Chris Seal, Roy Sanderson, Gavin B. Stewart, Charles Survival Commission No. 48. IUCN, Gland, Switzerland and
Benbrook, Bruno Biavati, Emilia Markellou, Charilaos Cambridge, UK. xii + 224pp.
Giotis, Joanna Gromadzka-Ostrowska, Ewa Rembiałkowska,
Krystyna Skwarło-Son´ ta, Raija Tahvonen, Dagmar Carter, C. et al. (2007). Palm oil markets and future supply.
Janovska, Urs Niggli, Philippe Nicot and Carlo Leifert. Eur. J. Lipid Sci. Technol., 109 pp. 307–314
Higher antioxidant and lower cadmium concentrations and
Cassidy, E.S., West, P.C., Gerber, J.S. and J.A. Foley (2013).
lower incidence of pesticide residues in organically grown
Redefining agricultural yields: from tonnes to people
crops: a systematic literature review and meta-analyses.
nourished per hectare. Environmental Research Letters,
The British journal of nutrition 06/2014; DOI:  10.1017/
8:034015
S0007114514001366

288 Connecting Global Priorities: Biodiversity and Human Health

CBD (2014) Emerging key messages for the state of De Vendômois, J. S., Cellier, D., Vélot, C., Clair, E., Mesnage,
knowledge review on the interlinkages between biodiversity R., & Séralini, G. E. (2010). Debate on GMOs health risks
and human health. Subsidiary Body on Scientific, Technical after statistical findings in regulatory tests. International
and Technological Advice, Eighteenth meeting, Montreal, journal of biological sciences, 6(6), 590.
23–28 June 2014, Item 9.7 of the provisional agenda*.
Department of Environment, Food and Rural (2004). Making
Available at: http://www.cbd.int/doc/meetings/sbstta/sbstta-
space for water: Taking forward a new Government strategy
18/information/sbstta-18-inf-15-en.pdf
for flood and coastal erosion risk management in England.
Chen, X.M. (2005). Epidemiology and control of strip rust First Government Response to the Autumn 2004 Making
[Puccini striiformis f. sp. tritici] on wheat. Canadian Journal Space for Water Consultation Exercise.
of Plant Pathology, 27:314–337.
Döll, P., Siebert, S. (2002). Global modeling of irrigation water
Chung, A. Y. C., P. Eggleton, M. R. Speight, P. M. Hammond, requirements. Water Resources Research, 38(4), 8–1.
and V. K. Chey (2000). The diversity of beetle assemblages
Dona, A., & Arvanitoyannis, I. S. (2009). Health risks of
in different habitat types in Sabah, Malaysia. Bulletin of
genetically modified foods. Critical reviews in food science and
Entomological Research 90 : 475 – 496.
nutrition, 49(2), 164–175.
Clay, J.(2004) World Agriculture and the Environment: A
Donald, P.F. (2004). Biodiversity impacts of some agricultural
Commodity-by-Commodity Guide to Impacts and Practices.
commodity productions systems. Conservation Biology,
Island Press
18(1)18–37
Corley, R.H.V. and P.B. Tinker (2003). The Oil Palm. Blackwell
Eilers, E.J., Kremen, C., Greenleaf, S.S., Garber, A.K. and A-M.
Science
Klein (2011) Contribution of pollinator-mediated crops to
Cornell University. 2001a. Pesticide Applicator Core nutrients in the human food supply. PloS One 6(6): e21363
Tutorial. Module 4: Toxicity of pesticides. Pesticide Safety
Ellis, E.C, Goldewijk K.K, Siebert, S, Lightma, D, Ramankutty,
Education Program (PSEP). Pesticide Management Education
N, (2010). Anthropogenic transformation of the biomes,
Programme. http://psep.cce.cornell.edu/Tutorials/core-
1700–2000, Global Ecology and Biogeography, 19, 589–606.
tutorial/module04/index.aspx (24 July 2014)
Ellis, E.C and Ramankutty, N, (2008).Putting people in the
Cornell University. 2001b. Pesticide Applicator Core Tutorial.
map: anthropogenic biomes of the world. Frontiers in Ecology
Module 6: Ecology and environmental considerations.
and the Environment, 6 439–447.
Pesticide Safety Education Program (PSEP). Pesticide
Management Education Programme. Http://psep.cce.cornell. Eyzaguirre P.B. and Linares O.F. (eds) 2004. Home Gardens
edu/Tutorials/core-tutorial/module06/index.aspx (28 July and Agrobiodiversity. Smithsonian Institution. Washington.
2014). 296 pp.
Costa-Font, M., Gil, J. M., & Traill, W. B. (2008). Consumer FAO. (2015). Coping with climate change – the roles of
acceptance, valuation of and attitudes towards genetically genetic resources for food and agriculture. Rome.
modified food: Review and implications for food policy. Food
FAO. (2014). State of Food Insecurity in the World (SOFI
policy, 33(2), 99–111.
2014). Food and Agriculture Organization of the United
Council on Scientific Affairs, American Medical Association. Nations, Rome.
1997. Educational and Informational Strategies to Reduce
FAO (2012). Intergovernmental group on Tea: Current
Pesticide Risks. Preventive Medicine, 26, 2. Available
and medium term outlook for tea. Food and Agriculture
at: http://www.ingentaconnect.com/content/ap/
Organization of the United Nations, committee on
pm/1997/00000026/00000002/art00122%3Bjsessionid=p
Commodity problems, Kenya.
kwgpommd0xm.alexandra
FAO. (2011). The State of the World’s land and water resources
Cribb J. (2010) The Coming Global Famine: The Global Food
for food and agriculture: Managing systems at risks. Available
Crisis and What we Can Do to Avoid it. CSIRO Publishing
at: http://www.fao.org/nr/solaw/solaw-home/it/
Damalas, C. A.; Eleftherohorinos, I. G. 2011. Pesticide
FAO. (2010). The Second Report of the State of the
Exposure, Safety Issues, and Risk Assessment Indicators.
World’s Plant Genetic Resources for Food and Agriculture.
International Journal of Environmental Research and Public
Commission on Genetic Resources for Food and Agriculture.
Health 8 (12): 1402. doi:10.3390/ijerph8051402. Available at:
FAO. Rome
http://www.mdpi.com/1660–4601/8/5/1402 (28 July 2014)
FAO (2007) The State of the World’s Animal Genetic
De Clerck, F., Fanzo, J., Palm, C. and Remans, R. (2011)
Resources for Food and Agriculture, FAO, Rome.
Ecological approaches to human nutrition. Food and Nutrition
Bulletin 32: S41-S50. FAO (2006). Livestock’s long shadow: environmental issues
and options. Food and Agriculture Organization of the United
De Vallavieille-Pope, C. (2004). Management of disease
Nations, Rome.
resistance diversity of cultivars of a species in single fields:
Controlling epidemics. Comptes Rendus Biol. 327: 611–620.

Connecting Global Priorities: Biodiversity and Human Health 289

 FAO. (2003). International Code of Conduct on the Galuzzi, G., P. Eyzaguirre, and V. Negri. 2010. Home gardens:
Distribution and Use of Pesticides (Revised Version) adopted neglected hotspots of agrobiodiversity and cultural diversity.
by the Hundred and Twenty-third Session of the FAO Council Biodiversity and Conservation 19:3635--3654.
in November 2002. Food and Agriculture Organization of the
Gardiner, M.M., Landis, D.A., Gratton, C., DiFonzo, C.D.,
United Nations. Rome, Italy. 36 p. ftp://ftp.fao.org/docrep/
O’Neal, M., Chacon, J.M. and G.E. Heimpel (2009). Landscape
fao/005/y4544e/y4544e00.pdf (24 July 2014)
diversity enhances biological control of an introduced crop
FAO (2003). Summary of food and agricultural statistics. pest in the north-central USA. Ecological Applications, 19(1),
Rome: Food and Agriculture Organization of United Nations, 143–154.
Rome.
Garibaldi, Lucas A., Ingolf Steffan-Dewenter, Rachael Winfree,
Food and Agriculture Organization (FAO), (1996). List of Marcelo A. Aizen, Riccardo Bommarco, Saul A. Cunningham,
animal species used in aquaculture prepared by L Garibaldi. Claire Kremen et al. (2013). Wild pollinators enhance fruit
FAO Fisheries Circular No. 914. set of crops regardless of honey bee abundance.” Science 339,
no. 6127: 1608–1611.
FAO/PAR, (2011). Biodiversity for Food and Agriculture:
Contributing to food security and sustainability in a changing Gibbs, H.K., Ruesh, A.S., Achard, F., Clayton, M.K., Holmgren,
world. FAO, Rome. Pp. 66. P., Ramankutty, N and J.A.. Foley (2010) Tropical forests were
the primary sources of new agriucltural land in the 1980s and
Fenner-Crisp, PE. Risk-assessment and risk management: the
1990s. Proc. Natl. Acad. Sci. 107 (38): 16732–16737
regulatory process. 2001. In: Kreiger, R., editor. Handbook
of Pesticide Toxicology. 2nd Ed. Academic; San Diego: 2001. Gilden RC, Huffling K, Sattler B. 2010. Pesticides and health
p. 681–690. risks. J Obstet Gynecol Neonatal Nurs 39 (1): 103–10.
Finckh, M.R. and M.S. Wolfe. 2006. Diversification strategies. Glenn, E. P., Lee, C., Felger, R., and Zengel, S. (1996). Effects
Pp. 269--308 in The Epidemiology of Plant Disease (B.M. of water management on the wetlands of the Colorado River
Cooke et al. Eds.). Springer, NY, USA. delta, Mexico. Conservation Biology, 10(4), 1175–1186.
Flath, K. and G. Barthels (2002). Virulenzsituation Glor, R. E., A. S. Flecker, M. F. Benard, and A. G. Power. 2001.
in osterreichischen und deutschen Populationen des Lizard diversity and agricultural disturbance in a Caribbean
Weizengelbrostes. Bereicht uber die 52. Tagung der forest landscape. Biodiversity and Conservation 10: 711 – 723
Vereinigung der Pflanzenzuchter und Saatgutkaufleute
Godfray, C.H.J., Beddington, J.R., Crute, I.R., Haddad, L.,
Osterreichs, Gumpenstein, pp. 51–56
Lawrence, D., Muir, J.F., Pretty J., Robinson, S., Thomas, S.M.
Foley, J.A. DeFries, R., Asner, G.P., Barford, C., Bonan, G., and C. Toulmin (2010) Food security: the challenge of feeding
Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, 9 billion people. Science 327: 812
H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik,
Godfray, H.C.J. et al. (2010) The future of the global food
C.J., Monfreda, C.,. Patz, J.A, Prentice, I.C., Ramankutty, N.
system. Phil. Trans. R. Soc. B2010 365: 2769–2777.
and P.K. Snyder (2005). Global consequences of land use.
Science, 309: 570–574 Golden, C.D., Fernald, L.C.H., Brashares, J.S., Rasolofoniaina,
B.J.R. and Kremen, C. 2011. Benefits of wildlife consumption
Foley, Jonathan A., Navin Ramankutty, Kate A. Brauman,
to child nutrition in a biodiversity hotspot. Proceedings of the
Emily S. Cassidy, James S. Gerber, Matt Johnston, Nathaniel
National Academy of Sciences of the United States of America,
D. Mueller et al. (2011). “Solutions for a cultivated planet.”
108(49): 19653–19656. DOI:10.1073/pnas.1112586108.
Nature 478, no. 7369: 337–342.
Grau, H.R., Aide, T.M., Zimmerman, J.K., Thomlinson, J.R.,
Food and Agricultural Policy Research Institute, FAPRI
Helmer, E., and Zou, X. (2003). The ecological consequences
(2011). World Biofuels: FAPRI-ISU 2011 Agricultural Outlook
of socioeconomic and land-use changes in postagriculture
(www.fapri.iastate.edu/outlook/2011/)
Puerto Rico. BioScience, 53(12), 1159–1168
Food Composition. Global Progress Report 2012. Rome:
Green, R.E., Cornell, S.J., Scharlemann, J.P. and A. Balmford
FAO. Available at: http://www.fao.org/infoods/infoods/
(2005) Farming and the fate of wild nature. Science 307, 550
food-biodiversity/en/
Grigg, D. B. (1974) The growth and distribution of the world’s
Fox, JE, Gulledge, J, Engelhaupt, E, Burrow, ME, and
arable land 1870–1970, Geography, 59, 104–110.
McLachlan, JA. 2007. Pesticides reduce symbiotic efficiency
of nitrogen-fixing rhizobia and host plants. Proceedings Grube A., Donaldson D., Kiely T, WuUS L. 2011. 2011.
of the National Academy of Sciences of the USA 104 (24): Pesticides Industry Sales and Usage: 2006 and 2007 Market
10282–10287. Available at: http://www.ncbi.nlm.nih.gov/ Estimates. US Environmental Protection Agency (EPA).
pmc/articles/PMC1885820/ Washington DC. 33 p. Available at: http://www.epa.gov/
opp00001/pestsales/07pestsales/market_estimates2007.
Frison, E. A., Cherfas, J., and Hodgkin, T. (2011). Agricultural
pdf (29 July 2014)
biodiversity is essential for a sustainable improvement in
food and nutrition security. Sustainability, 3(1), 238–253. Hajjar, R. and Hodgkin, T. (2007). The use of wild relatives in
crop improvement: a survey of developments over the last 20
Gallai, N., Salles, J.-M., Settele, J. and B.E. Vaissière (2009)
years. Euphytica 156: 1 – 13.
Economic valuation of the vulnerability of world agriculture
confronted with pollinator decline. Ecological Economics,
Volume 68, 3(15): 81–821

290 Connecting Global Priorities: Biodiversity and Human Health

Halwart, M. (2013) Valuing aquatic biodiversity in Hunter, D. and Heywood V.H. (eds) (2011) Crop Wild
agricultural landscapes. In: Fanzo, J. and Hunter, D. Borelli, Relatives; A Manual of In Situ Conservation. Issues in
T. and Mattei, F. (eds) Diversifying Food and Diets: Using Agricultural Biodiversity, Earthscan, UK. 414pp
Agricultural Biodiversity to Improve Nutrition and Health. Issues
Husband, B.C. and D.W. Schemske (1996). Evolution of the
in Agricultural Biodiversity, Earthscan, UK.
magnitude and timing of inbreeding depression in plants.
Halwart, M. (2006). Biodiversity and nutrition in rice-based Evolution, 50, 54–70.
aquatic ecosystems. Journal of Food Composition and
Ibragimov, N., Evett, S. R., Esanbekov, Y., Kamilov, B. S.,
Analysis, 19(6), 747–751.
Mirzaev, L., and Lamers, J. (2007). Water use efficiency
Halwart, M. and Bartley, D. (eds.). 2005. Aquatic biodiversity in of irrigated cotton in Uzbekistan under drip and furrow
rice-based ecosystems. Studies and reports from Cambodia, China, irrigation. Agricultural water management, 90(1), 112–120.
Lao PDR and Viet Nam. [CD-ROM]. Rome, FAO. Also available
Iosefa, T., Taylor, M., Hunter, D. and Tuia, V (2013). Supporting
at ftp://ftp.fao. org/FI/CD-Rom/AqBiodCD20Jul2005/Start.
farmers’ access to the global gene pool and participatory
pdf
selection in taro in the Pacific. In, De Boef, W.S., N. Peroni, A.
Henry, M.; Beguin, M.; Requier, F.; Rollin, O.; Odoux, J. Subedi and M.H. Thijssen (eds.) 2013. Community Biodiversity
-F.; Aupinel, P.; Aptel, J.; Tchamitchian, S.; Decourtye, A. Management: Promoting Resilience and the Conservation
2012. A Common Pesticide Decreases Foraging Success of Plant Genetic Resources. Earthscan, UK p. 285–289
and Survival in Honey Bees. Science 336 (6079): 348–350. Iris Macfarlane (2004). The Empire of Tea. The Overlook Press.
doi:10.1126/science.1215039. http://www.sciencemag.org/ p. 32.
content/336/6079/348 (28 July 2014)
Jackson L.E., Burger M., Cavagnaro T.R. 2008. Roots,
Heywood, V. (2013) Overview of agricultural biodiversity and Nitrogen Transformations, and Ecosystem Services. Annual
its contribution to nutrition and health, In: Fanzo, J. and Review of Plant Biology 59: 341–363. DOI: 10.1146/annurev.
Hunter, D. Borelli, T. and Mattei, F. (eds) Diversifying Food arplant.59.032607.092932. http://www.annualreviews.org/
and Diets: Using Agricultural Biodiversity to Improve Nutrition doi/abs/10.1146/annurev.arplant.59.032607.092932
and Health. Issues in Agricultural Biodiversity, Earthscan, UK.
Jaggard K.W. et al (2010) Possible changes to arable crop
Hodgkin, T. And Bordoni, P. (2012) Climate change and the yields by 2050. Philosophical Transactions of the Royal
conservation of plant genetic resources. Journal of Crop Society; Biological Sciences 365: 2835–2851
Improvement 26: 329–345
Jarvis D., Fadda C., De Santis P., Thompson J. (eds) 2012.
Hoehn, P., Tscharntke, T., Tylianakis, J. M. and I. Steffan- Damage, diversity and genetic vulnerability: the role of
Dewenter (2008) Functional group diversity of bee pollinators crop genetic diversity in the agricultural production system
increases crop yield. Proceedings of the Royal Society B: Biological to reduce pest and disease damage. Proceedings of an
Sciences, 275(1648), 2283–2291. international symposium, 15–17 February 2011, Rabat,
Morocco. Bioversity International. Rome, Italy.
Holstein Assoc. USA (1986). Holstein Type-Production Sire
Summaries. Holstein Association USA, Brattleboro, VT. Jarvis, A. Lane A. Hijmans R. 2008. The effect of climate
change on crop wild relatives. Agriculture, Ecosystems and
Holt-Giménez, E. (2002). Measuring farmers’ agroecological
Environment 126: 13–23
resistance after Hurricane Mitch in Nicaragua: a case study
in participatory, sustainable land management impact Jarvis, D., Hodgkin, T., Bhuwon, S., Fadda, C. and Lopez
monitoring. Agriculture, Ecosystems and Environment, 93(1), Noriega, I. (2011). A heuristic framework for identifying
87–105. multiple ways of supporting the conservation and use of
traditional crop varieties within the agricultural production
Horrigan, L., Lawrence, R. S., & Walker, P. (2002). How
systems. Critical Reviews in Plant Sciences 30:125–176. DOI:
sustainable agriculture can address the environmental and
10.1080/07352689.2011.554358
human health harms of industrial agriculture. Environmental
health perspectives, 110(5), 445. Jarvis, D.I., T. Hodgkin, B.R. Sthapit, C. Fadda, and I. Lopez-
Noriega, 2011. An heuristic framework for identifying
Hovmoller, M.S. and A.F. Justesen (2007) Appearance and
multiple ways of supporting the conservation and use of
interpretation of atypical phenotypes of Puccini striiformis
traditional crop varieties within the agricultural production
f. sp. tritici in NW-Europe. Australian Journal of Agricultural
system. Critical Reviews in Plant Science 30(1--2):125--176.
Research, 58:518–524.
Jeyaratnam J. 1990. Acute pesticide poisoning: a major
Hovmoller,M.S., Yahyaoui, A.H., Milus, E.S and A. Justesen
global health problem. World Health Stat Q 43 (3):139–
(2008). Rapid global spread of two aggressive strains of a
144. [PubMed: 2238694] http://www.ncbi.nlm.nih.gov/
wheat rust fungus. Molecular Ecology, online.
pubmed/2238694
Hunter, D. and Fanzo, J. (2013) Agricultural biodiversity,
Johns, T. and Maundu, P. (2006) Forest biodiversity, nutrition
diverse diets and improving nutrition. In, Diversifying Food
and population health in market-oriented food systems.
and Diets: Using Agricultural Biodiversity to Improve Nutrition
Unasylva 57: 34–40
and Health (Fanzo, J. and Hunter, D. et al eds) Issues in
Agricultural Biodiversity, Earthscan, UK p. 1–13 Johnson R.C. (1996). “Borrelia”. In Baron S., et al. Baron’s
Medical Microbiology (4th ed.). University of Texas Medical
Branch.

Connecting Global Priorities: Biodiversity and Human Health 291

 Johnston, AE. 1986. Soil organic-matter, effects on soils and Kremen, C. and A. Miles (2012) Ecosystem services in
crops. Soil Use Management 2 (3): 97–105. biologically diversified versus conventional farming systems:
Benefits, externalities and trade-offs. Ecology and Society
Jones, K.M., Specio, S.E., Shrestha, P., Brown, K.H. and
17(4): 40.
Allen, L.H. 2005. Nutrition knowledge and practices,
and consumption of vitamin a rich plants by rural Nepali Kremen, C., Iles, A. and C. Bacon. (2012). Diversified farming
participants and nonparticipants in a kitchen-garden systems: an agroecological, systems-based alternative to
program. Food and Nutrition Bulletin, 26(2): 198–208. modern industrial agriculture. Ecology and Society, 17(4): 44.
Jurewicz J., Hanke W. 2008. Prenatal and childhood exposure Lake R. et al. (2012) Climate change and food security:
to pesticides and neurobehavioral development: review of health impacts in developed countries. Environmental Health
epidemiological studies. Int J Occup Med Environ Health 21 Perspectives 120: 1520–1526
(2): 121–32.
Lamberth, C.; Jeanmart, S.; Luksch, T.; Plant, A. 2013. Current
Kahane, R., Hodgkin, T., Jaenicke, H., Hoogendoorn, Challenges and Trends in the Discovery of Agrochemicals.
C., Hermann, M., Keatinge, J. D. H., d’Arros Hughes, J., Science 341 (6147): 742–746. doi:10.1126/science.1237227.
Padulosi S., and N. Looney (2013). Agrobiodiversity for http://www.sciencemag.org/content/341/6147/742 (28 July
food security, health and income. Agron. Sustain. Dev. 2014)
DOI 10.1007/s13593–013–0147–8.
Lee, K.H., Isenhart, T.M. and R.C. Schultz (2003). Sediment
Kearns, C., Inouye, D. and N. Waser (1998). Endangered and nutrient removal in an established multi-species riparian
mutualisms: the conservation of plant–pollinator buffer. Journal of Soil and Water Conservation, 58(1), 1–8.
interactions. Annu. Rev. Ecol. Syst., 29, 83–112.
Letourneau, D. K., & Burrows, B. E. (Eds.). (2010). Genetically
Kellogg RL, Nehring R, Grube A, Goss DW, and Plotkin engineered organisms: assessing environmental and human
S. 2000. Environmental indicators of pesticide leaching health effects. CRC press.
and runoff from farm fields. United States Department of
Lin B. (2011) Resilience in agriculture through crop
Agriculture Natural Resources Conservation Service. http://
diversification: adaptive management for environmental
www.nrcs.usda.gov/wps/portal/nrcs/detail/national/
change. Bioscience 61: 183–193.
technical/?cid=nrcs143_014053 (28 July 2014)
Lira R. et al 2009. The effect of climate change on the
Khoury, C.K., Bjorkman, A.D., Dempewolf, H., Ramirez-
geographic distribution of Mexican wild relatives of
Villegas, J., Guarino, L., Jarvis, A., Riesenberg, L.H. and P.C.
domesticated Cucurbitaceae. Genetic Resources and Crop
Struik (2014). Increasing homogeneity in global food supplies
Evolution 56: 691–703.
and the implications for food security. Proc. Natl. Acad. Sci.
online. Lobell, D. B., Cassman, K. G., and Field, C. B. (2009). Crop
yield gaps: their importance, magnitudes, and causes. Annual
Kohler, H. -R and R. Triebskorn (2013). Wildlife Ecotoxicology
Review of Environment and Resources, 34(1), 179.
of Pesticides: Can We Track Effects to the Population Level
and Beyond? Science 341 (6147): 759. Lockie, S. And Carpenter, D. (2010) Agriculture, Biodiversity
and Markets. Earthscan.
Klein, A.M., Steffan–Dewenter, I. and T. Tscharntke (2003)
Fruit set of highland coffee increases with the diversity of Lotter DW, Seidel R, and Liebhardt W. 2003. The performance
pollinating bees. Proceedings of the Royal Society of London. of organic and conventional cropping systems in an extreme
Series B: Biological Sciences, 270(1518), 955–961. climate year. American Journal of Alternative Agriculture 18
(03): 146–154.
Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter,
I., Cunningham, S.A., Kremen, C. and T. Tscharntke (2007) Lundqvist, J., C. de Fraiture and D. Molden. Saving Water:
Importance of pollinators in changing landscapes for world From Field to Fork – Curbing Losses and Wastage in the Food
crops. Proceedings of the Royal Society B: Biological Sciences, Chain. SIWI Policy Brief. SIWI, 2008
274(1608), 303–313
MA, 2005. Ecosystems and Human Well-being: Synthesis.
Knobeloch L., Salna B., Hogan A., Postle J., Anderson H. 2000. In Millennium Ecosystem Assessment. Washington, DC: Island
Blue Babies and Nitrate-Contaminated Well Water. Environ Press.
Health Perspect 108:675–678. http://www.co.portage.wi.us/
Malaza, M.,and P.L. Howard, (2003). Modernization and
Groundwater/undrstnd/blbaby.htm (29 July 2014)
gender dynamics in the loss of agrobiodiversity in Swaziland’s
Koh L.P. (2007). Potential habitat and biodiversity losses food system. Women and plants: Gender relations in biodiversity
from intensified biodiesel feedstock production. Conservation management and conservation, 243–257.
Biology, 21: 1373–1375.
Maus, C. (2003). Safety of imidacloprid seed dressing to
Kothari, A. and Cooney, R., Hunter, D., McKinnon, K., honey bees: a comprehensive overview and compilation of
Muller, E., Nelson, F., Oli, K., Pandey, S., Rasheed, T. the current state of knowledge. Bulleting of Insectology 56:
and Vavrova, L. (2014) ‘Chapter 25, Resource Use and 51–58.
Development’ in Worboys, G.L., Lockwood, M., Kothari, A.,
McMichael, A. J., Powles, J. W., Butler, C. D., & Uauy, R.
Feary, S. and Pulsford, I. (eds) Protected Area Governance
(2007). Food, livestock production, energy, climate change,
and Management, Australian National University Press,
and health. The lancet, 370(9594), 1253–1263.
Canberra, Australia.

292 Connecting Global Priorities: Biodiversity and Human Health

Micronutrient Initiative (2009) Investing in the Future: A Padulosi S., D. Hunter, A. Jarvis and V. Heywood (2011)
united call to action on vitamin and mineral deficiencies Underutilized crops and climate change – current status and
[www.unitedcalltoaction.org] outlook. In, Crop Adaptation to Climate Change (S. Yadav, B.
Redden, J.L. Hatfield and H. Lotze-Campen, eds). Wiley-
Millennium Ecosystem Assessment (MA) (2005) Ecosystems
Blackwell, Ames Iowa, USA. pp. 507–521.
and Human Well-being – Health Synthesis.
Pan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E.,
Mitchell, M.G., Bennett, E.M. and A. Gonzalez (2014). Forest
Kurz, W. A., ... and Hayes, D. (2011). A large and persistent
fragments modulate the provision of multiple ecosystem
carbon sink in the world’s forests. Science, 333(6045),
services. Journal of Applied Ecology. online.
988–993.
Myers S. S., Zanobetti, A., Kloog, I., Huybers, P., Leakey, A. D.,
Papendick RI, Elliott LF, Dahlgren RB.1986. Environmental
Bloom, A. J., et al. (2014) Increasing CO2 threatens human
consequences of modern production agriculture: How can
nutrition. Nature 510 (7503), 139–142.
alternative agriculture address these issues and concerns?
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da American Journal of Alternative Agriculture, Volume 1, Issue
Fonseca, G. A.and J. Kent (2000). Biodiversity hotspots for 1, Pages 3–10. http://eap.mcgill.ca/MagRack/AJAA/AJAA_1.
conservation priorities. Nature, 403(6772), 853–858. htm (28 July 2014)
Myhre G. and D. Shindell (2013). Anthopogenic and Natural Patz, J.A., Daszak, P., Tabor, G.M., et al. (2004). “Unhealthy
Radiative Forcing. Intergovernmental Panel on Climate landscapes: Policy recommendations on land use change and
Change, Cambridge UK. 124 pp. infectious disease emergence” Environ. Health Perspect. 112
(10): 1092–98.
National Park Service. US Department of the Interior. (Page
last updated in 2014). Sequoia and Kings Canyon National Pejchar, L., & Mooney, H. A. (2009). Invasive species,
Park: Air quality – Airborne synthetic chemicals. Nps.gov. ecosystem services and human well-being. Trends in ecology
http://www.nps.gov/seki/naturescience/air_synthchem. & evolution, 24(9), 497–504.
htm (28 July 2014)
Pereira, H.M. et al. 2005. Condition and trends of ecosystem
Naug, D. (2009) Nutritional stress due to habitat loss services and biodiversity. In Capistrano, Doris et al. eds.
may explain recent honeybee colony collapse. Biological Millennium Ecosystem Assessment. Washington, USA, pp.
Conservation 142.10: 2369–2372 .: Island Press, pp. 171–203.
New Zealand Nutrition Survey (2011) (http:// Phipps, R. H., & Park, J. R. (2002). Environmental benefits of
w w w. s c i e n c e m e d i a c e n t r e . c o . n z / 2 0 1 1 / 0 9 / 1 5 / genetically modified crops: global and European perspectives
new-zealand-diet-and-nutrition-survey-experts-respond/) on their ability to reduce pesticide use. Journal of Animal and
Feed Sciences, 11(1), 1–18.
Nielsen, J., Haselow, N., Osei, A. and Talukder, Z. (2013)
Diversifying diets: using agricultural biodiversity to improve Pinstrup-Andersen, P. (2009) Food security: definition and
nutrition and health in Asia. In: Fanzo, J. and Hunter, D. measurement. Food Security 1: 5–7.
Borelli, T. and Mattei, F. (eds) Diversifying Food and Diets: Using
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P.,
Agricultural Biodiversity to Improve Nutrition and Health. Issues
Schweiger and W.E. Kunin (2010). Global pollinator declines:
in Agricultural Biodiversity, Earthscan, UK. pp 257–269.
trends impacts and drivers. Trends in Ecology and Evolution,
Notter, D. R. (1999). The importance of genetic diversity in 25(6): 345–353.
livestock populations of the future. Journal of Animal Science,
Power, A. G., and A. S. Flecker (1998). Agroecosystems and
77(1), 61–69.
biodiversity. Proceedings of the Smithsonian Migratory Bird
Ohio State University. 1999. Evergreens Help Block Center cacao conference. Available at: http://nationalzoo.
Spread Of Pesticide From Crop Fields. ScienceDaily. si.edu/conservationandscience/migratorybirds/research/
ScienceDaily, 19 November 1999. www.sciencedaily.com/ cacao/papers.cfm
releases/1999/11/991119075237.htm. (30 July 2014)
Prescott-Allen, R and C Prescott-Allen, 1990. How Many
Oliver, D.M., Heathwaite, L., Haygarth, P.M. and C.D. Clegg Plants Feed the World? Conservation Biology, 4; 365–374.
(2005). Transfer of Escherichia coli to water from drained and
Pretty, J., and Z. P. Bharucha, 2014. Sustainable intensification
undrained grassland after grazing. Journal of Environmental
in agricultural systems. Ann. Bot. 114 (8): 1571–1596.
Quality, 34 (2005), pp. 918–925
Priyadarshi A, Khuder SA, Schaub EA, Shrivastava S. 2000.
Osborne, L. L. and D. A. Kovacic, (1993). Riparian vegetated
A meta-analysis of Parkinson’s disease and exposure to
buffer strips in water-quality restoration and stream
pesticides. Neurotoxicology. 21(4):435–40. http://www.ncbi.
management. Freshwater biology, 29(2), 243–258.
nlm.nih.gov/pubmed/11022853
Padulosi S, Hodgkin T, Williams JT, Haq N (2002)
Underutilized crops: trends, challenges and opportunities in
the 21st century. In: Engels JMM, Ramanatha Rao V, Brown
AHD, Jackson MT (eds) Managing plant genetic resources.
CAB International, Wallingford, pp. 323–338.

Connecting Global Priorities: Biodiversity and Human Health 293

 Pudasaini, R., Sthapit, S., Suwal, R. Sthapit, B. (2013) The Rudel, T. K., Coomes, O. T., Moran, E., Achard, F., Angelsen,
role of integrated home gardens and local, neglected and A., Xu, J. And Lambin, E. (2005). Forest transitions: towards a
underutilized plant species in food security in Nepal and global understanding of land use change. Global Environmental
meeting the Millennium Development Goal 1. In: Fanzo, J. Change, 15(1), 23–31.
and Hunter, D. Borelli, T. and Mattei, F. (eds) Diversifying Food
Sampson, R.N.l. et al. (2005) Millennium Ecosystem
and Diets: Using Agricultural Biodiversity to Improve Nutrition
Assessment, Chapter 9: Timber, Fuel, and Fiber. Millennium
and Health. Issues in Agricultural Biodiversity, Earthscan, UK.
Ecosystem Assessment
pp 257–269.
Sanborn M., Bassil K., Vakil C., Kerr K., Ragan K. 2012.
Pushpakumara et al (2012) A review of research on home
Systematic Review of Pesticide Health Effects. Ontario College
gardens in Sri Lanka: the status, importance and future
of Family Physicians (OCFP). 83 p. http://ocfp.on.ca/docs/
perspective. Tropical Agriculturalist, 160: 55–125
pesticides-paper/2012-systematic-review-of-pesticide.pdf
Rahman, A.K.A. (1989) Freshwater Fishes of Bangladesh,
Sanborn M, Kerr KJ, Sanin LH, Cole DC, Bassil KL, Vakil
Zoological Society of Bangladesh, Dhaka
C. 2007. Non-cancer health effects of pesticides: systematic
Ramankutty, N. and J. Foley (1998) Characterizing patterns review and implications for family doctors. Can Fam Physician
of global land use: An analysis of global croplands data, Global 53 (10): 1712–20. PMC 2231436. PMID 17934035. http://
Biogeochem. Cycles, 124, 667–685. www.ncbi.nlm.nih.gov/pmc/articles/PMC2231436/ (24 July
2014)
Ramankutty, N. and J. Foley (1999). Estimating historical
changes in global land cover: Croplands from 1700 to 1992. Sanborn M., Cole D., Kerr K., Vakil C., Sanin L.H., Bassil
Global Biogeochemical Cycles, 13(4): 997–1027. K. 2004. Pesticides Literature Review: Systematic Review
of Pesticide Human Health Effects. The Ontario College of
Randall C. (ed.), et al. 2013. National Pesticide Applicator
Family Physicians. Toronto. 177 pp. Available at: https://
Certification Core Manual. National Association of State
www.premierinc.com/epp/downloads/01-systematic-review-
Departments of Agriculture Research Foundation.
canada-pesticides.pdf
Washington DC. 224 p. http://www.nasda.org/9381/
Foundation/11379/11383/6684.aspx (24 July 2014). Sanchez, P., Swaminathan, M.S., Dobie, P. and N. Yuksel. UN
Millennium Project 2005. Halving Hunger: It can be done.
Ratnieks, F. L., and Carreck, N. L. (2010). Clarity on honey
Task Forces on Hunger.
bee collapse?. Science, 327(5962), 152–153.
Scherr, S. J. and McNeely, J.A., 2008. Biodiversity
Reimer, A.P. and Prokopy, L.S. (2012). Environmental
conservation and agricultural sustainability: towards a new
attitudes and drift reduction behavior among commercial
paradigm of ‘ecoagriculture’ landscapes. Phil. Trans. R. Soc.
pesticide applicators in a US agricultural landscape. Journal
B (2008) 363, 477–494.
of Environmental Management, 30 (113): 361–9.
Schindler D. W., Hecky R.E. 2009. Eutrophication: More
Reynolds M.P. and Ortiz, R. (2010) Adapting crops to climate
Nitrogen Data Needed. Science 324 (5928): 721–722. DOI:
change: a summary. In, Climate change and Crop Production,
10.1126/science.324_721b http://www.sciencemag.org/
Edited M.P. Reynolds, 1–8. CABI
content/324/5928/721.2.full%20-%20R1
Richards, J. F. (1990) Land transformation, The Earth as
Scoones et al. (1992) Hidden Harvest: Wild Foods in
Transformed by Human ActionB. L. Turner, et al. 163–178,
Agricultural Systems. IIED, UK
Cambridge Univ. Press, New York.
Securing Soil Carbon Benefits. Available at: http://www.unep.
Ricketts, T.H. (2004) Tropical forest fragments enhance
org/yearbook/2014/PDF/chapt9.pdf
pollinator activity in nearby coffee crops. Conservation Biology,
18(5), pp.1262–1271. Self J.R. and Waskom R.M. 2013. Nitrates in Drinking
Water. Crop Series, Soil. Fact Sheet No. 0.517. Colorado State
Ricketts, T.H., Regetz, J. Steffan-Dewenter, I., Kremen, C.,
University Extension, USA. 2p. http://www.ext.colostate.
Bogdanski, A., Gemmil-Herren, B., Greenleaf, S.S., Klein
edu/pubs/crops/00517.pdf
A.-M., Mayfield, M.M., Morandin, L.A., Ochieng, A. and B.F.
Viana (2008). Landscape effects on crop pollination services: Shiklomanov, I. A., (Ed.), Assessment of Water Resources and
are there general patterns? Ecology letters, 11(5), pp.499–515. Water Availability in the World, Comprehensive Assessment
of the Freshwater Resources of the World, Stockholm
Robertson, C. J. (1956) The expansion of the arable area,
Environment Institute, Stockholm, 1997.
Scott. Geogr. Mag., 721, 1–20,
Shvidenko, A., Barber, C.V.and R. Persson (2005) Millennium
Rockstrom J. et al. 2009. A safe operating space for humanity.
Ecosystem Assessment, Chapter : Forest and Woodland
Nature 461, 472–475
Systems. Millennium Ecosystem Assessment
Rosenzweig, C., Iglesias, A., Yang, X. B., Epstein, P. R., and
Smale M, Hazell P, Hodgkin T, Fowler C (2009) Do we have
Chivian, E. (2001). Climate change and extreme weather
an adequate global strategy for securing the biodiversity of
events; implications for food production, plant diseases, and
major food crops? In: Kontoleon A, Pascual U, Smale M (eds)
pests. Global change and human health, 2(2), 90–104.
Agrobiodiversity conservation and economic development.
Rosin, C., Stock, P. and Campbell, H. (2012) Food Systems Routledge, Abingdon, pp 40–50.
Failure: The Global Food Crisis and the Future of Agriculture.
Earthscan from Routledge

294 Connecting Global Priorities: Biodiversity and Human Health

Smith, P. and M. Bustamante (2013) Mitigation of Climate Tyler Miller G. 2004. Sustaining the Earth: An Integrated
Change: Chapter 11 Agriculture, Forest and Other Land Uses. Approach. Thomson/Brooks/Cole. pp.  211–216.
Intergovernmental Panel on Climate Change, Cambridge,UK. ISBN 978–0-534–40088–0.
Steffen, W., Richardson, K., Rockström, J., Cornell, S. E., U.S. Environmental Protection Agency. 2007. Pesticides:
Fetzer, I., Bennett, E. M., et al. (2015). Planetary boundaries: Health and Safety. National Assessment of the Worker
Guiding human development on a changing planet. Science, Protection Workshop #3. Avaiable at: http://www.epa.gov/
1259855. oppfead1/safety/newnote/workshop3.htm (24 July 2014)
Stewart, W.M.; Dibb, D.W.; Johnston, A.E.; Smyth, T.J. 2005. U.S. Environmental Protection Agency, 2007. Setting
The Contribution of Commercial Fertilizer Nutrients to tolerances for pesticide residues in foods. Available at: http://
Food Production. Agronomy Journal 97: 1–6. doi:10.2134/ www.epa.gov/pesticides/factsheets/stprf.htm
agronj2005.0001. Available at: https://www.agronomy.org/
UNEP 2014. UNEP Year Book 2014 emerging issues update.
publications/aj/abstracts/97/1/0001(29 July 2014)
Chapter 1: Excess Nitrogen in the Environment. Available at:
Stewart, C. N., Halfhill, M. D., & Warwick, S. I. (2003). http://www.unep.org/yearbook/2014/PDF/chapt1.pdf
Transgene introgression from genetically modified crops to
UNEP 2014. UNEP Year Book 2014 emerging issues update.
their wild relatives. Nature Reviews Genetics, 4(10), 806–817.
Chapter 9:
Stoate, C., Boatman, N.D., Borralho, R.J., Carvalho, C.,
UNEP. 2013. UNEP year book 2013: Emerging issues in our
De Snoo, G.R. and P. Eden (2001). Ecological impacts of
global environment. Chapter: Reaching for the 2020 Goal:
arable intensification in Europe. Journal of environmental
The need for better information and sound management to
management, 63(4), 337–365.
minimize chemical risks. Available at: http://www.unep.org/
Stockholm Convention On Persistent Organic Pollutants. yearbook/2013/pdf/Minimizing_chemical_risks.pdf
Available at: http://chm.pops.int/Portals/0/Repository/
UNEP. 2012. UNEP Year Book 2012: The Benefits of Soil
convention_text/UNEP-POPS-COP-CONVTEXT-FULL.
Carbon: Managing soils for multiple economic, societal and
English.PDF (24 July 2014)
environmental benefits. Available at: http://www.unep.org/
Sunderland, K. and F. Samu (2000). Effects of agricultural yearbook/2012/pdfs/UYB_2012_CH_2.pdf
diversification on the abundance, distribution, and
UNEP. 2005. Ridding the world of POPS: A guide to the
pest control potential of spiders: a review. Entomologia
Stockholm Convention on Persistent Organic Pollutants.
Experimentalis et Applicata, 95(1), 1–13.
Secretariat of the Stockholm Convention on Persistent
Thies, C. and T. Tscharntke (1999). Landscape structure and Organic Pollutants. United Nations Environment Programme.
biological control in agroecosystems. Science, 285(5429), Switzerland. 17 p. http://www.pops.int/documents/
893–895. guidance/beg_guide.pdf (24 July 2014)
Tilman, D., Balzer C., Hill, J. and B.L. Befort (2011) United States Census Bureau, USCB (2013) U.S. Census
Global food demand and the sustainable intensification of Bureau – World POPClock Projection. July 2012–July 2013
agriculture. Proc. Natl. Acad. Sci. 108: 20260–4. data
Tilman, D. , Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., United States Department of Agriculture, USDA (2002).
Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D. Statistics of grain and feed Agricultural Statistics. Washington,
and D. Swackhamer (2001) Forecasting agriculturally driven D.C: USDA National Agricultural Statistics Service
global environmental change. Science, 292: 281–284 (NASS) pp 1–47 (www.nass.usda.gov/Publications/Ag_
Statistics/2002/02_ch1.pdf
Tirado M.C. et al. (2010) Climate change and food safety: a
review. Food Research International 43: 1745 – 1765 Walley F, Taylor A and Lupwayi N. 2006. Herbicide effects on
pulse crop nodulation and nitrogen fixation. FarmTech 2006
Tisdell, C. (2003). Socioeconomic causes of loss of animal
Proceedings 121–123.
genetic diversity: analysis and assessment. Ecological
Economics, 45(3), 365–376. Wellings, C.R., Wright, D.G., Keiper, F. and R. Loughman
(2003). First detection of wheat stripe rust in Western
Toledo, A. And Burlingame, B. (2006) Biodiversity and
Australia – possible means of entry and implications for plant
nutrition: a common path toward global food security and
quarantine. Plant Pathology, 36: 239–241
sustainable development. Journal of Food Composition and
Analysis 19: 477–483. Westphal, C., Steffan, Dewenter, I. and T. Tscharntke (2003).
Mass flowering crops enhance pollinator densities at a
Tooker, J F. and S. D Frank (2012). Genotypically diverse
landscape scale. Ecology Letters, 6(11), 961–965.
cultivar mixtures for insect pest management and increased
crop yields. J of Applied Ecology. 49:974–985. Wezel, A., Bellon, S., Doré, T., Francis, C., Vallod, D. and C.
David (2009) Agroecology as a science, a movement and a
Tscharntke, T., Clough, Y., Wanger, T. C., Jackson, L.,
practice. A review. Agron Sustain. Dev. 29, 503–515.
Motzke, I., Perfecto, I., ... and Whitbread, A. (2012). Global
food security, biodiversity conservation and the future of
agricultural intensification. Biological Conservation, 151(1),
53–59.

Connecting Global Priorities: Biodiversity and Human Health 295

 Whitehorn, P. O’Connor S., Wackers F.L., Goulson D. 2012. Achigan-Dako, E. G., Sogbohossou, O. E., and Maundu, P.
Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth (2014). Current knowledge on Amaranthus spp.: research
and Queen Production. Science (20): 351–352. http://www. avenues for improved nutritional value and yield in leafy
sciencemag.org/content/335/6076/1555.summary (28 July amaranths in sub-Saharan Africa. Euphytica, 197(3), 303–317.
2014)
AFROFOODS (2009) Call for action from the door of return
WHO 2012. Obesity and Overweight. WHO Fact Sheet No for food renaissance in Africa. 2009. Available at: http://www.
311. May 2012. WHO, Geneva. fao.org/fileadmin/templates/food_composition/documents/
pdf/AFROFOOD_CALL_and_APPEL.pdf
WHO Global malaria programme: World Malaria Report 2014
http://www.who.int/malaria/publications/world_malaria_ Akrofi, S., Price, L.L. and Struik, P.C. HIV and Severity of
report_2014/wmr-2014-no-profiles.pdf?ua=1 seasonal household food-related coping behaviours in rural
Ghana. Ecology of Food and Nutrition, 51: 148–175.
Wilby, A., Mitchell, C., Blumenthal, D., Daszak P., Friedman,
C.S., Jutro, P., Mazumder, A., Prieur-Richard, A-H., Desprez- Agriculture-Nutrition Community of Practice (Ag2Nut CoP)
Loustau, M.-L., Sharma, M. and M.B. Thomas (2009). (2013) Key Recommendations for Improving Nutrition
Biodiversity, food provision and human health. In Biodiversity through Agriculture and Food Systems. Avaialble at: http://
change and human health: From ecosystem services to spread www.fao.org/3/a-mm215e.pdf
of disease. (Eds) Osvaldo E. Sala, Laura A. Meyerson, Camille
Allen T.; Prosperi P.; Cogill B.; and G. Flichman.  2014.
Parmesan. Island Press, Washington, USA.
Agricultural Biodiversity, Social-Ecological Systems and
World Watch Institute (2009) Biofuel Production Up Sustainable Diets. Proceedings of the Nutrition Society 73;
Despite Economic Downturn Vital Signs. Available 498–508
at : htt p://vitalsig ns.worldwatch.org/vs - trend/
Amuna, P., and Zotor, F. B. (2008). Epidemiological and
biofuel-production-despiteeconomic-downturn
nutrition transition in developing countries: impact on
Wratten, S.D., Gillespie, M., Decourtye, A., Mader, E., and N. human health and development. Proceedings of the Nutrition
Desneux (2012). Pollinator habitat enhancement: benefits Society, 67(01), 82–90.
to other ecosystem services. Agriculture, Ecosystems and
Anderson, E.N., “Food cultures: Linking People to Landscapes”
Environment, 159:112–122.
Pilgrim, S., & Pretty, J. (2010). Nature and culture: rebuilding
Yadav, S., Hunter, D. Redden, R. and Yadav, D.K. (2014) lost connections. Earthscan
Impact of climate change on agriculture production, food
Andersen, R. et al., 2014. Dietary effects of introducing
security and strategies for mitigation and adaptation. In Crop
school meals based on the New Nordic Diet – a randomised
Wild Relatives and Climate Change (Redden, R. et al. eds).
controlled trial in Danish children. The OPUS School Meal
Wiley-Blackwell, UK.
Study. The British journal of nutrition, (4), pp.1–10.
Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., Fan, J. X.,
Angelsen, A., Jagger, P., Babigumira, R., Belcher, B., Hogarth,
Yang, S., Hu, L., Leung, H., Mew, T. W., Teng, P. S., Wang, Z.,
NJ., Bauch, S., Borner, J., Smith-Hall, C., and Wunder, S.
and Mundt, C. C. 2000. Genetic diversity and disease control
(2014) Environmental income and rural livelihoods: a global
in rice. Nature 406: 718– 722. 
comparative analysis. World Development

Chapter 6 Arimond, M. and Ruel, M.T. (2004). Dietary diversity is

associated with child nutritional status: evidence from 11
h t t p : / / w w w. c o n a b . g o v. b r / O l a l a C M S / u p l o a d s / demographic and health surveys. Journal of Nutrition, 134:
arquivos/14_09_15_16_03_05_artigo_evolucao_do_paa_2. 2579–2585.
pdf
Australian Bureau of Statistics (2014, Sept.) 4727.0.55.003 –
h t t p : / / w w w. c o n a b . g o v. b r / O l a l a C M S / u p l o a d s / Australian Aboriginal and Torres Strait Islander Health
arquivos/15_03_23_15_42_09_sumario_executivo_2014_ Survey: Biomedical Results, 2012–13. Canberra.
revisado.pdf
B4FN (2014). Biodiversity for Food and Nutrition home page
A. S. Huang, L. Tanudjaja, D. Lum. Journal of Food http://www.b4fn.org/
Composition and Analysis, Vol. 12, No. 2, Jun 1999, pp.
Bach-Faig A, Berry EM, Lairon D, Reguant J, Trichopoulou
147–151.
A, Dernini S, Medina FX, Battino M, Belahsen R, Miranda
Aberoumand, A. 2009. Nutritional evaluation of edible G, Serra-Majem L; Mediterranean Diet Foundation
Portulaca oleracia as plant food. Food Analytical Methods, 2: Expert Group (2011). Mediterranean diet pyramid today.
204–207. Science and cultural updates. Public Health Nutr. 2011
Dec;14(12A):2274–84. doi: 10.1017/S1368980011002515
Abu-Basutu, K. (2013). The contribution of wild foods to food
security in the face of climate change and HIV/AIDS (Doctoral Barker, B., Stanley, L., and Lopez, A. (2007). The burden of
dissertation, MSc thesis. Rhodes University, Grahamstown, disease and injury in Aboriginal and Torres Strait Islander peoples
South Africa). 2003. Centre for Burden of Disease and Cost-Effectiveness,
School of Population Health, University of Queensland.
Barrett, C.B. Measuring food insecurity. Science. 327 12
February 2010. DOI: 10.1126/science.1182768 , 825.

296 Connecting Global Priorities: Biodiversity and Human Health

Barnes, K.K., Collins, T.A., Dion, S., Reynolds, H., Riess, S.M., Burkle LA, Marlin JC, Knight TM. Plant-pollinator
Stanzyk, A., interactions over 120 years: Loss of species, co-occurrence,
and function. Science 2013; 339: 1611–5.
Wolfe, A., Lonergan, S.M., Boettcher, P., Charrondiere, R. and
Stadlmayr, B. (2012) Importance of cattle biodiversity and Burlingame B (2014) Grand challenges in nutrition and
its influence on the nutrient composition of beef. Animal environmental sustainability. Front. Nutr. 1:3. doi: 10.3389/
Frontiers 2; 54–60 fnut.2014.00003 Available at: http://journal.frontiersin.org/
Journal/10.3389/fnut.2014.00003/full#sthash.rOQTlIRN.
Barthel, S., Crumley, C., & Svedin, U. (2013). Bio-cultural
Qp3MxHAf.dpuf
refugia  – Safeguarding diversity of practices for food
security and biodiversity. Global Environment Change, 23(5), Burlingame, B. and Toledo, A. (Eds) (2006). Special Issue:
1142–1152. Biodiversity and Nutrition. Journal of Food Composition
and Analysis 19, 6–7, pages 477–770 (September-November
Batal, M. and Hunter, E. (2007) Traditional Lebanese recipes
2006).
based on wild plants: an answer to diet simplification? Food
and Nutrition Bulletin 28 (2), S303-S311 Burlingame, B., Charrondiere, U.R., Mouille, B. (2009). Food
composition is fundamental to the cross-cutting initiative
Becquey, E., Delpeuch, F., Konaté, A.M. Delsol, H., Lange,
on biodiversity for food and nutrition. Journal of Food
M., Zoungrana, M. and Martin-Prevel, Y. 2012. Seasonality
Composition and Analysis 22, 5: 361–365.
of the dietary dimension of household food security in urban
Burkina Faso. British Journal of Nutrition, 107: 1860–1870. Cadotte, M.W., Dinnage, R., Tilman, D. Phylogenetic diversity
promotes ecosystem stability. Ecology 93, S223–S233 (2012)
Bere, E. & Brug, J., 2009. Towards health-promoting and
environmentally friendly regional diets – a Nordic example. Caluwé E. De, Halamová K. and Damme P. van (2010)
Public health nutrition, 12(1), pp.91–6. Adansonia digitata L. – A review of traditional uses,
phytochemistry and pharmacology. Afrika Focus 23 (1):
Bharucha, Z. and Pretty, J. 2010. The roles and values of wild
11–51.
foods in agricultural systems. Philosophical Transactions of
the Royal Society B, 365: 2913–2926. Clarke, S. F., Murphy, E. F., Nilaweera, K., Ross, P. R.,
Shanahan, F., O’Toole, P. W., & Cotter, P. D. (2012). The gut
BIP (2013) Biodiversity Indicators Partnership > Homepage.
microbiota and its relationship to diet and obesity: new
Retrieved 13 December 2013, from http://www.bipindicators.
insights. Gut microbes, 3(3), 186–202.
net/
CBD. 2006. Agricultural biodiversity: A cross-cutting initiative
Black, R. E., Allen, L. H., Bhutta, Z. A., Caulfield, L. E.,
on biodiversity for food and nutrition.  https://www.cbd.int/
de Onis, M., Ezzati, M., et al. (2008). Maternal and child
decision/cop/default.shtml?id=11037 (accessed August 14,
undernutrition: Global and regional exposures and health
2014).
consequences. The Lancet, 371(9608), 243–260.
CBD. 2004.  COP 7 decision VII/32. Seventh Meeting
Blasbalg, T. L., Wispelwey, B., and Deckelbaum, R. J. (2011).
of the Conference of the Parties to the Convention on
Econutrition and utilization of food-based approaches for
Biological Diversity, Kuala Lumpur, Malaysia, 9  – 20
nutritional health. Food and Nutrition Bulletin, 32(1 SUPPL.),
February 2004.  http://www.cbd.int/decision/cop/default.
S4-S13
shtml?id=7769 
Bloom, D.E., Cafiero, E.T., Jané-Llopis, E., Abrahams-Gessel,
CBD. 2006. COP 8 Decision VIII/23, Eighth Meeting of the
S., Bloom, L.R., Fathima, S., Feigl, A.B., Gaziano, T., Mowafi,
Conference of the Parties to the Convention on Biological
M., Pandya, A., Prettner, K., Rosenberg, L., Seligman, B.,
Diversity, Curitiba, Brazil, 20 – 31 March 2006. http://www.
Stein, A.Z., and Weinstein, C. (2011). The Global Economic
cbd.int/agro/food-nutrition/default.shtml
Burden of Noncommunicable Diseases. Geneva: World
Economic Forum. Challe, J.F.X. and Price, L.L. 2009. Endangered edible orchids
and vulnerable gatherers in the context of HIV/AIDS in the
Boedecker, J., Termote, C., Assogbadjo, A.C., Van Damme,
Southern Highlands of Tanzania. Journal of Ethnobiology
P. and Lachat, C. (2014) Dietary contribution of wild edible
and Ethnomedicine, 5: 41. Online: http://www.ethnobiomed.
plants to women’s diets in the buffer zone around the Lama
com/contents/5/1/41.
forest, Benin – an underutilized potential. Food Security
Chaplin-Kramer R, Dombeck E, Gerber J, et al. Global
Boelee, E., S. Atapattu, J. Barron, P. Bindraban, S. W. Bunting,
malnutrition overlaps with pollinator-dependent
D. Coates, K. Descheemaeker, N. Eriyagama, M. Finlayson,
micronutrient production. Proceedings of the Royal Society B:
and L. Gordon. (2011). Ecosystems for water and food
Biological Sciences 2014; 281(1794).
security. Nairobi: United Nations Environment Programme;
Colombo: International Water Management Institute. Charrondiere, U.R., Stadlmayr, B., Rittenschober, D., Mouille,
B., Nilsson, E., Medhammar, E., Olango, T., Eisenwagen, S.,
Bonin CL, Tracy BF. Diversity influences forage yield and
Persijn, D., Ebanks, K., Nowak, V., Du, J.; Burlingame, B.
stability in perennial prairie plant mixtures. Agric Ecosyst
(2012). FAO/INFOODS Food Composition Database for
Environ.; 162:1–7 (2012)
Biodiversity. Food Chemistry 140 (2013) 408–412.
Brock JF, Hansen JDL, Howe EE, Pretorius PD, Daval JGA,
Cherfas, J (2006) Kenyans flock back to traditional leafy
Hendricks RG (1955) Kwashiorkor and protein malnutrition.
vegetables. Geneflow. Bioversity International, Rome, Italy
A dietary therapeutic trial. The Lancet 1955;2: 355–60.

Connecting Global Priorities: Biodiversity and Human Health 297

 Clemente, J.C. et al (2015) The microbiome of uncontacted De Merode, E., Homeoowd, K. and Cowlishaw, G. 2004. The
Amerindians. Science value of bushmeat and other wild foods to rural households in
extreme poverty in Democratic Republic of Congo. Biological
Coad, L., Abernethy, K., Balmford, A., Manica, A., Airey,
Conservation, 118: 573–581.
L. and Milner-Gulland, E.J. 2010. Distribution and use of
income from bushmeat in a rural village, central Gabon. Dernini S., Meybeck A., Burlingame B., Gitz V., Lacirignola C.,
Conservation Biology, 24: 1510–1518. Debs, P., Capone R., El Bilali, H. Developing a methodological
approach for assessing the sustainability of diets: The
Conchedda, G., Lambin, E.F. and Mayaux, P. 2011. between
Mediterranean Diet as a case study. New Medit (2013)
land and sea: livelihoods and environmental changes in
3/2013: 28–36.
mangrove ecosystems of Senegal. Annals of the Association
of American Geographers, 101: 1259–1284. Devereux, S. and Longhurst, R. 2010 Incorporating
seasonality into agricultural project design and learning. IDS
Cotty, P.J. and Jaime-Garcia, R. (2007) Influences of climate
Bulletin, 41: 88–95.
on aflatoxin producing fungi and aflatoxin contamination.
International Journal of Food Microbiology 119; 109–115 Dogan, Y. 2012. Traditionally used wild edible greens in
the Aegean Region of Turkey. Acta Societatis Botanicorum
Cunningham, A.B. 2011. Non-timber forest products
Poloniae, 81: 329–342.
and markets: lessons for export-orientated enterprise
development from Africa. In Shackleton, S.E., Shackleton, Donati, K., Taylor, C. and Pearson, C.J. (2013) Local food and
C.M., and Shanley, P. (eds). Non-timber forest products in the dietary diversity: farmers markets and community gardens
global context. Springer. Heidelberg. pp. 83–106. in Melbourne, Australia in: Fanzo, J. and Hunter, D. Borelli,
T. and Mattei, F. (eds) Diversifying Food and Diets: Using
Da Costa, M.dJ., Lopes, M., Ximenes, A., Ferreira, A.dR.,
Agricultural Biodiversity to Improve Nutrition and Health. Issues
Spyckerelle, L., Williams, R., Nesbitt, H. and Erskine, W. 2013.
in Agricultural Biodiversity, Earthscan, UK.
Household food security in Timor-Leste. Food Security, 5:
83–94. Dora, C., Haines, A., Balbus, J., Fletcher, E., Adair-Rohani, H.,
Alabaster, G., Hossain, R., de Onis, M., Branca, F. and Neira,
Dabalen, A. and Paul. S. 2014. Effect of conflict on dietary
M. (2015) Indicators linking health and sustainability in the
diversity: evidence from Côte d”ivoire. World Development,
post-2015 development agenda. The Lancet 385, 380–391
58: 143–158.
Drimie, S. 2003. HIV/AIDS and land: Case studies from
Davies, G. 2002. Bushmeat and international development.
Kenya, Lesotho, and South Africa. Development Southern
Conservation Biology, 16: 587–589.
Africa, 20: 647–658.
Davis AS, Hill JD, Chase CA, Johanns AM, Liebman M.
Dulloo, E., Hunter, D. and Leaman, D.L. (2014) Plant diversity
Increasing cropping system diversity balances productivity,
in addressing food, nutrition and medicinal needs. In, Novel
profitability and environmental health.  PLoS ONE
Plant Bioresources: Application in Food, Medicine and Cosmetics
7(10):e47149 (2012)
(A. Garib-Fakim, ed). Wiley-Blackwell, UK p. 1–21
Deckelbaum, R.J. (2011) Econutrition: integrating food-based
Dweba, T.P. and Mearns, M.A. 2011. Conserving indigenous
human nutrition with ecology and agrobiodiversity. Food and
knowledge as the key to the current and future use of
Nutrition Bulletin 32; p.S3
traditional vegetables. International Journal of Information
Deckelbaum, R.J., Palm, C., Mutuo, P., and DeClerck, F.A.J. Management, 31: 564–571.
(2006) Econutrition: implementation models from the
Edderai, D. and Dame, M. 2006. A census of the commercial
Millenium Villages Project in Africa. Food and Nutrition
bushmeat market in Yauonde, Cameroon. Oryx, 40: 472–475.
Bulletin 27; 335–342
Egeland, G. M., Harrison, G. G., (2013). Health disparities:
DeClerck, F.A.J. and Negreros-Castillio, P. (2000) Plant species
promoting Indigenous Peoples’ health through traditional
of traditional Mayan homegardenso Mexico as analogsfor
food systems and self-determination. In Indigenous peoples’
multistrata agroforests. Agroforestry Systems, 48; 303–317
food systems and well-being: interventions and policies for healthy
DeClerck, F.A.J., Fanzo, J., Palm, C., Remans, R. Ecological communities. FAO, Rome.
approaches to human nutrition. Food Nutr. Bull. 32, S4–13
Eilat-Adar, S., Jiaqiong, X., Zephier, E., O’Leary, V.,
(2011)
Howard, B.V., Resnick, H.E. (2008). Adherence to Dietary
De Clerck, F. (2013) Harnessing biodiversity: from diets Recommendations for Saturated Fat, Fiber, and Sodium
to landscapes. in: Fanzo, J. and Hunter, D. Borelli, T. and Is Low in American Indians and Other U.S. Adults with
Mattei, F. (eds) Diversifying Food and Diets: Using Agricultural Diabetes. Journal of Nutrition 138: 1699 – 1704.
Biodiversity to Improve Nutrition and Health. Issues in
Eilers EJ, Kremen C, Greenleaf SS, Garber AK, Klein A-M.
Agricultural Biodiversity, Earthscan, UK.
Contribution of pollinator-mediated crops to nutrients in the
Delzenne, N. M., & Cani, P. D. (2011). Interaction between human food supply. PLoS ONE 2011; 6(6): 6.
obesity and the gut microbiota: relevance in nutrition. Annual
Ellis A, M, Myers S, S., Ricketts T, H. Do pollinators contribute
review of nutrition, 31, 15–31.
to nutritional health? PLoS ONE 2015; 10(1): 17.

298 Connecting Global Priorities: Biodiversity and Human Health

Elyse Messer, A. (2015) World crop diversity survives from Fa, J.E., Olivero, J., Real, R., Farfan, M.A., Marquez, A.L.,
peri-urban to remote rural locations http://news.psu.edu/ Vargas, J.M., Ziegler, S., Wegmann, M., Brown, D., Margetts,
story/344861/2015/02/13/research/world-crop-diversity- B. and Nasi, R. (2015) Disentangling the relative effects of
survives-peri-urban-remote-rural-locations bushmeat availability on human nutrition in Central Africa.
Nature
Englberger, L., Aalbersberg, W., Ravi, P., Bonnin, E., Marks,
G.C., Fitzgerald, M.H., and Elymore, J. (2003a) ‘Further Fanzo J, Hunter D, Borelli T and Mattei F (eds). (2013).
analyses on Micronesian banana, taro, breadfruit and other Diversifying Food and Diets: Using Agricultural Biodiversity
foods for provitamin A carotenoids and minerals’, Journal of to Improve Nutrition and Health. Routledge.
Food Composition and Analysis, vol 16, no 2, pp.219–236.
FAO (2013a). Review of Key Issues on Biodiversity and
Englberger, L., Aalbersberg, W., Fitzgerald, M.H., Marks, G.C., Nutrition. Commission on Genetic Resources for Food and
and Chand, K. (2003b). ‘Provitamin A carotenoid content of Agriculture, CGRFA-14/13/8.
different cultivars of edible pandanus fruit tectorius’, Journal
FAO. (2013b) Greening the Economy with Agriculture –
of Food Composition and Analysis, 16, 2: 237–247.
Utilization. In: Greening the Economy with Agriculture. Swiss
Englberger, L., Schierle, J., Marks, G.C., and Fitzgerald, M.H. Federation and FAO, Rome.
(2003c) ‘Micronesian banana, taro, and other foods: newly
FAO (2013c)  The 2nd International Symposium on
recognized sources of provitamin A and other carotenoids’,
“Sustainable Diets: Human Nutrition and Livestock” 12–16
Journal of Food Composition and Analysis, vol 16, no 1,
June, 2013, Ulaanbaatar, Mongolia. FAO, Bangkok.
pp.3–19.
FAO (2012) Sustainable Diets: Directions and solutions for
Englberger, L., Marks, G. C., and Fitzgerald, M. H. (2003d)
policy, research and action. Eds. Burlingame and Dernini.
Insights on food and nutrition in the Federated States of
FAO, Rome
Micronesia: a review of the literature. Public Health Nutrition
6: 5–17. FAO (2010) Expert Consultation on Nutrition Indicators for
Biodiversity – 2. Food Consumption. Rome: FAO. Available
Englberger, L., Schierle, J., Aalbersberg, W., Hofmann,
at: http://www.fao.org/docrep/014/i1951e/i1951e00.htm
P., Humphries, J., Huang, A., Lorens, A., Levendusky,
A., Daniells, J., Marks, G.C., and Fitzgerald, M.H. (2006) FAO (2009). The State of Food and Agriculture, Livestock in
‘Carotenoid and vitamin content of Karat and other the Balance. Figure 16 p. 97. FAO, Rome. Available at: http://
Micronesian banana cultivars’, International Journal of Food www.fao.org/docrep/012/i0680e/i0680e.pdf
Science and Nutrition, vol 57, pp.399–418.
FAO (2008) Expert Consultation on Nutrition Indicators for
Englberger, L., Schierle, J., Kraemer, K., Aalbersberg, W., Biodiversity – 1. Food Composition. Rome: FAO. Available
Dolodolotawake, U., Humphries, J., Graham, R., Reid, at: ftp://ftp.fao.org/docrep/fao/010/a1582e/a1582e00.pdf
A.P., Lorens, A., Albert, K., Levendusky, A., Johnson, E.,
FAO (2005). Report of the Intergovernmental Technical
Paul, Y., and Sengebau, F. (2008) ‘Carotenoid and mineral
Working Group on Plant Genetic Resources for Food and
content of Micronesian giant swamp taro (Cyrtosperma)
Agriculture. Rome, Italy.
cultivars’, Journal of Food Composition and Analysis, vol
21, pp.93–106. FAO/INFOODS (2013). Food Composition Database for
Biodiversity (BioFoodComp 2.1). http://www.fao.org/
Englberger, L., Schierle, J., Hoffman, P., Lorens, A., Albert,
docrep/019/i3560e/i3560e.pdf
K., Levendusky, A., Paul, Y., Lickaneth, E., Elymore, A.,
Maddison, M., deBrum, I., Nemra, J., Alfred, J., Vander Velde, FAO/INFOODS (2013a) FAO/INFOODS Report on the
N., and Kraemer, K. (2009) ‘Carotenoid and vitamin content Nutrition Indicator for Biodiversity – Global Progress Report.
of Micronesian atoll foods: pandanus (Pandanus tectorius) FAO: Rome. Available at: http://www.fao.org/docrep/019/
and garlic pear (Crataeva speciosa) fruit’, Journal of Food i3559e/i3559e.pdf
Composition and Analysis, vol 22, no 1, pp.1–8.
FAO/INFOODS (2013b) FAO/INFOODS Food composition
Englberger, L., Lorens, A., Pretrick, M., Raynor, B., Currie, database for biodiversity version 2.1  – BioFoodComp2.1.
J., Corsi, A., Kaufer, L., Naik, R.I., Spegal, R. and Kuhnlein, Rome: FAO. Available at: http://www.fao.org/infoods/
H.V. (2011) Approaches and lessons learned for promoting infoods/food-biodiversity/en/
dietary improvement in Pohnpei, Micronesia. In, Combating
FAOSTAT. 2014. Food and Agricultural Commodities
Micronutrient Deficiencies: Food-Based Approaches (eds B.
Production, available at: http://faostat.fao.org/site/339/
Thompson and L. Amoroso). CABI Books. pp. 224–253.
default.aspx
Englberger, L. and Johnson, E. (2013) Traditional foods
Fentahun, M.T and Hager, H. 2009. Exploiting locally
of the Pacific: Go Local, a case study in Pohnpei, Federated
available resources for food and nutritional enhancement:
States of Micronesia in: Fanzo, J. and Hunter, D. Borelli,
wild fruits diversity, potential and state of exploitation in the
T. and Mattei, F. (eds) Diversifying Food and Diets: Using
Amahara region of Ethiopia. 2009. Food Security, 1: 207–219.
Agricultural Biodiversity to Improve Nutrition and Health. Issues
in Agricultural Biodiversity, Earthscan, UK. Final report: The transformative potential of the right to food.
A/HRC/25/57. http://www.srfood.org/images/stories/pdf/
officialreports/20140310_finalreport_en.pdf

Connecting Global Priorities: Biodiversity and Human Health 299

 Food Composition. Global Progress Report 2012. Rome: Guidetti, P., Bussotti, S., Pizzolante, F., & Ciccolella, A. (2010).
FAO. Available at: http://www.fao.org/infoods/infoods/ Assessing the potential of an artisanal fishing co-management
food-biodiversity/en/ in the Marine Protected Area of Torre Guaceto (southern
Adriatic Sea, SE Italy). Fisheries Research, 101(3), 180–187.
Foote J, Murphy S, Wilkens L, Basiotis P and Carlson A
(2004) Dietary variety increases the probability of nutrient Gussow J.D. and Clancy K. Dietary guidelines for
adequacy among adults. Journal of Nutrition 134:1779–1785 sustainability. Journal of Nutrition Education (1986)
18(1):1–5.
Frison, E. A., Smith, I. F., Johns, T., Cherfas, J., and Eyzaguirre,
P. B. (2006). Agricultural biodiversity, nutrition, and health: Haddad, L., Cameron, L. and Barnett, I. (2014) The double
Making a difference to hunger and nutrition in the developing burden of malnutrition in SE Asia and the Pacific: priorities,
world. Food and Nutrition Bulletin, 27(2), 167–179.  policies and politics. Healthy Policy and Planning.
Gahukar, R.T. 2011. Entomophagy and human food security. Hajjar R, Jarvis DI, Gemmill-Herren B. The utility of crop
International Journal of Tropical Insect Science, 31: 129–144. genetic diversity in maintaining ecosystem services. Agric
Ecosyst Environ. 123(4): 261–270 (2008)
Gallaher, C.M., Kerr, J.M., Njenga, M. and Karanja, N.K.
(2013) Urban agriculture, social capital, and food security in Hatloy, A., Torheim, L., Oshaug, A., 1998. Food variety – a
the Kibera slums of Nairobi, Kenya. Agriculture and Human good indicator of nutritional adequacy of the diet? A case
Values 30; 389–404 study from an urban area in Mali, West Africa. Eur. J. Clin.
Nutr. 52, 891–898.
Gamfeldt, L., Snäll, T., Bagchi, R., Jonsson,
M., Gustafsson, L ., Kjellander, P., et al. Hatloy, A., Hallund, J., Diarra, MM. and Oshaug A (2000)
Higher  levels  of  multiple  ecosystem  services  are found Food variety, socioeconomic status and nutritional status
in  forests  with  more  tree  species. Nat. Commun. 4, 1340 in urban and rural areas in Koutiala (Mali). Public Health
(2013) Nutrition 3:57–65
Garnett T. (2013) Food sustainability: problems, perspectives Heywood, V. (2013) Overview of agricultural biodiversity
and solutions. Proceedings of the Nutrition Society 72, 29–39. and its contribution to nutrition and health in: Fanzo, J. and
Hunter, D. Borelli, T. and Mattei, F. (eds) Diversifying Food
Gerster-Bentaya, M. (2013) Nutrition-sensitive urban
and Diets: Using Agricultural Biodiversity to Improve Nutrition
agriculture. Food Security 5; 723–737
and Health. Issues in Agricultural Biodiversity, Earthscan, UK.
Gold, K. and McBurney, R. 2012. Conservation of plant
Heywood, V. and Dulloo, E. (2005) In Situ Conservation of
diversity for sustainable diets. In: Sustainable diets and
Wild Plant Species: A Critical Global Review of Good Practices.
biodiversity: directions and solutions for policy, research and
IPGRI Technical Bulletin 11. IPGRI, Rome, Italy
action, eds B. Burlingame and S. Dernini, pp. 108–114. FAO,
Rome. www.fao.org/docrep/016/i3004e/i3004e.pdf Himmelgreen, D.A., Romero-Daza, N., Turkon, D., Watson,
S., Okello-Uma, I. and Sellen, D. 2009. Addressing the HIV/
Golden, C.D., Fernald, L.C.H., Brashares, J.S., Rasolofoniaina,
AIDS food insecurity syndemic in sub-Saharan Africa. African
B.J.R. and Kremen, C. 2011. Benefits of wildlife consumption
Journal of AIDS Research, (8): 401–412.
to child nutrition in a biodiversity hotspot. Proceedings of the
National Academy of Science, 108: 19653–19656. Ho, L.S. , Gittelsohn, J., Sharma, S., Cao, X.Treuth, M., Rimal,
R., et al. (2008). Food-Related Behavior, Physical Activity, and
Graham, R.D., Welch, R.M., Saunders, D.A., Ortiz-Monasterio,
Dietary Intake in First Nations – a Population at Risk for
I., Bouis, H.E., Bonierbale, M., de Haan, S., Burgos, G., Thiele,
Diabetes. Ethnicity and Health 13(4): 335–349.
G., Liria, R. et al. Nutritious subsistence food systems. Adv.
Agron. 92, 1–74 (2007) Hoddinott, J. and Yohannes, Y. (2002)Dietary diversity as
a food security indicator. Washington: International Food
Graham, R.D. Micronutrient Deficiencies in Crops and Their
Policy Research Institute, Food Consumption and Nutrition
Global Significance. In Alloway BJ (eds) Micronutrient
Division; Discussion Paper No. 136.
Deficiencies in Global Crop Production. Springer, pp 41–62
(2008) Hoffman, I. and Baumung, R. (2013) The role of livestock
diversity in sustainable diets in: Fanzo, J. and Hunter, D.
GRAIN (2015) Free trade and Mexico’s junk
Borelli, T. and Mattei, F. (eds) Diversifying Food and Diets: Using
food epidemic. http://www.grain.org/ar ticle/
Agricultural Biodiversity to Improve Nutrition and Health. Issues
entries/5170-free-trade-and-mexico-s-junk-food-epidemic
in Agricultural Biodiversity, Earthscan, UK.
Gray, C.L, Bozigar, M. & Bilsborrow, R.E. (2015) Declining
Hooper, D.U., Adair, E.C., Cardinale, B.J., Byrnes, J.E.,
use of wild resources by indigenous peoples of the Ecuadorian
Hungate, B.A., Matulich, K.L., Gonzalez, A., Duffy, J.E.,
Amazon. Biological Conservation; Vol. 182: 270–277.
Gamfeldt, L., O’Connor, M.I. A global synthesis reveals
Greyling, M. and Potgieter, M. 2004. Mopane worms as a
biodiversity loss as a major driver of ecosystem change.
key woodland resource: The use, trade and conservation of
Nature. 2; 486 (7401):105–8. doi: 10.1038/nature11118
Imbresia belina. In: Lawes, M.J., Eeley, C.M., Shackleton, C.M.,
(2012)
(Eds.). Indigenous Forest and woodlands in South Africa.
Policy, people and practice. University of Kwazulu Natal Press,
Pietermaritzburg, South Africa. pp 553–573.

300 Connecting Global Priorities: Biodiversity and Human Health

Hooper, D. U. , F. S. Chapin III, J. J. Ewel, A. Hector, P. Jarrell, W.M. and Beverly, R.B. (1981) in Adv. Agron, The
Inchausti, S. Lavorel, J. H. Lawton, D. M. Lodge, M. Loreau, dilution effect in plant nutrition studies, ed Brady N.C.
S. Naeem, B. Schmid, H. Setälä, A. J. Symstad, J. Vandermeer, (Academic Press, New York, NY), Vol. 34, pp 197–224.
and D. A. Wardle 2005. Effects of biodiversity on ecosystem
Johns, T. and Maundu, P. (2006) Forest biodiversity, nutrition
functioning: a consensus of current knowledge. Ecological
and population health in market-oriented food systems.
Monographs 75:3–35. http://dx.doi.org/10.1890/04–0922
Unasylva 57: 34–40
(2005)
Johnson, K. B., Jacob, A., and Brown, M. E. (2013). Forest
Hughes, R.G. and Lawrence, M.A. (2005) Globalization, food
cover associated with improved child health and nutrition:
and health in Pacific Island Countries. Asia Pacific Journal of
evidence from the Malawi Demographic and Health Survey
Clinical Nutrition 14 (4): 298–306.
and satellite data. Global Health: Science and Practice,  1(2),
Human Rights Council (2014). Report of the Special 237–248.
Rapporteur on the right to food,
Johnston J.; Fanzo J.; and Cogill, B. 2014 Understanding
Hunter, L.M., Twine, W. and Patterson, L. 2007. “Locusts are Sustainable Diets: A descriptive analysis of the determinants
our beef ”: adult mortality and household dietary use of local and processes that influence diets and their impact on health,
environmental resources in rural South Africa. Scandinavian food security and environmental sustainability. Advances in
Journal of Health, 35(Suppl. 69): 165–174. Nutrition Vol 5, No 4. 2014
Hunter D and Heywood V.H. (eds) (2011) Crop Wild Relatives; Jones, A.D., Shrinivasb, A., Bezner-Kerrc, R., 2014. Farm
A Manual of In Situ Conservation. Issues in Agricultural production diversity is associated with greater household
Biodiversity, Earthscan, UK. 414pp dietary diversity in Malawi: findings from
Ickowitz, A., Powell, B., Salim, M.A. and Sunderland, T.C.H. nationally representative data. Food Policy 46, 1–12.
(2014) Dietary quality and tree cover in Africa. Global
Junkers, J., Boesch, C., Mundry, R., Stephens, C., Lormie,
Environmental Change, 24, 287–294
M., Tweh, C. and Kuhl, H.S. (2015) Education and access to
INFOODS (2013). INFOODS: Food Biodiversity. Retrieved fish but not economic development predict chimpanzee and
13 December 2013, from http://www.fao.org/infoods/ mammal occurrence in West Africa. Biological Conservation
infoods/food-biodiversity/en/ 182: 27–35
International Food Policy Research Institute. 2014. Global Kaimowitz, D., and Sheil, D. (2007). Conserving what and
Nutrition Report 2014: Actions and Accountability to for whom? why conservation should help meet basic human
Accelerate the World’s Progress on Nutrition. Washington, needs in the tropics. Biotropica, 39(5), 567–574.
DC.
Kalipeni, E. and Oppong, J. 1998. The refugee crisis in Africa
ITC. (2006). International Trade Centre statistics. http:// and implications for health and disease: a political ecology
langues.p-maps.org/pmaps/index.php? approach. Social Science and Medicine, 46: 1637–1653.
ITC. (2007). International Trade Centre UNCTAD/WTO. Katz, D.L. and Meller, S. (2014) Can we say what diet is best
Overview of World Production and Marketing of Organic for health? Annual Review of Public Health, 35: 83–103
Wild Collected Products. Geneva. 91 pp.
Kehlenbeck, K., Asaah, E. and Jamnadass, R. (2013a).
IUCN (2008). Red list of threatened species. IUCN, Gland, Diversity of indigenous fruit trees and their contribution to
Switzerland. Available online at: http://www.iucnredlist.org/ nutrition and livelihoods in sub-Saharan Africa: examples
[Accessed on the 20 January 2009]. from Kenya and Cameroon. In J. Fanzo, D. Hunter, T.
Borelli and F. Mattei, eds. Diversifying food and diets: using
Jackson, R. (1997) Dietary genocide: eating to an early death
agricultural biodiversity to improve nutrition and health
in Micronesia. Pacific Health Dialog 4 (1): 88–89.
issues in agricultural biodiversity, pp. 257–269. London,
Jacobsen, S., Sørensen, M., Pedersen, S. M., and Weiner, Earthscan.
J. (2013). Feeding the world: Genetically modified crops
Kehlenbeck, K. McMullin, S. Kindt, R. Ofori, D. Jamnadass,
versus agricultural biodiversity. Agronomy for Sustainable
R. (2013b). Fruit tree diversity for enhancing year-round
Development, 33(4), 651–662.
food and nutrition security: developing a participatory
Jamnadass, R., Place, F., Torquebiau, E., Malézieux, E., Iiyama, and multidisciplinary approach Poster presented at the
M., Sileshi, G.W., Kehlenbeck, K., Masters, E., McMullin, S., International Conference for Global Food Security, 29 Sep – 2
Dawson, I.K. (2013). Agroforestry for food and nutritional Oct 2013, Noordwijkerhout, The Netherlands. Book of Poster
securityIn: Unasylva 241, 64 (2), FAO, Rome Italy. Abstracts p355–358 2013273 http://www.worldagroforestry.
org/downloads/publications/PDFs/PO13273.PDF
Jamnadass, R.H., Dawson, I.K., Franzel, S., Leakey, R.R.B.,
Mithöfer, D., Akinnifesi, F.K. and Tchoundjeu, Z. (2011). Kennedy, G. L., Pedro, M. R., Seghieri, C., Nantel, G., and
Improving livelihoods and nutrition in sub-Saharan Africa Brouwer, I. (2007). Dietary diversity score is a useful indicator
through the promotion of indigenous and exotic fruit of micronutrient intake in non-breast-feeding Filipino
production in smallholders’ agroforestry systems: a review. children. The Journal of nutrition, 137(2), 472–477.
International Forest Review, 13: 338–354.
Kennedy, G.; Burlingame, B. (2003). Analysis of food
composition data on rice from a plant genetic resources
perspective. Food Chemistry 80:589–596.

Connecting Global Priorities: Biodiversity and Human Health 301

 Khoury, C.K., Bjorkman, A.D., Dempewolf, H., Ramirez- Lobstein, T., Jackson-Leach, R., Moodie, M.L., Hall, K.D.,
Villegas, J., Guarino, L., Jarvis, A., Rieseberg, L.H., Struik, Gortmaker, S.L., Swinburn, B.A., James, W.P.T. and Wang, Y.
P.C. Increasing homogeneity in global food supplies and the (2015) Child and adolescent obesity: part of a bigger picture.
implications for food security. Proc. Natl. Acad. Sci. USA 111, The Lancet
4001–4006 (2014)
Loyd~Puryear MA et al. Vitamin A deficiency in Micronesia:
Kinley, A. (2012). Local food on a global scale: An exploration a statewide survey in Chuuk. Nutr Res 1991; 11: 1101–1110.
of the international slow food movement. Journal of
Luczaj, L., Končić, M.Z., Miličević, T., Dolina, K. and Pandža,
Integrated Studies, 1(3).
M. 2013. Wild vegetable mixes sold in the markets of
Klein A-M, Vaissiere BE, Cane JH, et al. Importance of Dalmatia (southern Croatia). Journal of Ethnobiology and
pollinators in changing landscapes for world crops. Proc R Ethnomedicine 2013, 9:2. Online http://www.ethnobiomed.
Soc B 2007; 274: 303–13. com/content/9/1/2
Kirwan L, et al. Evenness drives consistent diversity effects in Lynn, K., Daigle, J., Hoffman, J., Lake, F., Michelle, N., Ranco,
intensive grassland systems across 28 European sites. J Ecol. D., Viles, C., Voggesser, G. and Williams, P. (2013) The impacts
95(3):530–539 (2007 of climate change on tribal traditional foods. Climate Change
120: 545–556
Kobori, N.C. and Rodriguez-Amaya, D.B. (2008) Uncultivated
Brazilian green leaves are richer sources of carotenoids Lutaladio, N., Burlingame, B., Crews, J. (2010). Horticulture,
than are commercially produced leafy vegetables. Food and biodiversity and nutrition. Journal of Food Composition and
Nutrition Bulletin 29 (4); 320–328 Analysis 23, 6:481–485.
Kothari, A., Cooney, R., Hunter, D., McKinnon, K., Muller, Maillot, M., Issa, C., Vieux, F., Lairon, D. and Darmon, N.
E., Nelson, F., Oli, K., Pandey, S., Rasheed, T. and Vavrova, (2011) The shortest way to reach nutritional goals is to
L. (2015) ‘Chapter 25, Resource Use and Development’ adopt Mediterranean food choices: evidence from computer-
in Worboys, G.L., Lockwood, M., Kothari, A., Feary, S. generated personalized diets. American Journal of Clinical
and Pulsford, I. (eds) Protected Area Governance and Nutrition
Management, Australian National University Press, Canberra,
Martínez, I., Stegen, J. C., Maldonado-Gómez, M. X., Eren,
Australia.
A. M., Siba, P. M., Greenhill, A. R., & Walter, J. (2015). The
Kremen, C., Miles, A. Ecosystem services in biologically gut microbiota of rural Papua New Guineans: composition,
diversified versus conventional farming systems: benefits, diversity patterns, and ecological processes. Cell reports,
externalities, and trade-offs. Ecol. Soc. 17, 40 (2012) 11(4), 527–538.
Kuhnlein, H., Erasmus, B., Spigelski, D., Burlingame, B. Mavengahama, S., McLachlan, M., and De Clercq, W. (2013).
(2013). Indigenous Peoples Food and Wellbeing: Interventions The role of wild vegetable species in household food security
and Policies for Healthy Communities. FAO and CINE, Rome. in maize based subsistence cropping systems. Food Security,
5(2), 227–233.
Kuhnlein, H., Erasmus, B., Spigelski, D. (2009). Indigenous
Peoples’ Food Systems: the many dimensions of culture, diversity Maundu, P., Bosibori, E., Kibet, S., Morimoto, Y., Odubo, A.,
and environment for nutrition and health. FAO and CINE, Rome. Kapeta, B., Muiruri, P., Adeka, R. and Ombonya, J (2013a).
A practical guide to documenting traditional foodways. Nairobi:
Kümpel, N.F., Milner-Gulland, E.J., Cowlishaw, G. and
UNESCO.
Rowcliffe, J.M. 2010. Incentives for hunting: the role of
bushmeat in the household economy in rural Equatorial Maundu, P., Kapeta, B., Muiruri, P., Adeka, R., Ombonya, J.,
Guinea. Human Ecology, 38:251–264. Morimoto, Y., Bosibori, E., Kibet, S. and Odubo, A. (2013b)
Safeguarding Intangible Cultural Heritage: A photobook of
Lee, M. S., Woo, M. K., Kwak, C. S., Oh, S. I., & Park, S. C.
traditional foodways of the Isukha and East Pokot communities
(2001). Analysis of traditional Korean food patterns according
of Kenya . Nairobi. UNESCO.
to the healthy longevity diet based on the database of favorite
Korean foods. Annals of the New York Academy of Sciences, Maundu, P., Kapeta, B., Muiruri, P., Morimoto, Y., Bosibori,
928(1), 348–348. E., Kibet, S. and Odubo, A. (2013c) Safegurading Intangible
Cultural heritage: Traditional Foodways of the East Pokot
Lee, M.-J., Popkin, B.M. & Kim, S., 2002. The unique aspects
Community of Kenya. Nairobi. UNESCO.
of the nutrition transition in South Korea: the retention of
healthful elements in their traditional diet. Public Health Maundu, P., Muiruri, P. & Adeka, R., Ombonya, J., Morimoto,
Nutrition, 5(1A), pp.197–203. Y., Bosibori, E., Kibet, S. and Odubo, A. (2013d) Safeguarding
Intangible Cultural Heritage: Traditional Foodways of the Isukha
Lewis, M. C., Inman, C. F., Patel, D., Schmidt, B., Mulder, I.,
Community of Kenya. Nairobi. UNESCO.
Miller, B., et al. (2012). Direct experimental evidence that
early-life farm environment influences regulation of immune McBurney, R.P.H., Griffin, C., Paul, A.A and Greenberg, D.C.
responses. Pediatr Allergy Immunol, 23(3), 265–269. (2004) The nutritional composition of African wild food
plants: from compilation to utilization. Journal of Food
Lim SS, Vos T, Flaxman AD, et al. A comparative risk
Composition and Analysis, 17 (3–4): 277–89
assessment of burden of disease and injury attributable to
67 risk factors and risk factor clusters in 21 regions, 1990–
2010: a systematic analysis for the Global Burden of Disease
Study 2010. The Lancet 2012; 380(9859): 2224–60.

302 Connecting Global Priorities: Biodiversity and Human Health

McDermott, J., Johnson, N., Kadiyala, S., Kennedy, G. Moursi, M.M., Arimond, M., Dewey, K.G., Treche, S., Ruel,
and Wyatt, A.J. (2015) Agricultural research for nutrition M.T., 2008. Dietary diversity is a good predictor of the
outcomes – rethinking the agenda. Food Security DOI micronutrient density of the diet of 6- to 23- month-old
10.1007/s12571–0462–9 children in Madagascar. J. Nutr. 138, 2448–2453.
McEwan, M., Prain, G. and Hunter, D. (2013) Opening a can Myers et al (2014) Increasing CO2 threatens human
of mopane worms: can cross-sectoral partnerships leverage nutrition. Nature 510 (7503), 139–142.
agricultural biodiversity for better quality diets? in: Fanzo, J.
Nasi, R., Taber, A. and Van Vliet, N. 2011. Empty forests,
and Hunter, D. Borelli, T. and Mattei, F. (eds) Diversifying Food
empty stomachs? Bushmeat and livelihoods in the Congo
and Diets: Using Agricultural Biodiversity to Improve Nutrition
and Amazon Basins. International Forestry Review, 13(3):
and Health. Issues in Agricultural Biodiversity, Earthscan, UK.
355–368.
McGarry, D.K. and Shackleton, C.M. 2009a. Is HIV/AIDS
Nasi, R., Brown, D., Wilkie, D., Bennett, E., Tutin, C., van
jeopardising biodiversity? Environmental Conservation, 36:
Tol, G. and Christophersen, T. 2008. Conservation and use
5–7.
of wildlife-based resources: the bushmeat crisis. Technical
McGarry, D.K. and Shackleton, C.M. 2009b. Children Series 33. Montreal/Bogor, Secretariat of the Convention
navigating rural poverty: rural children’s use of wild resources on Biological Diversity/Center for International Forestry
to counteract food insecurity in the Eastern Cape province, Research (CIFOR).
South Africa. Journal of Children and Poverty, 15: 19–37.
Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N.,
McLaren DS (1966) A fresh look at protein calorie Margono, C., et al. (2014). Global, regional, and national
malnutrition. Lancet 1966;2:485–488 prevalence of overweight and obesity in children and adults
during 1980–2013: a systematic analysis for the Global
McLaren DS (1974) The great protein fiasco. Lancet
Burden of Disease Study 2013. The Lancet, 384(9945),
1974;2:93–96
766–781.
Medhammar, E., Wijesinha-Bettoni, R., Stadlmayr, B.,
Obopile, M. and Seeletso, T.G. 2013. Eat or not eat: an
Nilsson, E., Charrondiere, U.R., Burlingame, B. (2012).
analysis of the status of entomophagy in Botswana. Food
Composition of milk from minor dairy animals and buffalo
Security, 5: 817–824.
breeds: a biodiversity perspective. Journal of the Science of Food
and Agriculture, 92, 445–474. Ocho, D.L., Struik, P.C., Price, L.L., Kelbessa, E. and Kolo, K.
2012. Assessing the level of food shortage using the traffic
Merchant, C. American Environmental History: An
light metaphor by analysing the gathering and consumption
Introduction. Columbia University Press, New York (2007).
of wild foods plants, crop parts and crop residues in Konso,
Mertz, O., Lykke, A.M. and Reenburg, A. 2001. Importance Ethiopia. Journal of Ethnobiology and Ethnomedicine, 8: 30.
and seasonality of vegetable consumption and marketing in online http://www.ethnobiomed.com/content/8/1/30.
Burkina Faso. Economic Botany, 55: 276–289.
Olsen, A., Egeberg, R., Halkjær, J., Christensen, J., Overvad,
Mijatović D, van Oudenhoven F, Eyzaguirre P, Hodgkin T. The K., & Tjønneland, A. (2011). Healthy aspects of the Nordic
role of agricultural biodiversity in strengthening resilience to diet are related to lower total mortality. The Journal of
climate change: Towards an analytical framework. Int J Agric nutrition, 141(4), 639–644.
Sustain.; 11(2):95–107 (2013)
Orsini, F., Gasperi, D., Marchetti, L., Piovene, C., Draghetti,
Millenium Ecosystem Assessment (2005) Ecosystems and S., Ramazzotti, S., Bazzocchi, G. and Gianquinto, G. (2014)
Human Well-Being: Current State and Trends. Island Press. Exploring the production capacity of rooftop gardens (RTGs)
in urban agriculture: the potential impact on food and
Ministry of Health. 2012. The Health of New Zealand Adults
nutrition security, biodiversity and other ecosystem services
2011/12: Key findings of the New Zealand Health Survey.
in the city of Bologna. Food Security 6: 781–792
Wellington: Ministry of Health
Partnership for Interdisciplinary Studies of Coastal Oceans
Minjigdorja,, N Hauga, A. and Austbøa, D. (2012). Fatty acid
(PISCO). (2011). The Science of Marine Reserves (2nd
composition of Mongolian mare milk. Acta Agriculturae
Edition, Europe). www.piscoweb.org. 22 pages.
Scandinavica, Section A – Animal Science 62,2: 73–80.
Patel, K., Guenther, D., Wiebe, K. and Seburn, R.A. (2014)
Mirmiran P, Azadbakht L, Esmaillzadeh A and Azizi F (2004)
Promoting food security and livelihoods for urban poor
Dietary diversity score in adolescents- a good indicator of the
through the informal sector: a case study of street food
nutritional adequacy of diets: Tehran lipid and glucose study.
vendors in Madurai, Tamil Nadu, India. Food Security 6:
Asia Pacific Journal of Clinical Nutrition 13(1):56–60
861–878
Mojeremane, W. and Tshwenyane, S.O. 2004. Azanza
Paull, J. (2013) “Please pick me’: how Incredible Edible
garckeana: a valuable indigenous fruit tree of Botswana.
Todmorden is repurposing the commons for open source
Pakistan Journal of Nutrition, 3: 264–267.
food and agricultural biodiversity in: Fanzo, J. and Hunter,
Moomaw, W., Griffin, T., Kurczak, K., Lomax, J. The Critical D. Borelli, T. and Mattei, F. (eds) Diversifying Food and Diets:
Role of Global Food Consumption Patterns in Achieving Using Agricultural Biodiversity to Improve Nutrition and Health.
Sustainable Food Systems and Food for All. United Nations Issues in Agricultural Biodiversity, Earthscan, UK.
Environment Programme, Paris, France (2012).

Connecting Global Priorities: Biodiversity and Human Health 303

 Pedro, M.R.A., Benavides, R.C., Barba, C.V.C. 2006. Dietary Remans R, Flynn D, DeClerck F, Diru W, Fanzo J et al.
changes and their health implications in the Philippines. In Assessing nutritional diversity of cropping systems in African
The double burden of malnutrition: Case studies in six developing villages. PLoS ONE 6(6): e21235. doi:10.1371/journal.
countries. Food and Agriculture Organization Food and pone.0021235 (2011)
Nutrition Papers No. 83. FAO of the United Nations, Rome:
Remans, R. and Smukler, S. (2013) Linking biodiversity and
pp. 205 – 258 (ftp://ftp.fao.org/docrep/fao/009/a0442e/
nutrition in: Fanzo, J. and Hunter, D. Borelli, T. and Mattei, F.
a0442e00.pdf)
(eds) Diversifying Food and Diets: Using Agricultural Biodiversity
Penafiel, D., Lachat, C., Espinel, R., Van Damme, P., and to Improve Nutrition and Health. Issues in Agricultural
Kolsteren, P. (2011). A systematic review on the contributions Biodiversity, Earthscan, UK.
of edible plant and animal biodiversity to human diets.
Remans, R., Wood, S., Anderman, T.L., Saha, N., DeFries,
EcoHealth, 8(3), 381–399.
R. (2014) Measuring nutritional diversity of national
Petrini, C. (2013). Slow food nation: Why our food should be food supplies. Global food security. DOI: 10.1016/j.
good, clean, and fair. Rizzoli Publications. gfs.2014.07.001
Petrillo, P.L. (2012): Biocultural diversity and the Roberto, C.A., Swinburn, B., Hawkes, C., Huang, T, T-K,
Mediterranean diet. In: FAO. Sustainable Diets and Biodiversity: Costa, S.A., Ashe, M., Zwicker, L., Cawley, J.H. and Brownell,
Directions and Solutions for Policy, Research and Action. Eds. K.D. (2015) Patchy progress on obesity prevention: emerging
Burlingame and Dernini. FAO, Rome, pp. 224–229. examples, entrenched barriers and new thinking. The Lancet
Pezzana, A., Bersani, L., Baldereschi, F., Ponzio, R., Frighi, Rubiang-Yalambing, L., Arcot, J., Greenfield, H. and Holford,
Z., Durelli, P. C., Vassalo, D. and Petrini, C. (2014). An P. (2014) Aibika (Abelmoschus manihot L.): Genetic variation,
“LCA” approach to Slow Food Presidia products: from agro- morphology and relationships to micronutrient composition.
environmental and socio-cultural aspects to economic Food Chemistry
sustainability and nutritional evaluations. In Schenck,
Rook, G. A. (2013). Regulation of the immune system by
R., Huizenga, D. (Eds.), 2014. Proceedings of the 9th
biodiversity from the natural environment: an ecosystem
International Conference on Life Cycle Assessment in the
service essential to health. Proceedings of the National
Agri-Food Sector (LCA Food 2014), 8–10 October 2014, San
Academy of Sciences, 110(46), 18360–18367.
Francisco, USA. ACLCA, Vashon, WA, USA.
Ruel, M., Graham, J., Murphy, S., and Allen, L. (2004).
Picasso VD, Brummer EC, Liebman M, Dixon PM, Wilsey
Validating simple indicators of dietary diversity and animal
BJ. Crop species diversity affects productivity and weed
source food intake that accurately reflect nutrient adequacy
suppression in perennial polycultures under two management
in developing countries. Report submitted to GL-CRSP.
strategies. Crop Sci.; 48(1):331–342 (2008)
Ruel, M.T. (2003). Operationalising dietary diversity: a review
Pollan, M. (2008). In Defense of Food – An eater’s manifesto.
of measurement issues and research priorities. The Journal
New York, USA: Penguin Books.
of Nutrition (Supplement) 3911S-3926S.
Popkin, B. M., Adair, L. S., & Ng, S. W. (2012). Global nutrition
Ruel MT and Levin CE (2002) Food based approaches for
transition and the pandemic of obesity in developing
alleviating micronutrient malnutrition – an overview. J Crop
countries. Nutrition reviews, 70(1), 3–21.
Prod 2002; 6:31–35
Popkin, B. M. (2001). The nutrition transition and obesity
Ruiz Pérez M., Ndoye O. and Eyebe A. 1999. Marketing of
in the developing world. The Journal of nutrition, 131(3),
non-timber forest products in the humid forest zone of
871S-873S.
Cameroon. Unasylva, 50: 12–19.
Poulsen, S.K., Due, A., Jordy, A.B., Kiens, B., Stark, K.D.,
Saxe, H., 2014. The New Nordic Diet is an effective tool
Stender, S., Holst, C., Astrup, A., and Larsen, T.M. (2014):
in environmental protection: it reduces the associated
Health effect of the New Nordic Diet in adults with increased
socioeconomic cost of diets. The American Journal of Clinical
waist circumference : a 6-mo randomized controlled trial. The
Nutrition, 99(5), pp.1117–25.
American Journal of Clinical Nutrition 99 (1), pp.35–45.
Schaumberg, D. A., Linehan, M., Hawley, G., O’Connor, J. O.,
Powell, B., Ouarghidi, A., Johns, T., Tattou, M. I., and
Dreyfuss, M., and Semba, R. D. (1995). Vitamin A deficiency
Eyzaguirre, P. (2014). Wild leafy vegetable use and
in the South Pacific. Public Health, 109, 311–317.
knowledge across multiple sites in Morocco: a case study for
transmission of local knowledge?. Journal of Ethnobiology Schneider, S. (2008). Good, clean, fair: The rhetoric of the
and Ethnomedicine, 10(1), 34. slow food movement. College English, 70(4), 384–402.
Powell, B., Thilsted, S. H., Ickowitz, A., Termote, C., Schreckenberg, K. 2004. The contribution of shea butter
Sunderland, T. and Herforth, A. (2015) Improving diets with (Vitellaria paradoxa C.F. Gaertner) to local livelihoods
wild and cultivated biodiversity from across the landscape. in Benin. In: Sunderland, T. and Ndoye, O. (eds). Forest
Food Security DOI 10.1007/s12571–015–0466–5 products, livelihoods and conservation: case studies of non-
timber forest product systems, vol 2: Africa. CIFOR, Bogor,
Prosperi P.; Allen T.; Padilla M.; Peri I.; and Cogill, B. 2014.
pp 149–168.
Sustainability and Food and Nutrition Security: A Vulnerability
Assessment Framework for the Mediterranean Region. Sage
Open 2014 4: DOI: 10.1177/2158244014539169

304 Connecting Global Priorities: Biodiversity and Human Health

Schulp, C.J.E., Thuiller, W. and Verburg, P.H. (2014) Wild food Song, Y. & Joung, H., 2012. A traditional Korean dietary
in Europe: a synthesis of knowledge and data of terrestrial pattern and metabolic syndrome abnormalities. Nutrition,
wild food and as an ecosystem service. Ecological Economics Metabolism and Cardiovascular Diseases, 22(5), pp.456–462.
105; 292–305
Stadlmayr, B., et al. (2013) Review: Nutrient composition of
Scoones, I. Melnyk, M. and Pretty, J. N. (1992) Hidden selected indigenous fruits from sub-Saharan Africa. Journal
Harvest: Wild Foods in Agricultural Systems, A literature of the Science of Food and Agriculture. 93(11): 2627 – 2636
review and annotated bibliography. IIED, UK, 256, pp.
Stadlmayr, B., Nilsson, E., Medhammar, E., Burlingame,
Secretariat of the Convention on Biological Diversity (2012) B., and Charrondiere, U. R. (2011) . Nutrition indicator for
Cities and Biodiversity Outlook. Montreal, 64 pages. biodiversity on food composition – A report on the progress
of data availability. Journal of Food Composition and
Shackleton, S.E., Kirby, D. and Gambiza, J. 2011. Invasive
Analysis, 24(4–5), 692–698.
plants – friends or foes? Contribution of prickly pear (Opuntia
ficus-indica) to livelihoods in Makana Municipality, Eastern Steyn, N.P., Nel., J.H., Nantel, G., Kennedy, G. and Labadarios,
Cape, South Africa. Development southern Africa, 28: D. 2006. Food variety and dietary diversity scores in children:
177–193. are they good indicators of dietary adequacy? Public Health
Nutrition, 9: 644–650.
Shackleton, C.M., Shackleton, S.E., Gambiza, J., Nel, E.,
Rowntree, K., Urquhart, P., Fabricus, C. and Ainslie, A. 2010. Styles, C.V. 1994. There’s big value in mopane worms.
Livelihoods and vulnerability in the arid and semi-arid lands Farmer’s Weekly, 22 July, 20–22
of southern Africa: exploring the links between ecosystem
Styles, C.V. 1995. The elephant and the worm. BBC Wildlife
services and poverty alleviation. Nova Publishers, New York.
13:22–24
pp 267.
Sujarwo, W., Arinasa, I.B.K., Salomone, F., Caneva, G. and
Shackleton, C., Pasquini, M. and Drescher, A.W. (2009) African
Fattorini, S. (2014) Cultural erosion of Balinese indigenous
indigenous vegetables in urban agriculture. Earthscan, UK
knowledge of food and nutraceutical plants. Economic Botany
Shackleton, S.E., Campbell, B., Lotz-Sisitka, H. and 68, 426–437.
Shackleton, C.M. 2008. Links between the local trade in
Swinburn, B., Kraak, V., Rutter, H., Vandevijvere, S., Lobstein,
natural products, livelihoods and poverty alleviation in a
T., Sacks, G., Gomes, F., Marsh, T. and Magnusson, R. (2015)
semi-arid region of South Africa. World Development, 36:
Strengthening of accountability systems to create healthy
505–526. Shackleton, C.M. and Shackleton, S.E. 2004.The
food environments and reduce global obesity. The Lancet
importance of non-timber forest products in rural livelihood
security and as safety-nets: evidence from South Africa. South Talavera MT, Felix A and Narciso M. 2011. Integrated
African Journal of Science, 100: 658–664. Report on Formative Research on Food Preparation and
Complementary Feeding Practices of Mothers of 0–23 month
Shackleton, C.M., Dzerefos, C.M., Shackleton, S.E. and
old children. IHNF, CHE, UPLB.
Mathabela, F.R. 2000. The use of and trade in indigenous
edible fruits in the Bushbuckridge savanna region, South Thow, A. M., Swinburn, B., Colagiuri, S., Diligolevu, M.,
Africa. Ecology of Food and Nutrition, 39: 225–245. Quested, C., Vivili, P. and Leeder, S. (2010) Trade and food
policy: case studies from three Pacific Island countries. Food
Shackleton, S.E., Shackleton, C.M., Dzerefos, C.M. and
Policy 35: 556–564.
Mathabela, F.R. 1998. Use and trading of wild edible herbs
in the central lowveld savanna region, South Africa. Economic Termote et al. (2012a) Wild edible plant markets in Kisangani,
Botany, 52: 251–259. Democratic Republic of Congo. Human Ecology 40: 269–285.
Shimbo, S., Kimura, K., Imai, Y., Yasumoto, K., Yamamoto, Termote et al. (2012b) A biodiverse rich environment does
K., et al.. Number of food items as an indicator of nutrient not contribute to a better diet: a case study from DRCongo.
intake. Ecol. Food Nutr. 32, 197–206 (1994) PLoS One 7: 1–10.
Sho, H., 2001. History and characteristics of Okinawan Termote et al. (2011) Eating from the wild: Turumbu, Mbole
longevity food. Asia Pacific Journal of Clinical Nutrition, 10(2), and Bali traditional knowledge on non-cultivated edible
pp.159–164. plants, District Tshopo, DRCongo. Genetic Resources and
Crop Evolution: 58: 585–618.
Shrimpton R, Rokx C. The double burden of malnutrition: a
review of global evidence. Health, Nutrition, and Population Termote, C., Van Damme, P. and Djailo, B.D. 2010. Eating
(HNP) Discussion Paper. Washington, DC: The World Bank, from the wild: Turumbu indigenous knowledge on non-
2012. http://www-wds.worldbank.org cultivated edible plants, Tshopo District, DRCongo. Ecology
of Food and Nutrition, 49: 173–207.
Simmonds, N.W. (1995) The relation between yield and
protein in cereal grain. J. Sci. Food Agr. 67:309–315. Tetens, I. Hels, O., Khan, N.I., Tilsted, S.H. and Hassan, N.
2003. Rice-based diets in rural Bangladesh: how do different
Snowdon, W. and Thow, A.M. (2013) Trade policy and obesity
age and sex groups adapt to seasonal changes in energy
prevention: challenges and innovation in the Pacific Islands.
intake? American Journal of Clinical Nutrition, 23: 406–413.
Obesity Reviews 14: 150–158

Connecting Global Priorities: Biodiversity and Human Health 305

 Thebo, A.L., Drechsel, P. and Lambin, E.F. (2014) Global UN (2012). Report of the United Nations Conference on
assessment of urban and peri-urban agriculture: irrigated Sustainable Development, Rio de Janeiro, Brazil, 20–22 June
and rainfed croplands. Environmental Research Letters 9: 2012. United Nations, New York.
doi:10.1088/1748–9326/9/11/114002
UN SCN (2013). Nutrition and Sustainability. A long-
Tilsted, S.H. (2013) Fish diversity and fish consumption term vision for effective strategies. http://www.unscn.
in Bangladesh in: Fanzo, J. and Hunter, D. Borelli, T. and org/files/NutCC/Nutrition-and-Sustainability-Seminar/
Mattei, F. (eds) Diversifying Food and Diets: Using Agricultural NutSus_12Nov2013.pdf
Biodiversity to Improve Nutrition and Health. Issues in
UNEP (2012). The Critical Role of Global Food Consumption
Agricultural Biodiversity, Earthscan, UK.
Patterns in Achieving Sustainable Food Systems and Food for
Tirado, M.C., Crahay, P., Mahy, L., Zanev, C., Neira, M., All, A UNEP Discussion Paper”, United Nations Environment
Msangi, S., Brown, R., Scaramella, C., Costa Coitinho, D. and Programme. Paris, France.
Muller, A. (2013) Climate change and nutrition: creating a
UNESCO (2010). Intangible heritage: The Mediterranean
climate for nutrition security. Food and Nutrition Bulletin
diet. Available at: http://www.unesco.org Accessed March
34: 533–547
25, 2015.
The Lancet (2013). Maternal and Child Nutrition Series.
UNESCO (2013). Intergovernmental Committee for the
Richard Horton Editor-in-Chief. 6 June 2013.
Safeguarding of the Intangible Cultural Heritage: Decisions,
The Lancet (2008). Maternal and Child Undernutrition Series. Available at: http://www.unesco.org/culture/ich/index.
Richard Horton Editor-in-Chief. January 16, 2008. php?pg=00473.
Tilman, D. and Clark, M. (2014) Global diets link Vanbergen AJ. Insect Pollinators Initiative (2013) Threats to
environmental sustainability and human health. Nature an ecosystem service: Pressures on pollinators. Frontiers in
515:518–522 Ecology and the Environment 2013; 11: 251–9.
Tilsted, S.H. (2013) Fish diversity and fish consumption Van Huis, A., Van Itterbeeck, J., Klunder, H., Mertens, E.,
in Bangladesh in: Fanzo, J. and Hunter, D. Borelli, T. and Halloran, A., Muir, G., and Vantomme, P. (2013) Edible
Mattei, F. (eds) Diversifying Food and Diets: Using Agricultural insects: future prospects for food and feed security. FAO
Biodiversity to Improve Nutrition and Health. Issues in Forestry Paper 171.
Agricultural Biodiversity, Earthscan, UK.
Van Oudenhoven, F. and Haider, J. (2015) With Our
Toledo, A. and Burlingame, B. (2006). Biodiversity and Own Hands; A Celebration of Food and Life in the Pamir
nutrition: A common path toward global food security and Mountains of Afghanistan and Tajikistan. LM Publishers, the
sustainable development. Journal of Food Composition and Netherlands. 672 pp.
Analysis 19, 6–7, 477–483.
Van Vliet, N., Nebesse, C., Gambalemoke, S., Akaibe, D.
Turner, N.J., Luczaj, L.J., Migliorini, P., Pieroni, A., Dreon, and Nasi, R. 2012. The bush meat market of Kisangana,
A.L., Sacchetti, L.E. Paoletti, M.G. (2011) Edible and tended Democratic Republic of Congo: implications for conservation
wild plants, traditional ecological knowledge and agroecology. and food security. Oryx, 46: 196–203.
Critical Reviews in Plant Sciences 30: 198–225
Vinceti, B., Ickowitz, A., Powell, B., Kehlenbeck, K., Termote,
Turner, N., Plotkin, M., Kuhnlein, H. (2013). Global C., Cogill, B. and Hunter, D. (2013) The contribution of forest
environmental challenges to the integrity of Indigenous foods to sustainable diets. Unasylva 64; 54–64.
Peoples’ food systems. In In Indigenous peoples’ food systems
Vira, B., Wildburger, C. and Mansourian, S. (2015) Forests,
and well-being: interventions and policies for healthy communities.
Trees and Landscapes for Food Security and Nutrition; A
FAO, Rome.
Global Assessment Report. IUFPRO World Series Volume
Turner, R., Hawkes, J. Waage, J., Ferguson, E., Haseen, F., 33. Vienna. 172p
Homans, H., Hussein, J., Johnston, D., Marais, D., McNeill, G.,
Wahlqvist, M. & Specht, R. (1998). Food variety and
and Shankar, B. (2013) Agriculture for improved agriculture:
biodiversity: Econutrition. Asia Pacific Journal of Clinical
the current research landscape. Food and Nutrition Bulletin
Nutrition  12; 7(3/4):314–9.
34 (4); 369–377
Wahlqvist ML, Specht RL. 1998. Food variety and
UN Administrative Committee on Coordination/
biodiversity: Econutrition. Asia Pacific Journal of Clinical
Subcommittee on Nutrition (ACC/SCN) (2000).Fourth report
Nutrition 7(3/4): 314–319.
on the world nutrition situation: ACC/
Weinberg, K. andPichop, G.N. 2009. Marketing of African
SCN in collaboration with the International Food Policy
indigenous vegetables along urban and peri-urban supply
Research Institute (IFPRI).
chains in sub-Saharan Africa. In Shackleton, C.M., Pasquini,
UN (2014). Proposal of The Open Working Group For M.W. and Drescher, A.W., (Eds.). African Indigenous
Sustainable Development Goals. 4 Aug 2014. Available Vegetables in Urban Agriculture. Earthscan, London. pp
at: http://www.un.org/en/ga/president/68/pdf/ 225–244.
letters/08042014_OWG%20Sustainable%20Goals.pdf
WHO (1981). International Code of Marketing of Breast-milk
Substitutes. World Health Organization, Geneva.

306 Connecting Global Priorities: Biodiversity and Human Health

WHO (2012a). Obesity and Overweight. (2012) WHO Fact Ahlenius, H. (2008). The economy of legal wildlife
Sheet No 311. May 2012. WHO, Geneva. trade. In Environment and Poverty Times #5: Pro-poor
growth issue; http://www.grida.no/graphicslib/detail/
WHO (2012b). Our Planet, our Health, our Future: Human
the-economy-of-legal-wildlife-trade_e1b8.
health and the Rio Conventions, Biological diversity, climate
change and desertification. Geneva. Akhavan D. (2000) Análise de Custo-efetividade do Programa
de Controle da Doença de Chagas no Brasil, Organização Pan-
Willcox, D.C. et al., (2009). The Okinawan Diet: Health
Americana da Saúde, Brasília, 271 pp.
Implications of a Low-Calorie, Nutrient-Dense, Antioxidant-
Rich Dietary Pattern Low in Glycemic Load. Journal of the Alderman, D. J. (1996). Geographical spread of bacterial and
American College of Nutrition, 28(4), pp.2–6. fungal diseases of crustaceans. In Preventing the spread of
aquatic animal diseases (B.J. Hill & T. Håstein, eds). Rev. sci.
Wolfe, N. D., Daszak, P., Kilpatrick, A. M., & Burke, D. S.
tech. Off. int. Epiz., 15 (2), 603–632.
(2005). Bushmeat hunting, deforestation, and prediction
of zoonotic disease. Emerging infectious diseases, 11(12), Allan, B. F., Keesing, F., & Ostfeld, R. S. (2003). Effect of forest
1822–1827. fragmentation on Lyme disease risk. Conservation Biology
17:267–272.
World Cancer Research Fund / American Institute for Cancer
Research (2007). Food, Nutrition, Physical Activity, and the Allen, H. K., Donato, J., Wang, H. H, Cloud-Hansen, K.
Prevention of Cancer: a Global Perspective. Washington DC, A., Davies, J., & Handelsman, J. (2010). Call of the wild:
AICR. antibiotic resistance genes in natural environments. Nature
Reviews Microbiology. 8:251–259.
Wunder, S., Angelsen, A., and Belcher, B. (2014). Forests,
Livelihoods, and Conservation: Broadening the Empirical Base. Amos, W. & Acevedo-Whitehouse, K. (2009). A new test for
World Development. DOI:10.1016/j.worlddev.2014.03.007 genotype-fitness associations reveals a single microsatellite
allele that strongly predicts the nature of tuberculosis
Xu, Y-K, Tao, G-D., Liu, H-M., Yan, K-L and Dao, X-S.
infections in wild boar. Molecular Ecology Resources. DOI:
(2004). Wild vegetable resources and market survey in
10.1111/j.1755–0998.2009.02560.x
Xishuangbanna, southwest China. Economic Botany, 58:
647–667. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales,
F. J., Epstein, P. R., Daszak, P. (2004). “Emerging infectious
Yamano, T. and Jayne, T.S. (2004). Measuring the impacts
diseases of plants: pathogen pollution, climate change and
of working age adult mortality among small-scale farm
agrotechnology drivers.” Trends in Ecology and Evolution
households in Kenya. World Development, 32: 323–335.
19:535–544.
Yang, R. and Keding, G.B. (2009). Nutritional contributions
Araujo, C. A., Waniek, P. J., Jansen, A. M. (2009). An
of important African Indigenous Vegetables. In Shackleton,
overview of Chagas disease and the role of Triatomine on its
C.M., Pasquini, M.W. and Drescher, A.W., (Eds.). African
distribution in Brazil. Vector Borne and Zoonotic Diseases,
Indigenous Vegetables in Urban Agriculture. Earthscan,
9: 227–234.
London. Pp. 105–135.
Armién AG, Armién B, Koster F, Pascale JM, Avila M ,
Zhang, Y., Y. Chen. Modeling and evaluating ecosystem in
Gonzalez P, de la Cruz M , Zaldivar Y, Mendoza Y, Gracia
1980s and 1990s for American lobster (Homarus americanus)
F, Hjelle B , Lee SJ, Yates TL & Salazar-Bravo J (2009).
in the Gulf of Maine. Ecological Modeling 203: 475–489
Hantavirus Infection and Habitat Associations among Rodent
(2007).
Populations in Agroecosystems of Panama: Implications for
Human Disease Risk. Am. J. Trop. Med. Hyg., 81(1): 59–66.
Chapter 7 Bandyopadhyay, R., Frederiksen. R. A. (1999). “Contemporary
Acevedo-Whitehouse, K., Gulland, F., Greig, D. & Amos, W. global movement of emerging plant diseases.” Annals of the
(2003). Inbreeding: disease susceptibility in California sea New York Academy of Sciences 894: 28–36.
lions. Nature 422, 35. Baize, S., Pannetier, D., Oestereich, L., Rieger, T., Koivogui,
Acevedo-Whitehouse, K., Vicente, J. ,Gortazar, C., Hofle, L., Magassouba, N. F., ... & Günther, S. (2014). Emergence of
U., Fernandez-de-Mera, I. G. & Amos, W. (2005) Genetic Zaire Ebola virus disease in Guinea – preliminary report. New
resistance to bovine tuberculosis in the Iberian wild boar. England Journal of Medicine.
Molecular Ecology 14, 3209–3217. Bastos EGMB; Araújo AFB & Silva HRS. (2005) Records of the
Acevedo-Whitehouse, K., Spraker, T. R., Lyons, E., Melin, S. rattlesnakes Crotalus durissus terrificus (Laurenti) (Serpentes,
R., Gulland, F., Delong, R. L., Amos, W. (2006) Contrasting Viperidae) in the State of Rio de Janeiro, Brazil: a possible case
effects of heterozygosity on survival and hookworm resistance of invasion facilitated by deforestation. Rev. Bras. Zool. 22 (3)
in California sealion pups. Molecular Ecology 15(7):1973–82. pp. 812–815

Afrane, Y.A.; Zhou, G.; Lawson , B.W.; Githeko, A.K.& Yan, Bourne, D. G., Garren, M., Work, T. M., Rosenberg, G. W.
G. Life-table analysis of Anopheles arabiensis in Western & Harvell, C. D. (2009). Microbial disease and the coral
Kenya highlands: effects of land covers on larval and adult holobiont. Trends in Microbiology 17(12): 554–562.
survivorship. American Journal of Tropical Medicine and
Hygiene, 77: 660–666, 2007.

Connecting Global Priorities: Biodiversity and Human Health 307

 Brearley, G., Rhodes, J., Bradley, A., Baxter, G., Seabrook, Cleaveland, S., Laurenson, K., & Mlengeya, T. (2005).
L., Lunney, D., Liu, Y., McAlpine, C. (2012). Wildlife disease “Impacts of Wildlife Infections on Human and Livestock
prevalence in human-modified landscapes. Biological Reviews Health with Special Reference to Tanzania: Implications for
88(2):427–442. Protected Area Management”. Chapter 20. IN: Conservation
and Development Interventions at the Wildlife/Livestock
Brown, A. W. A. (1977). Yellow fever, dengue and dengue
Interface- Implications for Wildlife, Livestock and Human
haemorrhagic fever. In A world geography of human diseases,
Health”. IUCN. Ed. Osofsky S.A.
ed. Howe, G.M. London: Academic Press, pp. 271–3127.
Cleaveland, S., Packer, C., Hampson, K., Kaare, M., Kock,
Bunnag, T., Sornmani, S., Pinithpongse, S. & Harinasuta,
R., Craft, M., Lembo, T., Mlengeya, T., Dobson, A. (2008).
C. (1979). Surveillance of water-borne parasitic infections
The multiple roles of infectious diseases in the serengeti
and studies on the impacts of ecological changes on vector
ecosystem. In: Sinclair ARE, Packer C, Mduma S, Fryxell JM
mosquitoes of malaria after dam construction. Southeast
(eds) In Serengeti III: Human impacts on dynamic ecosystems.
Asian J Trop Med Public Health, 10:656–660.
University of Chicago Press, Chicago, pp 209–240
Burge, C. A., Eakin, C. M., Friedman, C. S., Froelich, B.,
Cohen, J. E. (2003). Human population: The next half century.
Hershberger, P. K., Hoffman, E. E., Petes, L. E., Prager, K.
Science 302(5648):1172–1175.
C., Weil, E., Willis, B. L., Ford, S. E. & Harvell, C. D. (2014).
Climate change influences on marine infectious disease: Coluzzi, M. (1984). Heterogeneities of the malaria vectorial
implications for management and society. Annual Review in system in tropical Africa and their significance in malaria
Marine Science 6: 249–277. epidemiology and control. Bulletin WHO 62(suppl):107–113
Burge, C. A., Kim, C. J. S., Lyles, J. M., Harvell, C. D. (2013). Coluzzi, M. (1994). Malaria and the Afrotropical ecosystems:
Special Issue Oceans and Humans Health: the ecology of impact of man-made environmental changes. Parassitologia
marine opportunists. Microb. Ecol. 65:869–79. 36:223–227.
Butchart, S. H. M., Walpole, M., Collen, B., van Strien, A., Conrad, K. (2012). Trade bans: a perfect storm for poaching?
Scharlemann, J. P. W., Almond, R. E. A., Baillie, J. E. M., Tropical Conservation Science 5(3):245–254.
Bomhard, B., Brown, C., Bruno, J., Carpenter, K. E., Carr, G.
Couacy-Hymann, E., Bodjo, C., Danho, T., Libeau, G., Diallo,
M., Chanson, J., Chenery, A. M., Csirke, J., Davidson, N. C.,
A. (2005). Surveillance of wildlife as a tool for monitoring
Dentener, F., Foster, M., Galli, A., Galloway, J. N., Genovesi,
rinderpest and peste des petits ruminants in West Africa.
P., Gregory, R. D., Hockings, M., Kapos, V., Lamarque, J.-F.,
Rev. sci. tech. Off. int. Epiz., 24 (3), 869–877.
Leverington, F., Loh, J., McGeoch, M. A., McRae, L., Minasyan,
A., Morcillo, M. H., Oldfield, T. E. E., Pauly, D., Quader, S., Cox, C. M., Bockus, W. W., Holt, R. D., Fang, L., & Garrett, K.
Revenga, C., Sauer, J. R., Skolnik, B., Spear, D., Stanwell- A. (2013). Spatial connectedness of plant species: potential
Smith, D., Stuart, S. N., Symes, A., Tierney, M., Tyrrell, T. D., links for apparent competition via plant diseases. Plant
Vié, J.-C., & Watson. R. (2010). Global Biodiversity: Indicators Pathol. Doi: 10.1111.ppa.12045.
of Recent Declines. Science 328: 1164–1168.
Crowl, T. A., Crist, T. O., Parmenter, R. P., Belovsky, G. & Lugo,
Capinha, C., Larson, E. R., Tricario, E., Olden, J. D., Gherardi, A. E. (2008). “The Spread Of Invasive Species And Infectious
F. (2013). Effects of climate change, invasive species, and Disease As Drivers Of Ecosystem Change.” Frontiers In Ecology
disease on the distribution of native European crayfishes. And The Environment 6: 238–246.
Conservation Biology 27(4): 731–740.
Daszak, P., Zambrana-Torrelio, C., Bogich, T. L., Fernandez,
Cardona, G. A. & Carmena, D. (2013). A review of the global M., Epstein, J.H., Murray, K.A., Hamilton, H. (2013).
prevalence, molecular epidemiology and economics of cystic Interdisciplinary approaches to understanding disease
echinococcosis in production animals. Veterinary Parasitology, emergence: The past, present, and future drivers of Nipah
192:10–32. virus emergence. Proc Natl Acad Sci U S A. 110(Suppl 1):
3681–3688.
Castro, V., Rivera, C., Isard, S. A., Gamez, R., Fletcher, J. &
Irwin, M. (1992). The influence of weather and microclimate de Balogh, K., Halliday, J., & Lubroth, J. (2013). Integrating
on Dalbulus maidis (Homoptera: Cicadellidae) flight activity the surveillance of animal health, foodborne pathogens and
and the incidence of diseases within maize and bean foodborne diseases in developing and in-transition countries.
monocultures and bicultures in tropical America. Ann. Appl. Rev. sci. tech. Off. int. Epiz., 32 (2), 539–548.
Biol. 121:469–482.
DeFries, R. S., et al. (2010). Deforestation driven by urban
Charlwood J. D. & Alecrim, W. A. (1989). Capture-recapture population growth and agricultural trade in the twenty-first
studies with the South American malarial vector Anopheles century. Nature Geosci 3(3):178–181.
darlingi, Root. Ann Trop Med Parasitol 83:569–576
Dethlefsen, L., McFall-Ngai, M. & Relman, D. A. (2007).
Chomel, B., Belotto, A. & Meslin, F. (2007). “Wildlife, exotic Review Article An ecological and evolutionary perspective on
pets, and emerging zoonoses. Emerging Infectious Diseases 13: human–microbe mutualism and disease Nature 449, 811–818
6–11. doi:10.1038/nature06245
Domenach, J., Lubroth, J., & Sumption, K. (2010). Immune
Protection in Animals: The Examples of Rinderpest and Foot-
and-Mouth Disease. J. Comp. Path. 142: S120eS124.

308 Connecting Global Priorities: Biodiversity and Human Health

Dornelas, M., Gotelli, N. J., McGill, B., Shimadzu, H., Moyes, Foxcroft, L. C., Pyšek, P., Richardson, D. M., Genovesi, P. (eds)
F., Sievers, C. & Magurran, A. E. (2014). Assemblage time (2013). Plant invasions in protected areas: patterns, problems
series reveal biodiversity change but not systematic loss. and challenges. Springer, Dordrecht. http://www.springer.
Science 344:296–299. com/life+sciences/ecology/book/978–94–007–7749–1
Driscoll, E. E., Hoffman, J. I., Green, L. E., Medley, G. F., Friedman, C. S., Andree, K. B., Beauchamp, K., Moore, J.
Amos, W. (2011). A preliminary study of genetic factors that D., Robbins, T. T., et al. (2000). “Candidatus Xenohaliotis
influence susceptibility to bovine tuberculosis in the British californiensis”, a newly described pathogen of abalone,
cattle herd. PLoS One 6(4):e18806. Haliotis spp., along the west coast of North America. Int. J.
Syst. Evol. Microbiol. 50:847–55.
Dunn, R. R., Davies, T. J., Harris, N. C., & Gavin, M. C.
(2010). Global drivers of human pathogen richness and Garrett, K. A., Dobson, A. D .M., Kroschel, J., Natarajan, B.,
prevalence. Proceedings of the Royal Society B: Biological Sciences Orlandini, S., Tonnang, H. E. Z., & Valdivia, C. (2013). The
277:2587–2595. effects of climate variability and the color of weather time
series on agricultural diseases and pests, and on decisions for
Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris
their management. Agr. Forest Meteorol. 170:216–227.
AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin
R, Reise K, Stouffer DB, Thieltges DW, Williams RJ, Zander Gibbs, H. K., et al. (2010). Tropical forests were the primary
CD (2013) Parasites Affect Food Web Structure Primarily sources of new agricultural land in the 1980s and 1990s. Proc
through Increased Diversity and Complexity. PLoS Biol 11(6): Natl Acad Sci U S A 107(38):16732–7.
e1001579. doi:10.1371/journal.pbio.1001579.
Gilbert, M., Golding, N., Zhou, H., Wint, G.R.W., Robinson,
Dutta, M., Sokhandan B. N., Palmer, M. W., & Melcher, U. T.P., Tatem, A.J., Lai, S., Zhou, S., Jiang, H., Guo, D., Huang,
(2014). Genomic characterization of Ambrosia asymptomatic Z., Messina, J.P., Xiao, X., Linard, C., Boeckel, T.P. van, Martin,
virus 1 and evidence of other Tymovirales members in the V., Bhatt, S., Gething, P.W., Farrar, J.J., Hay, S.I. et al. 2014.
Oklahoma tallgrass prairie revealed by sequence analysis. Arch Predicting the risk of avian influenza A H7N9 infection in
Virol., in press. live-poultry markets across Asia. Nature Communications 5:
4116.
Estrada-Peña, A., Ostfeld, R. S., Peterson, A. T., Poulin, R.,
& de la Fuente, J. (2014). Effects of environmental change Gottdenker, N.L., Streicker, D.G., Faust, C.L., & Carroll,
on zoonotic disease risk: an ecological primer. Trends in C.R. (2014). Anthropogenic land use change and infectious
Parasitology 30:205–214. diseases: A review of the evidence. Ecohealth.
Ezenwa, V. O., Godsey, M. S., King, R. J., & Guptill, S. C. (2006). Grace, D., Mutua, F., Ochungo, P., Kruska, R., Jones, K.,
Avian diversity and West Nile virus: testing associations Brierley, L., Lapar, L., Said, M., Herero, M., Phuc, P. M. Thao,
between biodiversity and infectious disease risk. Proceedings N. B., Akuku, I. & Ogutu, F. (2012). Mapping of poverty and
of the Royal Society B: Biological Sciences 273:109–117. likely zoonoses hotspots. Zoonoses Project 4. Report to the
UK Department for International Development. Nairobi,
Ezenwa, V. O. & Jolles, A. E. (2011). From host immunity to
Kenya: ILRI.
pathogen invasion: the effects of helminth coinfection on the
dynamics of microparasites. Integrated Comparative Biology Hacker, K. P., Seto, K. C., Costa, F., Corburn, J., Mitermayer, G.
51(4):540–51. R., Ko, A. I., Duik-Wasser, M. (2013). Urban slum structure:
integrating socioeconomic and land cover data to model slum
Feldmann H. and Geisbert T.W. (2011) Ebola haemorrhagic
evolution in Salvador, Brazil. Int J Health Geogr. 12: 45.
fever. The Lancet 377:849–62.
Hansen, M. C., et al. (2013). High-Resolution Global
Ferreira LF; Araujo AJG; Confalonieri U; Nunez L. (1984) The
Maps of 21st-Century Forest Cover Change. Science
finding of Diphyllobothrium in human coprolites (4.100–1.950
342(6160):850–853.
BC) from northern Chile. Memórias do Instituto Oswaldo
Cruz, Rio de Janeiro, v. 79, p. 775–780 Harvell, C. D., Jordan-Dahlgren, E., Merkel, S., Rosenberg.
E., Raymundo, L., et al. (2007). Coral disease, environmental
Fletcher, J., Franz, D., & LeClerc, J. E. (2009). Healthy Plants:
drivers, and the balance between coral and microbial
Necessary for a Balanced ‘One Health’ Concept. Veterinaria
associates. Oceanography 20(1):172–195
Italiana 45 (1) / January – March 2009. http://www.izs.it/
vet_italiana/2009/45_1/45_1.htm Harwood, J., Hall, A. (1990). Mass mortality in marine
mammals  – its implications for population-dynamics and
Food and Agriculture Organization of the UN (FAO). Plants.
genet-ics. Trends in Ecology & Evolution 5:254–257.
http://www.fao.org/biodiversity/components/plants/en/
Hatcher, M. J., Dick, J. T. A., & Dunn, A. M. (2012). Disease
Food and Agriculture Organization of the UN (FAO). (2013).
emergence and invasions. Functional Ecology 26, 1275–1287.
World Livestock 2013- Changing disease landscapes. Ed.
Slingenbergh, J. Rome. Hethcote, H. W., Wang, W., Han, L., Ma, Z. (2004). A
predator–prey model with infected prey. Theoretical Population
Ford, S. E., Tripp, M. R. (1996). Disease and defense
Biology 66(3), Pages 259–268.
mechanisms. In The Eastern Oyster: Crassostrea virginica,
ed. VS Kennedy, RLE Newell, AE Eble, pp. 581–660. College Holdo, R. M., Sinclair. A. R. E., Dobson, A. P., Metzger, K.
Park: Univ. Md. Sea Grant L., Bolker, B. M., et al. (2009). A Disease-Mediated Trophic
Cascade in the Serengeti and its Implications for Ecosystem
PLoS Biol 7(9): e1000210.doi:10.1371/journal.pbio.1000210.

Connecting Global Priorities: Biodiversity and Human Health 309

 Holt, R.D. (2008). The community context of disease Keesing, F., Holt, R. D., & Ostfeld, R. S. (2006). Effects of
emergence: could changes in predation be a key driver? species diversity on disease risk. Ecology Letters 9:485–498.
Pages 324–346 in R.S. Ostfeld, F. Keesing and V.T. Eviner,
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C.
eds. Infectious Disease Ecology: Effects of Ecosystems on
D, Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitcell, C.
Disease and of Disease on Ecosystems. Princeton University
E., Myers, S. S., Bogich, T., Ostfeld, R. S. (2010). Impacts of
Press, Princeton, NJ.
biodiversity on the emergence and transmission of infectious
Huchzermeyer,  F. W., Penrith, M. L., Elkan, P. W. (2001). diseases. Nature 468(7324):647–52.
Multifactorial mortality in bongos and other wild ungulates
Khan, S. U., Gurley, E. S., Hossain, M. J., Nahar ,N., Sharker,
in the north of the Congo Republic. Onderstepoort J Vet Res
M. A. Y., et al. (2012). A Randomized Controlled Trial of
68(4):263–9.
Interventions to Impede Date Palm Sap Contaminated by
Hudson, P. J., Dobson, A. P. & Newborn, D. (1998). Bats to Prevent Nipah Virus Transmission in Bangladesh.
Prevention of population cycles by parasite removal. Science PLoS ONE 7(8):e42689.
282:2256–2258.
Kock, R. (2014). Drivers of disease emergence and spread:
Ingram, D.S.  (2014). Biodiversity and plant pathogens Is wildlife to blame?.Onderstepoort J Vet Res, North America,
and conservation. APS Features. https://www.apsnet.org/ 81. Date accessed: 28 Jul. 2014. Available at: http://www.ojvr.
publications/apsnetfeatures/Pages/ICPP98Ingram.aspx org/index.php/ojvr/article/view/739.
Johnson, P. T., Preston, D. L., Hoverman, J. T., & LaFonte, B. Kock, R. (2013). Will the damage be done before we feel the
E. (2013a). Host and parasite diversity jointly control disease heat? Infectious disease emergence and human response.
risk in complex communities. Proceedings of the National Animal Health Research Reviews, pg. 1–6 doi:10.1017/
Academy of Sciences 110:16916–16921. S1466252313000108
Johnson, P. T., Preston, D. L., Hoverman, J. T., & Richgels, Kurath, G., Winton, J. (2011). Complex dynamics at the
K. L. (2013b). Biodiversity decreases disease through interface between wild and domestic viruses of finfish. Curr.
predictable changes in host community competence. Nature Opin. Virol. 1:73–80
494:230–233.
Lambin, E. F. & Meyfroidt, P. (2011). Global land use change,
Johnson, P. T., Rohr, J. R., Hoverman, J. T., Kellermanns, E., economic globalization, and the looming land scarcity. Proc
Bowerman, J. & Lunde, K. B. (2012). Living fast and dying Natl Acad Sci U S A. 108(9):3465–72.
of infection: host life history drives interspecific variation in
Leroy, E. M., Rouquet, P., Formenty, P., Souquiere, S.,
infection and disease risk. Ecology Letters 15:235–242.
Kilbourne, A., Froment, J. -M., Bermejo, M., Smit, S., Karesh,
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, W., Swanepoel, R., Zaki, S. R., Rollin, P. E. (2004). Multiple
D., Gittleman, J. L, & Daszak, P. (2008). Global trends in Ebola Virus Transmission Events and Rapid Decline of
emerging infectious diseases. Nature 451:990–993. Central African Wildlife. Science 303: 387–390.
Jones, B. A., Grace, D., Kock, R., Alonso, S., Rushton, J., & Lessios, H. A., Robertson, D. R., Cubit, J. D. (1984). Spread
Said, M. Y. (2013). Zoonosis emergence linked to agricultural of Diadema mass mortality throughout the Caribbean. Science
intensification and environmental change, PNAS 110(21), 226:335–37.
8399–8404. doi:10.1073/pnas.1208059110
Liverani, M. et al. (2013). Understanding and Managing
Joseph, M. B., Mihaljevic, J. R., Orlofske, S. A., & Paull, S. H. Zoonotic Risk in the New Livestock Industries. Environmental
(2013). Does life history mediate changing disease risk when Health Perspectives 121(8):873–877.
communities disassemble? Ecology Letters 16:1405–1412.
(a) Luby, S.P., Gurley, E.S., Hossain, M.J. (2009). Transmisison
Karesh, W. B. & Cook, R. A. (2005). The Human-Animal Link. of Human Infection with Nipah Virus. Clinical Infectious
Foreign Affairs 84(4):38–50. Diseases. 49(11):1743–1748.
Karesh, W. B., Cook, R. A., Bennett, E. L., Newcomb, J. (b) Luby, S.P., Hossain, M.J., Gurley, E.S., Ahmed, B.-N., Banu,
(2005). Wildlife trade and global disease emergence, Emerging S., Khan, S.U., et al. (2009). Recurrent Zoonotic Transmission
Infectious Diseases, 11: 7, 1000–1002. of Nipah Virus into Humans, Bangladesh, 2001–2007.
Emerging Infectious Diseases 15(8).
Karesh, W. B., Dobson, A., Lloyd-Smith, J. O., Lubroth,
J., Dixon, M. A., Bennett, M., Aldrich, S., Harrington, T., Loh, EH, Olival, KJ, Zambrana-Torellio, C, Bogich, TL,
Formenty, P., Loh, E. H., Machalaba, C. C., Thomas, M. J., Johnson, CK, Mazet, JAK, Karesh, WB, Daszak, P. Targeting
& Heymann, D. L. (2012). Ecology of zoonoses: natural and transmission pathways for emerging zoonotic disease
unnatural histories. Lancet 380:1936–1945. surveillance and control. Vector Borne and Zoonotic Diseases.
In press.
Karesh, W. B., Smith, K. M., Asmussen, M. (2012). The
unregulated and informal trade in wildlife: implications for Luquet, E., Garner, T. W., Léna, J. P., Bruel, C., Joly,
biodiversity and health. In: Animal Health and Biodiversity – P., Lengagne, T., Grolet, O., Plénet, S. (2012). Genetic
Preparing for the Future. Compendium of the OIE Global erosion in wild populations makes resistance to a
Conference on Wildlife.  23–25 February 2011. Paris, Pp pathogen more costly. Evolution 66(6):1942–1952. doi:
51–57.  10.1111/j.1558–5646.2011.01570.x.

310 Connecting Global Priorities: Biodiversity and Human Health

Mack, R., Simberloff D., Lonsdale W., Evans H., Clout M. & Murray, K. A., & Daszak, P. (2013). Human ecology in
Bazzaz F. (2000). “Biotic invasions: causes, epidemiology, pathogenic landscapes: two hypotheses on how land use
global consequences, and control.” Ecological Applications 10: change drives viral emergence. Current Opinion in Virology,
689–710. 3(1), 79–83. doi:10.1016/j.coviro.2013.01.006
Machalaba C. and Karesh W.B. “Other Relevant International Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford,
Standards to the Control of Rabies”. Rabies Control – Towards K. H., Ricketts, T. H., Turner, W. R., & Osofsky, S. A. (2013).
Sustainable Prevention at the Source. Compendium of the Human health impacts of ecosystem alteration. Proceedings of
OIE Global Conference on Rabies Control. 2012. Available the National Academy of Sciences 110:18753–18760.
at: http://www.oie.int/doc/ged/d12061.pdf
Newcomb, J., Harrington, T., Aldrich, S. (2011). The Economic
Marcogliese, D. J. (2002). Food webs and the transmission Impact of Selected Infectious Disease Outbreaks. Cambridge,
of parasites to marine fish Parasitology. 124 Suppl:S83–99. MA: Bio Economic Research Associates.
Marques, A. C. (1987). Human migration and the spread of Nóbrega, A.A., Garcia, M.H., Tatto, E., Obara, M.T., Costa, E.,
malaria in Brazil. Parasitol Today 3:166–170. Sobel, J. & Araujo, W.N. (2009). Oral Transmission of Chagas
Disease by Consumption of Açaí Palm Fruit, Brazil. Emerg
Mazza, G., Tricarico, E., Genovesi, P., & Gherardi,
Infect Dis. 15(4): 653–655.
F. (2013). “Biological invaders are threats to human
health: an overview.” Ethology Ecology & Evolution, DOI: Oliveira-Ferreira, J.,  Lacerda, M.V.,  Brasil, P.,  Ladislau,
10.1080/03949370.2013.863225 J.L.,  Tauil, P.L.,  Daniel-Ribeiro, C.T. (2010). Malaria
in Brazil: an overview. Malar J.  30; 9:115. doi:
McVicar, A. H. (2011). Ichthyophonus. In Fish Diseases and
10.1186/1475–2875–9-115.
Disorders, Vol. 3: Viral, Bacterial, and Fungal Infections, ed.
PTK Woo, DW Bruno, pp. 721–47. Cambridge, MA: CAB Olson, S.H., Reed, P., Cameron, K.N., Ssebide, B.J., Johnson,
Int. 2nd ed. C.K., Morse, S.S., Karesh, W.B., Mazet, J.A.K., Joly, D.O.
(2012). Dead or alive: animal sampling during Ebola
Meira, A.M., Cooper, M., Ferraz, K.M.P.M.B., Monti, J.A.,
hemorrhagic fever outbreaks in humans. Emerg Health Threats
Caramez, R.B. & Delitti, W.B.C. (Orgs) (2013). Febre maculosa:
J 5:9134.
dinâmica da doença, hospedeiros e vetores. Universidade de
São Paulo, ESALQ, 175p. Ostfeld, R.S., & Holdt, R.D. (2004). Are predators good for
health? Evaluating evidence for top-down regulation of
Messenger, A. M., Barnes, A. N., Gray, G. C. (2014). Reverse
zoonotic disease reservoirs. Ecol. Evironm 2(1): 13–20.
Zoonotic Disease Transmission (Zooanthroponosis): A
Systematic Review of Seldom- Documented Human Biological Ostfeld, R. S., & Keesing, F. (2012). Effects of host diversity
Threats to Animals. PLOS One. 9(2): e89055. on infectious disease. Annual Review of Ecology, Evolution, and
Systematics 43:157.
Miller, R.S., Farnsworth, M.L., & Malmberg J.L. (2013).
Diseases at the livestock-wildlife interface: Status, challenges, Pagan, I., Gonzalez-Jara, P. Moreno-Letelier, A., Rodelo-
and opportunities in the United States. Preventive Veterinary Urrego, M., Fraile, A., Pinero, D., & Garcia-Arenal, F. (2012).
Medicine. 110(2):119–132. Effect of biodiversity changes in disease risk: exploring
disease emergence in a plant-virus system. PLoS Pathogens
Mills, J.N. (2006) Biodiversity loss and emerging infectious
8:e1002796. Doi:10.1371/journal.ppat.1002786.
disease: An example from the rodent-borne hemorrhagic
fevers Biodiversity 7(1). Palma, R.E., Polop, J.J., Owen, R.D., Mills, J.N. (2012).
Ecology of rodent-associated hantaviruses in the southern
Ministério da Saúde. (2005). Guia de Vigilância
cone of South America: Argentina, Chile, Paraguay, and
Epidemiológica – BVS Ministério da Saúde, 6ª edição –www.
Uruguay. Journal of Wildlife Diseases, 45(2): 267–281.
bvsms.saude.gov.br/bvs/publicacoes,
Paterson, S., Wilson, K. & Pemberton, J. M. (1998). Major
Ministério da Saúde. (2006). Guia de Vigilância
histocompatibility complex variation associated with juvenile
Epidemiológica – Ministério da Saúde, 7ª edição. www. bvsms.
survival and parasite resistance in a large unmanaged ungulate
saude.gov.br/bvs/publicacoes
population (Ovis aries L.). Proceedings of the National Academy
Morozov, A. & Best, A. (2012). Predation on infected host of Sciences of the United States of America 95, 3714–3719.
promotes evolutionary branching of virulence and pathogens’
Patz, JP, Daszak, P., Tabor, G.M., Aguirre, A.A.; Pearl, M.,
biodiversity. Journal of theoretical biology. 307C:29–36.
Epstein, J., Wolfe, N.D., Kilpatrick, A.M., Foufopoulos, J.,
Moura, J.F., Roges, E.M., Souza, R.L., Siciliano, S. & Rodrigues, Molyneux, D., & Bradley, D.J. (2004). Unhealthy Landscapes:
D.P. (2012). Marine Environment and Public Health, Policy Recommendations on Land Use Change and Infectious
Biodiversity Conservation and Utilization in a Diverse World, Disease. Environ Health Perspect. 112(10): 1092–1098.
Gbolagade Akeem Lameed (Ed.), ISBN: 978–953–51–0719–4,
Patz, J. A., Graczyk, T. K., Geller, N., & Vittor, A. Y. (2000).
InTech, Available from: http://www.intechopen.com/books/
Effects of environmental change on emerging parasitic
biodiversity-conservation-and-utilization-in-a-diverse-world/
diseases. International journal for parasitology, 30(12),
marine-environment-and-public-health
1395–1405.
Mundt, C.C. (2002). Use of multiline cultivars and cultivar
Pejchar, L. & Mooney, H. (2009). “Invasive Species, Ecosystem
mixtures for disease management. Annual Review of
Services, and Human Well-being.” Trends in Ecology and
Phytopathology 40:381–410.
Evolution 24:9, 497–504.

Connecting Global Priorities: Biodiversity and Human Health 311

 Perkins, S., et al. (2010). “Invasion Biology and Parasitic Rouquet, P., Froment, J.-F., Bermejo, M., Kilbourn, A., Karesh,
Infections.” IN O. Ostfeld, F. Keesing, and V. Eviner, eds. W.B., Reed, P., Kumulungui, B., Yaba, P., Delicat, A., Rollin,
Infectious Disease Ecology: Effects of Ecosystems on Disease and of P.E., Leroy, E.M. (2005). Wild Animal Mortality Monitoring
Disease on Ecosystems (Princeton University Press), 179–207. and Human Ebola Outbreaks, Gabon and Republic of Congo,
2001–2003. Emerging Infectious Diseases 11(2):283–290.
Pfleeger, T. G. & Mundt, C. E. (1998). Wheat rust severity as
affected by plant density andspecies proportions in simple Salkeld, D. J., Padgett, K. A., & Jones, J. H. (2013). A meta-
communities of wheat and wild oats. Phytopathology 88: analysis suggesting that the relationship between biodiversity
708–714. and risk of zoonotic pathogen transmission is idiosyncratic.
Ecology Letters 16:679–686.
Phalan, B., et al. (2013). Crop expansion and conservation
priorities in tropical countries. PLoS One 8(1):e51759. Santini, A., et al. (2013). “Biogeographical patterns and
determinants of invasion by forest pathogens in Europe.”
Pimentel, D., Zuniga, R., Morrison, D. (2005). Update on the
New Phytologist 197: 238–250.
environmental and economic costs associated with alien-
invasive species in the United States. Ecological Economics Schneider, M.C., Aron, J., Santos-Burgoa, C., Uieda, W., Ruiz-
52; 273–288. Velazco, S. (2001). Common vampire bat attacks on humans
in a village of the Amazon region of Brazil. Cad. Saúde Pública,
Pinto, J., Bonacic, C., Hamilton-West, C., Romero, J., Lubroth,
Rio de Janeiro, 17(6):1531–1536.
J. (2008). Climate change and animal diseases in South
America. Rev. sci. tech. Off. int. Epiz., 27(2):599–613. Secretariat of the Convention on Biological Diversity. (2010).
Global Biodiversity Outlook 3. Montreal.
Poulin, R. (2010). Network analysis shinnig light on parasite
ecology and diversity. Trends in Parasitology 26:492–498. Seto, K., Güneralp, B., Hutyra, L. R. (2012). Global forecasts of
urban expansion to 2030 and direct impacts on biodiversity
Previtali, M. A., Ostfeld, R. S., Keesing, F., Jolles, A. E.,
and carbon pools. Proc. Natl Acad. Sci. USA 109, 16 083–16
Hanselmann, R. & Martin, L. B. (2012). Relationship between
088. 
pace of life and immune responses in wild rodents. Oikos
121:1483–1492. Shin, Y. J., Rochet, M.J., Jennings, S., Field, J.G. & Gislason, H.
(2005). Using size-based indicators to evaluate the ecosystem
Rahman, S.A. et al. (2013). Risk Factors for Nipah Virus
effects of fishing ICES Journal of Marine Science 62(3) :
Infection among Pteropid Bats, Peninsular Malaysia. Emerging
384–396 http://dx.doi.org/10.1016/j.icesjms.2005.01.004
Infectious Diseases 19(1).
Singh, N., Singh, O. P. & Soan, V. (1989). Mosquito breeding
Randolph, S. E. & Dobson, A. D. M. (2012). Pangloss revisited:
in rice fields and its role in malaria transmission in Mandla
a critique o the dilutione effect and the biodiversity-buffers-
district, M.P. Indian J Malariology, 26(4):191–8.
disease paradigm. Parasitology 139, 847–863.
Smith, K. M., Loh, E., Rostal, M., Zambrana-Torrelio, C.,
Rapport, D. J., Daszak, P., Froment, A., Guegan, J. F., Lafferty,
Daszak, P. (2013). Pathogens, pests and economics: Drivers
K. D., Larigauderie, A., Mazumder, A., & Winding, A. (2009).
of honey bee colony declines and losses. EcoHealth, 10(4):
The impact of Anthropogenic stress at global and regional
434–45.
scales on biodiversity and health. In Biodiversity change and
human health: From ecosystem services to spread of disease. Stentiford, G. D., Neil, D. M., Peeler, E. J., Shields, J. D., Small,
(Eds) Osvaldo E. Sala, Laura A. Meyerson, Camille Parmesan. H. J., et al. (2012). Disease will limit future food supply from
Island Press, Washington, USA the global crustacean fishery and aquaculture sectors. J.
Invertebr. Pathol. 110:141–57.
Reed, P.E., Mulangu, S., Cameron, K.N., Ondzie, A.U., Joly, D.,
et al. (2014). A New Approach for Monitoring Ebolavirus in Stoett, P. (2010). Framing bioinvasion: biodiversity, climate
Wild Great Apes. PLoS Negl Trop Dis 8(9): e3143. doi:10.1371/ change, security, trade, and global governance. Global
journal.pntd.0003143. Governance: A Review of Multilateralism and International
Organizations, 16(1), 103–120.
Richards, A. L., Jiang, J., Omulo, S., Dare, R., Abdirahman, K.,
Ali, A., Sharif, S. K., Feikin, D. R., Breiman, R. F., & M. Kariuki Strieder, M.N., Santos, J.E.  &  Vieira, E.M.  (2006).
Njenga, M. K. (2010). Human Infection with Rickettsia Distribution, abundance and diversity of Simuliidae (Diptera)
felis, Kenya. Emerging Infectious Diseases 16(7), 1081–6. in an impacted watershed in southern Brazil.  Rev. Bras.
doi:10.3201/eid1607.091885. Entomol vol.50, n.1, pp. 119–124. ISSN 0085–5626.  http://
dx.doi.org/10.1590/S0085–56262006000100018.
Rocha, F.L., Roque, A.L.R., Arrais, R.C., Santos, J.P., Lima,
V.S., Xavier, S.C.C., Cordeiro-Estrela, P., D’andrea, P.S., Jansen, Sutherland, K. P., Porter, J. W., Torres, C. (2004). Disease
A.M. (2013). Trypanosoma cruzi TcI and TcII transmission and immunity in Caribbean and Indo-Pacific zooxanthellate
among wild carnivores, small mammals and dogs in a corals. Mar Ecol Prog Ser. 266: 273–302.
conservation unit and surrounding areas, Brazil. Parasitology
Sutherst, R. W. (1993). Arthropods as disease vectors in a
(Cambridge. Online), v. 140, p. 160–170.
changing environment. Environmental Change and Human
Roque, A.L.R., Xavier, S.C., D’Andrea, P.S. & Jassen, A.M. Health. Ciba Foundation Sym, 175, 124–145.
(2008). Trypanosoma cruzi transmission cycle among wild
and domestic mammals in three areas of orally transmitted
Chagas disease outbreaks. American Journal of Tropical
Medicine and Hygiene, 95:742–749.

312 Connecting Global Priorities: Biodiversity and Human Health

Suzán, G., Marcé, E., Giermakowski, J. T., Mills, J. N., Ceballos, Vittor, A. Y., Pan, W., Robert, H., Gilman, R. H., Tielsch,
G., Ostfeld, R. S., Armién, B., Pascale, J. M., & Yates, T. L. J., Glass, G., Shields, T., Sánchez-Lozano, W., Pinedo, V. V.,
(2009). Experimental evidence for reduced rodent diversity Salas-Cobos, E., Silvia Flores, S. & Patz. J.A. (2009). Linking
causing increased hantavirus prevalence. PLoS One 4:e5461. deforestation to malaria in the Amazon: Characterization of
the breeding habitat of the principal malaria vector, Anopheles
Swei, A., Rowley, J. J., Rödder, D., Diesmos, M. L., Diesmos, A.
darling. Am. J. Trop. Med. Hyg., 81(1): 5–12.
C., Briggs, C. J., Brown, R., Cao, T. T., Cheng, T. L., & Chong, R.
A. (2011). Is chytridiomycosis an emerging infectious disease Vourc’h, G., Plantard, O. & Morand, S. (2012). How Does
in Asia? PLoS One 6:e23179. Biodiversity Influence the Ecology of Infectious Disease?
Dordrecht: Springer.
Tadei, W. P., Thatcher, B. D., Santos, J. M. Scarpassa, V. M.,
Rodrigues, I. B. & Rafael, M. S. (1998). Ecologic observation Walsh, P. D., Abernethy, K. A., Bermejo, M., Beyers, R., De
on anopheline vectors of malaria in the Brazilian Amazon. Wachter, P., Akou, M. E., ... & Wilkie, D. S. (2003). Catastrophic
Am J Trop Med Hyg 59:325–335. ape decline in western equatorial Africa. Nature, 422(6932),
611–614.
Takahashi, C. K., Lourenço, N. G. G. S., Lopes, T. F., Rall, V.
L. M. & Lopes, C. A .M. (2008). “Ballast water: a review of Wolfe, N. D., et al. (2005) Bushmeat hunting, deforestation
the impact on the world public health.” Journal of Venomous and prediction of zoonotic emergence. Emerging Infectious
Animals and Toxins Including Tropical Diseases 14 (3): 393–408. Diseases 11:1822–1827.
Taylor, L. H., Latham, S. M. & Mark, E. (2001). Risk factors Wood, C. L. & Lafferty, K. D. 2013. Biodiversity and disease:
for human disease emergence. Philosophical Transactions a synthesis of ecological perspectives on Lyme disease
of the Royal Society of London. Series B: Biological Sciences transmission. Trends in Ecology & Evolution 28:239–247.
356:983–989.
Wood, C. L., Lafferty, K. D., DeLeo, G., Young, H. S., Hudson,
Terborgh, J., Lopez, L., Nuñez, P., Rao, M.,  Shahabuddin, G., P. J. & Kuris, A. M. (2014). Does biodiversity protect humans
Orihuela, G., Riveros, M., Ascanio, R.,  Adler, G.H., Lambert, against infectious disease? Ecology 95:817–832.
D.T.,  Balbas, L. (2001). Ecological Meltdown in Predator-
World Bank (2012). People, pathogens and our
Free Forest Fragments Science  30  Vol. 294  no. 5548  pp.
planet: the economics of One Health. Washington,
1923–1926 
DC: World Bank. Available at: http://documents.
Thomson, G. R, Penrith, M.-L., Atkinson, M. W., Atkinson, w o r l d b a n k . o r g / c u ra t e d / e n / 2 0 1 2 / 0 6 / 1 6 3 6 0 9 4 3 /
S. J., Cassidy, D. & Osofsky, S. A. (2013). Balancing Livestock people-pathogens-planet-economics-one-health
Production and Wildlife Conservation in and around Southern
World Health Organization (WHO). (2015). One year into
Africa’s Transfrontier Conservation Areas. Transboundary and
the Ebola outbreak: a deadly, tenacious and unforgiving virus.
Emerging Diseases. 60:492–506.
http://www.who.int/csr/disease/ebola/one-year-report/
Valle, D., & Clark, J. (2013). Conservation efforts may increase ebola-report-1-year.pdf?ua=1
malaria burden in the Brazilian Amazon. PLoS One 8:e57519.
World Organisation for Animal Health (OIE). (2012)
Van Gils, J. A, Munster, V. J., Radersma, R., Liefhebber, Guidelines for Assessing the Risk of Non-Native Species
D., Fouchier, R. A. M., & Klaassen, M. (2007). Hampered Becoming Invasive. Paris, France. http://www.oie.int/
foraging and migratory performance in swans infected with fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/
low-pathogenic avian influenza A virus. PLoS One, 2(1), e184. OIEGuidelines_NonNativeAnimals_2012.pdf
doi:10.1371/journal.pone.0000184
Young, H., R. H. Griffin, C. L. Wood, & C. L. Nunn. (2013).
Varella, C. L., Xavier, S. C., Herrera, H. M., Jansen, A. M. Does habitat disturbance increase infectious disease risk for
(2009). The ecology of the Trypanosoma cruzi transmission primates? Ecology Letters 16:656–663.
cycle: Dispersion of Zymodeme 3(Z3) in wild hosts of
Young, H. S., Dirzo, R., Helgen, K. M., McCauley, D. J.,
Brazilian biomes. Veterinary Parasitology, 10:19–24.
Billeter, S. A., Kosoy, M. Y. Osikowicz, L. M., Salkeld, D. J.,
Vasconcelos, C. H., Novo, E.M.L.M. & Donalisio, M.R. (2006). Young, T. P., & Dittmar, K. (2014). Declines in large wildlife
Uso do sensoriamento remoto para estudar a influência de increase landscape-level prevalence of rodent-borne disease
alterações ambientais na distribuição da malária na Amazônia in Africa. Proceedings of the National Academy of Sciences
brasileira. Cad. Saúde Pública, 22(3): 517–526. 111:7036–7041.
Vilà, M., Basnou, C., Pyšek, P., Josefsson, M., Genovesi,
P., Gollasch, S., Nentwig, W., Olenin, S., Roques, A., Roy, Chapter 8
D., & Hulme, P. E. (2010). How well do we understand the
impacts of alien species on ecosystem services? A pan- Aichbhaumik N, Zoratti EM, Strickler R, Wegienka G,
European, cross-taxa assessment. Frontiers in Ecology and the Ownby DR, Havstad S, Johnson CC. 2008. Prenatal exposure
Environment, 8: 135–144. to household pets influences fetal immunoglobulin E
production. Clin Exp Allergy. 38(11): 1787–1794.

Connecting Global Priorities: Biodiversity and Human Health 313

 Andersson MA, Mikkola R, Kroppenstedt RM, Rainey FA, Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM,
Peltola J, Helin J, Sivonen K, Salkinoja-Salonen MS. 1998. Delzenne NM, Burcelin R. 2008. Changes in gut microbiota
The mitochondrial toxin produced by Streptomyces griseus control metabolic endotoxemia-induced inflammation in
strains isolated from an indoor environment is valinomycin. high-fat diet-induced obesity and diabetes in mice. Diabetes.
Appl Environ Microbiol. 64(12): 4767–4773. 57(6): 1470–1481.
Aspinall P, Mavros P, Coyne R, Roe J. 2013. The urban brain: Carrigan MA, Uryasev O, Frye CB, Eckman BL, Myers CR,
analysing outdoor physical activity with mobile EEG. Br J Hurley TD, Benner SA. 2014. Hominids adapted to metabolize
Sports Med. ethanol long before human-directed fermentation. Proc Natl
Acad Sci U S A. 112(2): 458–463.
Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T,
Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, et al. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor
2011. Induction of Colonic Regulatory T Cells by Indigenous EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan
Clostridium Species. Science. 331: 337–341. B, O’Sullivan O, et al. 2012. Gut microbiota composition
correlates with diet and health in the elderly. Nature.
Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster
488(7410): 178–184.
MT, Perloski M, Liberg O, Arnemo JM, Hedhammar A,
Lindblad-Toh K. 2013. The genomic signature of dog Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. 2009.
domestication reveals adaptation to a starch-rich diet. Nature. Cancer-related inflammation, the seventh hallmark of cancer:
495(7441): 360–364. links to genetic instability. Carcinogenesis. 30(7): 1073–1081.
Babu S, Blauvelt CP, Kumaraswami V, Nutman TB. 2006. Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-
Regulatory networks induced by live parasites impair Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, et al.
both Th1 and Th2 pathways in patent lymphatic filariasis: 2013. Out-of-Africa migration and Neolithic coexpansion
implications for parasite persistence. J Immunol. 176(5): of Mycobacterium tuberculosis with modern humans. Nat
3248–3256. Genet. 45(10): 1176–1182.
Bach JF. 2002. The effect of infections on susceptibility to Correale J, Farez M. 2007. Association between parasite
autoimmune and allergic diseases. N Engl J Med. 347(12): infection and immune responses in multiple sclerosis. Ann
911–920. Neurol. 61(2): 97–108.
Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte Correale J, Farez MF. 2013. Parasite infections in multiple
M. 2011. Exposure to a social stressor alters the structure of sclerosis modulate immune responses through a retinoic acid-
the intestinal microbiota: implications for stressor-induced dependent pathway. J Immunol. 191(7): 3827–3837.
immunomodulation. Brain Behav Immun. 25(3): 397–407.
Cuzick J, Otto F, Baron JA, Brown PH, Burn J, Greenwald P,
Balkwill F. 2009. Tumour necrosis factor and cancer. Nat Rev Jankowski J, La Vecchia C, Meyskens F, Senn HJ, et al. 2009.
Cancer. 9(5): 361–371. Aspirin and non-steroidal anti-inflammatory drugs for cancer
prevention: an international consensus statement. Lancet
Benn CS, Melbye M, Wohlfahrt J, Bjorksten B, Aaby P. 2004.
Oncol. 10(5): 501–507.
Cohort study of sibling effect, infectious diseases, and risk
of atopic dermatitis during first 18 months of life. Brit Med Dadvand P, de Nazelle A, Figueras F, Basagana X, Su J, Amoly
J. 328: 1223–1228. E, Jerrett M, Vrijheid M, Sunyer J, Nieuwenhuijsen MJ. 2012.
Green space, health inequality and pregnancy. Environ Int.
Borody TJ, Brandt LJ, Paramsothy S, Agrawal G. 2013. Fecal
40: 110–115.
microbiota transplantation: a new standard treatment option
for Clostridium difficile infection. Expert Rev Anti Infect Ther. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet
11(5): 447–449. JB, Massart S, Collini S, Pieraccini G, Lionetti P. 2010. Impact
of diet in shaping gut microbiota revealed by a comparative
Bowers RM, McLetchie S, Knight R, Fierer N. 2011. Spatial
study in children from Europe and rural Africa. Proc Natl Acad
variability in airborne bacterial communities across land-use
Sci U S A. 107(33): 14691–14696.
types and their relationship to the bacterial communities of
potential source environments. ISME J. 5(4): 601–612. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim
EK, Lanctot KL. 2010. A meta-analysis of cytokines in major
Breidt F, McFeeters RF, Perez-Diaz I, Lee CW. 2013. Fermented
depression. Biol Psychiatry. 67(5): 446–457.
vegetables. In: Doyle MP and Buchanan, RL editors. Food
Microbiology: Fundamentals and Frontiers. Washington: Dunder T, Tapiainen T, Pokka T, Uhari M. 2007. Infections
ASM Press. p. in child day care centers and later development of asthma,
allergic rhinitis, and atopic dermatitis: prospective follow-up
Bremner SA, Carey IM, DeWilde S, Richards N, Maier WC,
survey 12 years after controlled randomized hygiene
Hilton SR, Strachan DP, Cook DG. 2008. Infections presenting
intervention. Arch Pediatr Adolesc Med. 161(10): 972–977.
for clinical care in early life and later risk of hay fever in two
UK birth cohorts. Allergy. 63(3): 274–283. Dunn RR, Fierer N, Henley JB, Leff JW, Menninger HL. 2013.
Home life: factors structuring the bacterial diversity found
Cammarota G, Ianiro G, Gasbarrini A. 2014. Fecal Microbiota
within and between homes. PLoS One. 8(5): e64133.
Transplantation for the Treatment of Clostridium difficile
Infection: A Systematic Review. J Clin Gastroenterol. 48(8):
693–702.

314 Connecting Global Priorities: Biodiversity and Human Health

Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa
Braun-Fahrlander C, Heederik D, Piarroux R, von Mutius K, Laatikainen T, Karisola P, Auvinen P, Paulin L, Makela MJ,
E. 2011. Exposure to environmental microorganisms and et al. 2012. Environmental biodiversity, human microbiota,
childhood asthma. N Engl J Med. 364(8): 701–709. and allergy are interrelated. Proc Natl Acad Sci U S A. 109(21):
8334–8339.
Erdman SE, Rao VP, Olipitz W, Taylor CL, Jackson EA,
Levkovich T, Lee CW, Horwitz BH, Fox JG, Ge Z, et al. 2010. Harnett MM, Melendez AJ, Harnett W. 2010. The therapeutic
Unifying roles for regulatory T cells and inflammation in potential of the filarial nematode-derived immunodulator,
cancer. Int J Cancer. 126(7): 1651–1665. ES-62 in inflammatory disease. Clin Exp Immunol. 159(3):
256–267.
Fahlen A, Engstrand L, Baker BS, Powles A, Fry L. 2012.
Comparison of bacterial microbiota in skin biopsies from Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Boraston
normal and psoriatic skin. Arch Dermatol Res. 304(1): 15–22. AB. 2012. Bacteria of the human gut microbiome catabolize
red seaweed glycans with carbohydrate-active enzyme
Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer
updates from extrinsic microbes. Proc Natl Acad Sci U S A.
A, Lee J, Goldfine AB, Benoist C, Shoelson S, et al. 2009.
109(48): 19786–19791.
Lean, but not obese, fat is enriched for a unique population
of regulatory T cells that affect metabolic parameters. Nat Heijtz RD, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson
Med. 15(8): 930–939. A, Hibberd ML, Forssberg H, Pettersson S. 2011. Normal gut
microbiota modulates brain development and behavior. Proc
Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO,
Natl Acad Sci U S A. 108(7): 3047–3052.
Dantas G. 2012. The shared antibiotic resistome of soil
bacteria and human pathogens. Science. 337(6098): Hesselmar B, Sjoberg F, Saalman R, Aberg N, Adlerberth I,
1107–1111. Wold AE. 2013. Pacifier Cleaning Practices and Risk of Allergy
Development. Pediatrics. 131(6): e1829-e1837.
Frei R, Akdis M, O’Mahony L. 2015. Prebiotics, probiotics,
synbiotics, and the immune system: experimental data and Hildebrand F, Nguyen TL, Brinkman B, Yunta RG, Cauwe
clinical evidence. Curr Opin Gastroenterol. B, Vandenabeele P, Liston A, Raes J. 2013. Inflammation-
associated enterotypes, host genotype, cage and
Fujimura KE, Johnson CC, Ownby DR, Cox MJ, Brodie
inter-individual effects drive gut microbiota variation in
EL, Havstad SL, Zoratti EM, Woodcroft KJ, Bobbitt KR,
common laboratory mice. Genome Biol. 14(1): R4.
Wegienka G, et al. 2010. Man’s best friend? The effect of pet
ownership on house dust microbial communities. J Allergy Hong HA, Khaneja R, Tam NM, Cazzato A, Tan S, Urdaci M,
Clin Immunol. 126(2): 410–412, 412 e411–413. Brisson A, Gasbarrini A, Barnes I, Cutting SM. 2009. Bacillus
subtilis isolated from the human gastrointestinal tract. Res
Gilbert SF, Sapp J, Tauber AI. 2012. A symbiotic view of life:
Microbiol. 160(2): 134–143.
we have never been individuals. Q Rev Biol. 87(4): 325–341.
Howren MB, Lamkin DM, Suls J. 2009. Associations of
Gilham C, Peto J, Simpson J, Roman E, Eden TO, Greaves
depression with C-reactive protein, IL-1, and IL-6: a meta-
MF, Alexander FE. 2005. Day care in infancy and risk of
analysis. Psychosom Med. 71(2): 171–186.
childhood acute lymphoblastic leukaemia: findings from UK
case-control study. BMJ. 330(7503): 1294. Karlsson F, Tremaroli V, Nielsen J, Backhed F. 2013. Assessing
the human gut microbiota in metabolic diseases. Diabetes.
Gimeno D, Kivimaki M, Brunner EJ, Elovainio M, De Vogli R,
62(10): 3341–3349.
Steptoe A, Kumari M, Lowe GD, Rumley A, Marmot MG, et
al. 2009. Associations of C-reactive protein and interleukin-6 Karvonen AM, Hyvarinen A, Rintala H, Korppi M, Taubel
with cognitive symptoms of depression: 12-year follow-up of M, Doekes G, Gehring U, Renz H, Pfefferle PI, Genuneit J, et
the Whitehall II study. Psychol Med. 39(3): 413–423. al. 2014. Quantity and diversity of environmental microbial
exposure and development of asthma: a birth cohort study.
Goldberg RB. 2009. Cytokine and cytokine-like inflammation
Allergy. 69(8): 1092–1101.
markers, endothelial dysfunction, and imbalanced coagulation
in development of diabetes and its complications. J Clin Kembel SW, Jones E, Kline J, Northcutt D, Stenson J, Womack
Endocrinol Metab. 94(9): 3171–3182. AM, Bohannan BJ, Brown GZ, Green JL. 2012. Architectural
design influences the diversity and structure of the built
Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus
environment microbiome. ISME J. 6(8): 1469–1479.
Y, Filbey KJ, Finney CAM, Greenwood EJD, Knox DP, Wilson
MS, et al. 2010. Helminth secretions induce de novo T cell Khoury CK, Bjorkman AD, Dempewolf H, Ramirez-Villegas J,
Foxp3 expression and regulatory function through the TGF- Guarino L, Jarvis A, Rieseberg LH, Struik PC. 2014. Increasing
beta pathway. J Exp Med. 207(11): 2331–2341. homogeneity in global food supplies and the implications for
food security. Proc Natl Acad Sci U S A. 111(11): 4001–4006.
Greaves M. 2006. Infection, immune responses and the
aetiology of childhood leukaemia. Nat Rev Cancer. 6(3): Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson
193–203. MA, Nomicos E, Polley EC, Komarow HD, Murray PR, et
al. 2012. Temporal shifts in the skin microbiome associated
Hang L, Setiawan T, Blum AM, Urban J, Stoyanoff K, Arihiro
with disease flares and treatment in children with atopic
S, Reinecker HC, Weinstock JV. 2010. Heligmosomoides
dermatitis. Genome Res. 22(5): 850–859.
polygyrus infection can inhibit colitis through direct
interaction with innate immunity. J Immunol. 185(6):
3184–3189.

Connecting Global Priorities: Biodiversity and Human Health 315

 Kron MA, Metwali A, Vodanovic-Jankovic S, Elliott D. 2012. McDade TW, Tallman PS, Madimenos FC, Liebert MA, Cepon
Nematode AsnRS resolves intestinal inflammation in murine TJ, Sugiyama LS, Snodgrass JJ. 2012b. Analysis of variability
T-cell transfer colitis. Clin Vaccine Immunol. 20(2): 276–281. of high sensitivity C-reactive protein in lowland ecuador
reveals no evidence of chronic low-grade inflammation. Am
Lachowycz K, Jones AP. 2014. Does walking explain
J Hum Biol. 24(5): 675–681.
associations between access to greenspace and lower
mortality? Soc Sci Med. 107: 9–17. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-
Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF,
Lakritz JR, Poutahidis T, Levkovich T, Varian BJ, Ibrahim
et al. 2013. Animals in a bacterial world, a new imperative for
YM, Chatzigiagkos A, Mirabal S, Alm EJ, Erdman SE. 2014.
the life sciences. Proc Natl Acad Sci U S A. 110(9): 3229–3236.
Beneficial bacteria stimulate host immune cells to counteract
dietary and genetic predisposition to mammary cancer in McGovern PE. 2009. Uncorking the past: the quest for wine,
mice. Int J Cancer. 135(3): 529–540. beer, and other alcoholic beverages. Berkeley and Los Angeles:
University of California Press.
Leroy F, Geyzen A, Janssens M, De Vuyst L, Scholliers P.
2013. Meat fermentation at the crossroads of innovation McGovern PE, Zhang J, Tang J, Zhang Z, Hall GR, Moreau
and tradition: A historical outlook. Trends in Food Science RA, Nunez A, Butrym ED, Richards MP, Wang CS, et al. 2004.
& Technology. 31: 130–137. Fermented beverages of pre- and proto-historic China. Proc
Natl Acad Sci U S A. 101(51): 17593–17598.
Lewis MC, Inman CF, Patel D, Schmidt B, Mulder I, Miller
B, Gill BP, Pluske J, Kelly D, Stokes CR, et al. 2012. Direct Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D,
experimental evidence that early-life farm environment Nejdi A, Bisson JF, Rougeot C, Pichelin M, Cazaubiel M,
influences regulation of immune responses. Pediatr Allergy et al. 2011. Assessment of psychotropic-like properties of
Immunol. 23(3): 265–269. a probiotic formulation (Lactobacillus helveticus R0052 and
Bifidobacterium longum R0175) in rats and human subjects.
Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac
Br J Nutr. 105(5): 755–764.
P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, et
al. 2007. An African origin for the intimate association Miller AH, Haroon E, Raison CL, Felger JC. 2013. Cytokine
between humans and Helicobacter pylori. Nature. 445(7130): targets in the brain: impact on neurotransmitters and
915–918. neurocircuits. Depress Anxiety. 30(4): 297–306.
Lu MF, Xiao ZT, Zhang HY. 2013. Where do health benefits Mitchell R, Popham F. 2008. Effect of exposure to natural
of flavonoids come from? Insights from flavonoid targets and environment on health inequalities: an observational
their evolutionary history. Biochem Biophys Res Commun. population study. Lancet. 372(9650): 1655–1660.
434(4): 701–704.
Mozaffarian D, Hao T, Rimm EB, Willett WC, Hu FB. 2011.
Lynch SV, Wood RA, Boushey H, Bacharier LB, Bloomberg Changes in diet and lifestyle and long-term weight gain in
GR, Kattan M, O’Connor GT, Sandel MT, Calatroni A, Matsui women and men. N Engl J Med. 364(25): 2392–2404.
E, et al. 2014. Effects of early-life exposure to allergens and
Mulder IE, Schmidt B, Lewis M, Delday M, Stokes CR,
bacteria on recurrent wheeze and atopy in urban children. J
Bailey M, Aminov RI, Gill BP, Pluske JR, Mayer CD, et al.
Allergy Clin Immunol. 134(3): 593–601.
2011. Restricting microbial exposure in early life negates
Ma X, Buffler PA, Selvin S, Matthay KK, Wiencke JK, the immune benefits associated with gut colonization in
Wiemels JL, Reynolds P. 2002. Daycare attendance and risk environments of high microbial diversity. PLoS One. 6(12):
of childhood acute lymphoblastic leukaemia. Br J Cancer. e28279.
86(9): 1419–1424.
Mulder IE, Schmidt B, Stokes CR, Lewis M, Bailey M,
Maas J, Verheij RA, Groenewegen PP, de Vries S, Aminov RI, Prosser JI, Gill BP, Pluske JR, Mayer CD, et al.
Spreeuwenberg P. 2006. Green space, urbanity, and health: 2009. Environmentally-acquired bacteria influence microbial
how strong is the relation? J Epidemiol Community Health. diversity and natural innate immune responses at gut
60(7): 587–592. surfaces. BMC Biol. 7: 79.
Maas J, Verheij RA, Spreeuwenberg P, Groenewegen PP. Ngure FM, Humphrey JH, Mbuya MN, Majo F, Mutasa K,
2008. Physical activity as a possible mechanism behind the Govha M, Mazarura E, Chasekwa B, Prendergast AJ, Curtis
relationship between green space and health: a multilevel V, et al. 2013. Formative research on hygiene behaviors and
analysis. BMC Public Health. 8: 206. geophagy among infants and young children and implications
of exposure to fecal bacteria. Am J Trop Med Hyg. 89(4):
Mathers CD, Loncar D. 2006. Projections of global mortality
709–716.
and burden of disease from 2002 to 2030. PLoS Med. 3(11):
e442. Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J,
Sunagawa S, Plichta DR, Gautier L, Pedersen AG, Le Chatelier
McDade TW. 2012. Early environments and the ecology
E, et al. 2014. Identification and assembly of genomes and
of inflammation. Proc Natl Acad Sci U S A. 109 Suppl 2:
genetic elements in complex metagenomic samples without
17281–17288.
using reference genomes. Nat Biotechnol. (online 6 July
McDade TW, Borja JB, Adair L, Kuzawa CW. 2012a. 2014; DOI: 10.1038/nbt.2939).
Depressive symptoms are not associated with inflammation
in younger and older adults in the Philippines. Evolution,
Medicine and Public Health. 2013(1): 18–23.

316 Connecting Global Priorities: Biodiversity and Human Health

O’Byrne KJ, Dalgleish AG, Browning MJ, Steward WP, Harris Riedler J, Braun-Fahrlander C, Eder W, Schreuer M, Waser M,
AL. 2000. The relationship between angiogenesis and the Maisch S, Carr D, Schierl R, Nowak D, von Mutius E. 2001.
immune response in carcinogenesis and the progression of Exposure to farming in early life and development of asthma
malignant disease. Eur J Cancer. 36(2): 151–169. and allergy: a cross-sectional survey. Lancet. 358(9288):
1129–1133.
Osada Y, Kanazawa T. 2010. Parasitic helminths: new weapons
against immunological disorders. J Biomed Biotechnol. 2010: Rook GAW. 2013. Regulation of the immune system by
743–758. biodiversity from the natural environment: An ecosystem
service essential to health. Proc Natl Acad Sci USA. 110(46):
Ownby DR, Johnson CC, Peterson EL. 2002. Exposure
18360–18367.
to dogs and cats in the first year of life and risk of allergic
sensitization at 6 to 7 years of age. JAMA. 288(8): 963–972. Rook GAW, Dalgleish A. 2011. Infection, immunoregulation
and cancer. Immunological Reviews. 240: 141–159.
Pakarinen J, Hyvarinen A, Salkinoja-Salonen M, Laitinen S,
Nevalainen A, Makela MJ, Haahtela T, von Hertzen L. 2008. Rook GAW, Lowry CA, Raison CL. 2013. Microbial Old
Predominance of Gram-positive bacteria in house dust in the Friends, immunoregulation and stress resilience. Evolution,
low-allergy risk Russian Karelia. Environ Microbiol. 10(12): Medicine and Public Health. EMPH (2013)(1): 46–64
3317–3325. doi:10.1093/emph/eot1004.
Parker W, Ollerton J. 2013. Evolutionary biology and Rook GAW, Lowry CA, Raison CL. 2014a. Hygiene and other
anthropology suggest biome reconstitution as a necessary early childhood influences on the subsequent function of the
approach toward dealing with immune disorders. Evol Med immune system. Brain Research. http://dx.doi.org/10.1016/j.
Public Health. 2013(1): 89–103. brainres.2014.04.004.
Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann Rook GAW, Raison CL, Lowry CA. 2014b. Microbial “Old
K, Lau S, Hamelmann E. 2013. Establishment of the Friends”, immunoregulation and socio-economic status.
intestinal microbiota and its role for atopic dermatitis in Clinical and Experimental Immunology. 177(1): 1–12.
early childhood. J Allergy Clin Immunol. 132(3): 601–607.
Rothman SW. 1981. Presence of Clostridium difficile toxin in
Porta C, Larghi P, Rimoldi M, Totaro MG, Allavena P, guinea pigs with penicillin-associated colitis. Med Microbiol
Mantovani A, Sica A. 2009. Cellular and molecular pathways Immunol. 169(3): 187–196.
linking inflammation and cancer. Immunobiology. 214(9–
Round JL, Mazmanian SK. 2010. Inducible Foxp3+
10): 761–777.
regulatory T-cell development by a commensal bacterium of
Poutahidis T, Kleinewietfeld M, Smillie C, Levkovich T, the intestinal microbiota. Proc Natl Acad Sci U S A. 107(27):
Perrotta A, Bhela S, Varian BJ, Ibrahim YM, Lakritz JR, 12204–12209.
Kearney SM, et al. 2013. Microbial reprogramming inhibits
Sahlberg B, Wieslander G, Norback D. 2010. Sick building
Western diet-associated obesity. PLoS One. 8(7): e68596.
syndrome in relation to domestic exposure in Sweden--a
Price KC, Hyde JS, Coe CL. 1999. Matrilineal transmission of cohort study from 1991 to 2001. Scand J Public Health.
birth weight in the rhesus monkey (Macaca mulatta) across 38(3): 232–238.
several generations. Obstet Gynecol. 94(1): 128–134.
Schele E, Benrick A, Grahnemo L, Egecioglu E, Anesten F,
Radon K, Windstetter D, Poluda AL, Mueller B, von Mutius E, Palsdottir V, Jansson JO. 2013a. Inter-relation between
Koletzko S. 2007. Contact with farm animals in early life and interleukin (IL)-1, IL-6 and body fat regulating circuits of
juvenile inflammatory bowel disease: a case-control study. the hypothalamic arcuate nucleus. J Neuroendocrinol. 25(6):
Pediatrics. 120(2): 354–361. 580–589.
Raison CL, Borisov AS, Majer M, Drake DF, Pagnoni G, Schele E, Grahnemo L, Anesten F, Hallen A, Backhed F,
Woolwine BJ, Vogt GJ, Massung B, Miller AH. 2009. Jansson JO. 2013b. The gut microbiota reduces leptin
Activation of central nervous system inflammatory pathways sensitivity and the expression of the obesity-suppressing
by interferon-alpha: relationship to monoamines and neuropeptides proglucagon (Gcg) and brain-derived
depression. Biol Psychiatry. 65(4): 296–303. neurotrophic factor (Bdnf) in the central nervous system.
Endocrinology. 154(10): 3643–3651.
Ramirez-Puebla ST, Servin-Garciduenas LE, Jimenez-Marin B,
Bolanos LM, Rosenblueth M, Martinez J, Rogel MA, Ormeno- Schneider MK, Luscher G, Jeanneret P, Arndorfer M, Ammari
Orrillo E, Martinez-Romero E. 2013. Gut and root microbiota Y, Bailey D, Balazs K, Baldi A, Choisis JP, Dennis P, et al. 2014.
commonalities. Appl Environ Microbiol. 79(1): 2–9. Gains to species diversity in organically farmed fields are not
propagated at the farm level. Nat Commun. 5: 4151.
Rastogi T, Devesa S, Mangtani P, Mathew A, Cooper N, Kao
R, Sinha R. 2008. Cancer incidence rates among South Asians Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, Rey
in four geographic regions: India, Singapore, UK and US. Int FE, Smith MI, Simon GM, Scheffrahn RH, Woebken D, et al.
J Epidemiol. 37(1): 147–160. 2014. Bacteria from diverse habitats colonize and compete
in the mouse gut. Cell. 159(2): 253–266.
Rehman A, Lepage P, Nolte A, Hellmig S, Schreiber S, Ott SJ.
2010. Transcriptional activity of the dominant gut mucosal Selhub EM, Logan AC, Bested AC. 2014. Fermented foods,
microbiota in chronic inflammatory bowel disease patients. microbiota, and mental health: ancient practice meets
J Med Microbiol. 59(Pt 9): 1114–1122. nutritional psychiatry. J Physiol Anthropol. 33: 2.

Connecting Global Priorities: Biodiversity and Human Health 317

 Shoelson SE, Herrero L, Naaz A. 2007. Obesity, inflammation, Tremaroli V, Backhed F. 2012. Functional interactions
and insulin resistance. Gastroenterology. 132(6): 2169–2180. between the gut microbiota and host metabolism. Nature.
489(7415): 242–249.
Smillie CS, Smith MB, Friedman J, Cordero OX, David LA,
Alm EJ. 2011. Ecology drives a global network of gene Troyer K. 1984. Behavioral acquisition of the hindgut
exchange connecting the human microbiome. Nature. fermentation system by hatchling Iguana iguana. Behavioral
480(7376): 241–244. Ecology and Sociobiology. 14(3): 189–193.
Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL,
K, van Capel TM, Zaat BA, Yazdanbakhsh M, Wierenga EA, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit
van Kooyk Y, et al. 2005. Selective probiotic bacteria induce JP, et al. 2009. A core gut microbiome in obese and lean twins.
IL-10-producing regulatory T cells in vitro by modulating Nature. 457(7228): 480–484.
dendritic cell function through dendritic cell-specific
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER,
intercellular adhesion molecule 3-grabbing nonintegrin. J
Gordon JI. 2006. An obesity-associated gut microbiome with
Allergy Clin Immunol. 115(6): 1260–1267.
increased capacity for energy harvest. Nature. 444(7122):
Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey 1027–1031.
G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC,
Valkanova V, Ebmeier KP, Allan CL. 2013. CRP, IL-6 and
Nakielny S, et al. 2013. Cohabiting family members share
depression: a systematic review and meta-analysis of
microbiota with one another and with their dogs. Elife. 2:
longitudinal studies. J Affect Disord. 150(3): 736–744.
e00458.
von Hertzen L, Hanski I, Haahtela T. 2011a. Natural
Sozanska B, Blaszczyk M, Pearce N, Cullinan P. 2013. Atopy
immunity. Biodiversity loss and inflammatory diseases are
and allergic respiratory disease in rural Poland before
two global megatrends that might be related. EMBO Rep.
and after accession to the European Union. J Allergy Clin
12(11): 1089–1093.
Immunol. 133(5): 1347–1353.
von Hertzen LC, Joensuu H, Haahtela T. 2011b. Microbial
Strachan DP. 1989. Hay fever, hygiene, and household size.
deprivation, inflammation and cancer. Cancer Metastasis Rev.
Brit Med J. 299(6710): 1259–1260.
30(2): 211–223.
Su MS, Oh PL, Walter J, Ganzle MG. 2012. Intestinal origin
Wang FH, Qiao M, Su JQ, Chen Z, Zhou X, Zhu YG. 2014.
of sourdough Lactobacillus reuteri isolates as revealed by
High throughput profiling of antibiotic resistance genes in
phylogenetic, genetic, and physiological analysis. Appl
urban park soils with reclaimed water irrigation. Environ Sci
Environ Microbiol. 78(18): 6777–6780.
Technol. 48(16): 9079–9085.
Sugiyama A, Vivanco JM, Jayanty SS, Manter DK. 2010.
Wells JC, Stock JT. 2011. Re-examining heritability: genetics,
Pyrosequencing assess- ment of soil microbial communities
life history and plasticity. Trends Endocrinol Metab. 22(10):
in organic and conventional potato farms. Plant Dis. 94:
421–428.
1329–1335.
West CE, Renz H, Jenmalm MC, Kozyrskyj AL, Allen KJ,
Swain MR, Anandharaj M, Ray RC, Parveen Rani R. 2014.
Vuillermin P, Prescott SL, in FMIG, in FMIG. 2015. The gut
Fermented fruits and vegetables of Asia: a potential source
microbiota and inflammatory noncommunicable diseases:
of probiotics. Biotechnol Res Int. 2014: 250424.
Associations and potentials for gut microbiota therapies. J
Thalmann O, Shapiro B, Cui P, Schuenemann VJ, Sawyer SK, Allergy Clin Immunol. 135(1): 3–13.
Greenfield DL, Germonpre MB, Sablin MV, Lopez-Giraldez
Whitlock DR, Feelisch M. 2009. Soil bacteria, nitrite, and the
F, Domingo-Roura X, et al. 2013. Complete mitochondrial
skin. In: Rook GAW editors. The Hygiene Hypothesis and
genomes of ancient canids suggest a European origin of
Darwinian Medicine. Basel: Birkhäuser. p. 103–116.
domestic dogs. Science. 342(6160): 871–874.
Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters
Thorburn AN, Macia L, Mackay CR. 2014. Diet, Metabolites,
EC, Siuzdak G. 2009. Metabolomics analysis reveals large
and “Western-Lifestyle” Inflammatory Diseases. Immunity.
effects of gut microflora on mammalian blood metabolites.
40(6): 833–842.
Proc Natl Acad Sci U S A. 106(10): 3698–3703.
Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B,
Wolfe ND, Dunavan CP, Diamond J. 2007. Origins of major
Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, et al.
human infectious diseases. Nature. 447(7142): 279–283.
2013. Consumption of fermented milk product with probiotic
modulates brain activity. Gastroenterology. 144(7): 1394– Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-
1401, 1401 e1391–1394. Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano
RN, Anokhin AP, et al. 2012. Human gut microbiome viewed
Timm S, Svanes C, Janson C, Sigsgaard T, Johannessen A,
across age and geography. Nature. 486(7402): 222–227.
Gislason T, Jogi R, Omenaas E, Forsberg B, Toren K, et al.
2014. Place of upbringing in early childhood as related to Yoo J, Tcheurekdjian H, Lynch SV, Cabana M, Boushey HA.
inflammatory bowel diseases in adulthood: a population- 2007. Microbial manipulation of immune function for
based cohort study in Northern Europe. Eur J Epidemiol. asthma prevention: inferences from clinical trials. Proc Am
29(6): 429–437. Thorac Soc. 4(3): 277–282.

318 Connecting Global Priorities: Biodiversity and Human Health

Zeeuwen PL, Kleerebezem M, Timmerman HM, Schalkwijk J. Hunt, B. and Vincent, A.C.J. (2006). Scale and sustainability
2013. Microbiome and skin diseases. Curr Opin Allergy Clin of marine bioprospecting for pharmaceuticals. Ambio, 35 (2),
Immunol. 13(5): 514–520. 57–64.
Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld Krishnakumar, J., Fox, J., & Anitha, V. (2012). Non-timber
RD, Hashsham SA, Tiedje JM. 2013. Diverse and abundant forest products. Economic & Political Weekly, 47(52), 133
antibiotic resistance genes in Chinese swine farms. Proc Natl
Levy, S. B., & Marshall, B. (2004). Antibacterial resistance
Acad Sci U S A. 110(9): 3435–3440.
worldwide: causes, challenges and responses. Nature medicine,
10, S122-S129.
Chapter 9 May, R. M. (1988). How many species are there on earth?.
Barry, J. M. (2005). The great influenza: The story of the Science (Washington), 241(4872), 1441–1449.
deadliest pandemic in history. Penguin.
McNeely, J. A. (2006). Risks to people of losing medicinal
Beutler, J. A., Cragg, G. M., & Newman, D. J. (2012). The species. Conserving medicinal species: securing a healthy
National Cancer Institute and Natural Product-Based Drug future. IUCN: Ecosystems and Livelihoods Group, Asia,
Discovery in Africa. In Drug Discovery in Africa (pp. 29–52). 17–31.
Springer Berlin Heidelberg.
Meijaard, E., Sheil, D., Guariguata, M. R., Nasi, R., Sunderland,
Biodiversity Indicators Partnership (BIP). 2010. Biodiversity T. C. H., & Putzel, L. (2011). Ecosystem services certification:
indicators and the 2010 Target: Experiences and lessons learnt Opportunities and constraints. CIFOR.
from the 2010 Biodiversity Indicators Partnership. Secretariat
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G., & Worm,
of the Convention on Biological Diversity, Montréal, Canada.
B. (2011). How many species are there on Earth and in the
Technical Series No. 53, 196 pages. Retrieved from: http://
ocean?. PLoS biology, 9(8), e1001127.
www.bipindicators.net/foodandmedicine
Newman, D.J. and Cragg, G.M. (2007). Natural products as
Brock, T. D., & Freeze, H. (1969). Thermus aquaticus gen. n.
sources of new drugs over the last 25 years. Journal of Natural
and sp. n., a nonsporulating extreme thermophile. Journal
Products, 70, 461–477.
of Bacteriology, 98(1), 289–97.
Newman, D. J., & Cragg, G. M. (2012). Natural products as
Bortenschlager, S., & Oeggl, K. (Eds.). (2000). The iceman
sources of new drugs over the 30 years from 1981 to 2010.
and his natural environment: Palaeobotanical results. Springer
Journal of natural products, 75(3), 311–335.
Vienna.
Petersen, C., & Round, J. L. (2014). Defining dysbiosis
Chivian, E. and Bernstein, A. (2008). Sustaining life: How
and its influence on host immunity and disease. Cellular
human health depends on biodiversity. New York: Oxford
microbiology, 16(7), 1024–1033.
University Press.
Pew Health Initiatives. Tracking the Pipeline of Antibiotics
Cho, I., & Blaser, M. J. (2012). The human microbiome: at
in Development. (2014). Available at http://www. health.
the interface of health and disease. Nature Reviews Genetics,
org/other-resource/tracking-the-pipeline-of-antibiotics-in-
13(4), 260–270.
development-85899541556. Accessed 29 April 2014.
Costello, M. J., May, R. M., & Stork, N. E. (2013). Can
Phelps, J., Carrasco, L. R., & Webb, E. L. (2014). A Framework
we name Earth’s species before they go extinct? Science,
for Assessing Supply-Side Wildlife Conservation. Conservation
339(6118), 413–416.
biology, 28(1), 244–257.
Davies, J., & Davies, D. (2010). Origins and evolution of
Pimentel, D., Wilson, C., McCullum, C., Huang, R., Dwen, P.,
antibiotic resistance. Microbiology and Molecular Biology
Flack, J., Tran, Q., Saltman, T. & Cliff, B. (1997). Economic and
Reviews, 74(3), 417–433.
environmental benefits of biodiversity. BioScience, 747–757.
Franco, A., Hill, J. K., Kitschke, C., Collingham, Y. C., Roy, D.
Podolsky, S. H. (2006). Pneumonia before antibiotics: therapeutic
B., Fox, R. I. C. H. A. R. D., et al. (2006). Impacts of climate
evolution and evaluation in twentieth-century America. JHU
warming and habitat loss on extinctions at species’ low-
Press.
latitude range boundaries. Global Change Biology, 12(8),
1545–1553. Pounds, J. A., Bustamante, M. R., Coloma, L. A., Consuegra,
J. A., Fogden, M. P., Foster, P. N., et al. (2006). Widespread
Kandel, E. R. (2007). In search of memory: The emergence of a
amphibian extinctions from epidemic disease driven by global
new science of mind. WW Norton & Company.
warming. Nature, 439(7073), 161–167.
Hamilton, A. (2003). Medicinal plants and conservation:
Convention on Biological Diversity, Secretariat (2010) Global
issues and approaches. International Plants Conservation
Biodiversity Outlook 3. Montréal,94 p. Available at http://
Unit, WWF-UK, 51.
www.cdb.int/gbo3/
Hostettmann, K., Potterat, O., & Wolfender, J. L. (1998). The
Convention on Biological Diversity, Secretariat (2014) Global
potential of higher plants as a source of new drugs. Chimia
Biodiversity Outlook 4. Montréal, 94 p. Available at http://
International Journal for Chemistry, 52(1–2), 10–17.
www.cdb.int/gbo3/

Connecting Global Priorities: Biodiversity and Human Health 319

 Spellberg, B., Guidos, R., Gilbert, D., Bradley, J., Boucher, H. Brodin, T., Piovano, S., Fick, J., Klaminder, J., Heynen, M., &
W., Scheld, W. M., Bartlett, J.G. & Edwards, J. (2008). The Jonsson, M. (2014). Ecological effects of pharmaceuticals in
epidemic of antibiotic-resistant infections: a call to action for aquatic systems – impacts through behavioural alterations.
the medical community from the Infectious Diseases Society Philosophical Transactions of the Royal Society of London B:
of America. Clinical Infectious Diseases, 46(2), 155–164. Biological Sciences, 369(1656), 20130580.
Sukhdev, P., Wittmer, H., & Miller, D. (2014). The economics Bruce, G. M., Pleus, R. C., & Snyder, S. A. (2010). Toxicological
of ecosystems and biodiversity (TEEB): challenges and relevance of pharmaceuticals in drinking water. Environmental
responses. Nature in the Balance: The Economics of Science & Technology, 44(14), 5619–5626.
Biodiversity (Helm D, Hepburn C, eds). Oxford, UK: Oxford
Campbell TA, Lapidge SJ, Long DB, (2006). Using Baits to
University Press, 135–152.
Deliver Pharmaceuticals to Feral Swine in Southern Texas.
Urban, M. C. (2015). Accelerating extinction risk from climate Wildlife Society Bulletin 34(4):1184–1189.
change. Science, 348(6234), 571–573.
Cardoso O, Porcher JM, Sanchez W, (2014). Factory-
Wilson, E. O. (2003). The encyclopedia of life. Trends in discharged pharmaceuticals could be a relevant source of
Ecology & Evolution, 18(2), 77–80. aquatic environment contamination: Review of evidence and
need for knowledge. Chemosphere 115; 20–30
Chapter 10 Carroll, D., Wang, J., Fanning, S., & McMahon, B. J. (2015).
Antimicrobial Resistance in Wildlife: Implications for Public
Backhaus, T. (2014). Medicines, shaken and stirred: a critical Health. Zoonoses and Public Health. (online ahead of print; doi:
review on the ecotoxicology of pharmaceutical mixtures. 10.1111/zph.12182)
Philosophical Transactions of the Royal Society B: Biological
Sciences, 369(1656), 20130585. COHAB Initiative Secretariat, (2014). Ecosystem Approaches
to Health 2: The impacts of health care systems on biodiversity.
Baker-Austin, C., Wright, M. S., Stepanauskas, R., & Policy Brief for CBD COP 12, Pyeongchang, Republic of Korea,
McArthur, J. V. (2006). Co-selection of antibiotic and metal October 2014
resistance. Trends in Microbiology, 14(4), 176–182.
Cortez, F.S., Pereira, C.D.S., Santos, A.R., Cesar, A., Choueri,
Bean, T. G., Boxall, A. B., Lane, J., Herborn, K. A., Pietravalle, R.B., Martini, G.d.A. and Bohrer-Morel, M.B. (2012).
S., & Arnold, K. E. (2014). Behavioural and physiological Biological effects of environmentally relevant concentrations
responses of birds to environmentally relevant concentrations of the pharmaceutical Triclosan in the marine mussel Perna
of an antidepressant. Philosophical Transactions of the Royal perna. Environmental Pollution, 168, 145–150.
Society B: Biological Sciences, 369(1656), 20130575.
Coyne R, Hiney M, O’Conner B, Cazabon D, Smith P, (1994).
Bound JP, Voulvoulis N, 2005. Household Disposal of Concentration and persistence of oxytetracycline in sediments
Pharmaceuticals as a Pathway for Aquatic Contamination under a marine salmon farm. Aquaculture 123;31–42.
in the United Kingdom. Environmental Health Perspectives
113(12); 1705–1711. Cuthbert RJ, Dave R, Sunder Chakraborty S, Kumar S, Prakash
S, Ranade SP, Prakash V, (2011). Assessing the ongoing threat
Boxall ABA, 2004. The environmental side effects of from veterinary non-steroidal anti-inflammatory drugs to
medication. EMBO Reports 5:1110–1116. Critically Endangered Gyps vultures in India. Oryx 45;
Boxall ABA, Fogg LA, Blackwell PA, Kay P, Pemberton EJ, 420–426.
Croxford A (2004) Veterinary medicines in the environment. Daughton CG. (2003b). Cradle-to-cradle stewardship of
Reviews of Environmental Contamination and Toxicology 180: drugs for minimizing their environmental disposition while
1–91. promoting human health. II. Drug disposal, waste reduction,
Boxall, A. B., Sherratt, T. N., Pudner, V., & Pope, L. J. (2007). and future directions. Environmental Health Perspectives
A screening level index for assessing the impacts of veterinary 111:775–785.
medicines on dung flies. Environmental Science & Technology, Daughton, C. G. (2014). Eco-directed sustainable prescribing:
41(7), 2630–2635. feasibility for reducing water contamination by drugs. The
Boxall, A., Hardy, A., Beulke, S., Boucard, T., Burgin, L., Science of the Total Environment, 493, 392–404.
Falloon, P. D., ... & Williams, R. J. (2008). Impacts of climate Daughton CG, Ternes TA., (1999). Pharmaceuticals and
change on indirect human exposure to pathogens and personal care products in the environment: agents of subtle
chemicals from agriculture. Environmental Health Perspectives, change? Environmental Health Perspectives 107(Suppl 6):
117(4), 508–514. 907–937.
Boxall ABA, Rudd MA, Brooks BW, Caldwell DJ, Choi K, Fick J., Söderström H., Lindberg RH., Phan C., Tysklind M.
Hickmann S et al, (2012). Pharmaceuticals and Personal Care and Larsson, D. G. J., (2009). Contamination of surface,
Products in the Environment: What are the big questions? ground, and drinking water from pharmaceutical production.
Environmental Health Perspectives 120(9);1221–1229. Environmental Toxicology and Chemistry, 28: 2522–2527.
Breton, R. and Boxall, A. (2003), Pharmaceuticals and Finley, R. L., Collignon, P., Larsson, D. J., McEwen, S. A., Li, X.
Personal Care Products in the Environment: Regulatory Z., Gaze, W. H., ... & Topp, E. (2013). The scourge of antibiotic
Drivers and Research Needs. QSAR & Combinatorial Science, resistance: the important role of the environment. Clinical
22: 399–409. Infectious Diseases, 57; 704–710.

320 Connecting Global Priorities: Biodiversity and Human Health

Floate KD, Wardhaugh KG, Boxall ABA, Sherratt TN, (2005). Lange R., Hutchinson TH, Croudace CP, Siegmund F,
Faecal residues of veterinary parasiticides: non-target effects Schweinfurth H, Hampe P, Panter GH, Sumpter JP, (2001).
in the pasture environment. Annual Reviews of Entomology Effects of the synthetic oestrogen 17 alpha-ethinylestradiol
50: 153–179. over the life-cycle of the fathead minnow (Pimephales
promelas). Environmental Toxicology and Chemistry. (20/6);
Guler Y, Ford AT, 2010. Aquatic Toxicology. Antidepressants
1216–1227.
make amphipods see the light. Aquatic Toxicology 99(3);
397–404. Larsson DJ, de Pedro C, Paxeus N., (2007). Effluent from
drug manufactures contains extremely high levels of
Halling-Sørensen B., Nielsen SN, Lanzky,PF, Ingerslev, F.,
pharmaceuticals. Journal of Hazardous Materials 148(3):751–5.
Holten Lützhøft HC, Jørgensen SE, 1998. Occurrence, fate
and effects of pharmaceutical substances in the environment- Larsson DJ, (2010). Release of active pharmaceutical
A review. Chemosphere 36(2); 357–393. ingredients from manufacturing sites  – need for new
management strategies. Integrated Environmental Assessment
Hegglin DA, Bontadina F, Gloor S, Romer J, Müller U,
and Management, 6: 184–186.
Breitenmoser U, Deplazes P, 2004. Baiting red foxes in
an urban area: a camera trap study. Journal of Wildlife Lumaret, J. P., Errouissi, F., Floate, K., Römbke, J., &
Management 68(4):1010–1017. Wardhaugh, K. (2012). A review on the toxicity and non-
target effects of macrocyclic lactones in terrestrial and aquatic
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk,
environments. Current pharmaceutical biotechnology, 13(6),
D., Gittleman, J. L., & Daszak, P. (2008). Global trends in
1004.
emerging infectious diseases. Nature, 451(7181), 990–993.
Margalida, A., Bogliani, G., Bowden, C. G. R., Donázar, J. A.,
Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD,
Genero, F., Gilbert, M., ... & Green, R. E. (2014). One Health
Barber LB, et al., 2002. Pharmaceuticals, hormones, and other
approach to use of veterinary pharmaceuticals. Science,
organic wastewater contaminants in U.S. streams, 1999–
346(6215); 1296–1298.
2000: a national reconnaissance. Environmental Science and
Technology 36:1202–1211. Markandya A, Taylor T, Longo A, Murty MN, Murty S,
Dhavala K. (2008). Counting the cost of vulture decline – an
Kampa, E., Dworak, T., Laaser, C., & Vidaurre, R. (2010).
appraisal of the human health and other benefits of vultures
European Regulations. In: Kümmerer and Hempel (eds) Green
in India. Ecological Economics 67:194–204.
and Sustainable Pharmacy (pp. 253–277). Springer Berlin
Heidelberg, 313pp Monteiro SC, Boxall ABA, (2009). Factors affecting the
degradation of pharmaceuticals in agricultural soils.
Kay P, Blackwell PA, Boxall ABA, (2004). Fate of veterinary
Environmental Toxicology and Chemistry 28:2546–2554.
antibiotics in a macroporous tile drained clay soil.
Environmental Toxicology and Chemistry, 23: 1136–1144. Morgon, P. A. (2015) Sustainable Development for the
Healthcare Industry. Springer, Berlin. 154 pp
Kim, J., Park, J., Kim, P. G., Lee, C., Choi, K., & Choi, K. (2010).
Implication of global environmental changes on chemical Musson SE, Townsend TG, (2009). Pharmaceutical compound
toxicity-effect of water temperature, pH, and ultraviolet B content of municipal solid waste. Journal of Hazardous
irradiation on acute toxicity of several pharmaceuticals in Materials 162(2–3); 730–735.
Daphnia magna. Ecotoxicology, 19(4), 662–669.
Naidoo, V., Wolter, K., Cuthbert, R., & Duncan, N. (2009).
Kookana, R. S., Williams, M., Boxall, A. B., Larsson, D. J., Veterinary diclofenac threatens Africa’s endangered vulture
Gaw, S., Choi, K., ... & Carriquiriborde, P. (2014). Potential species. Regulatory toxicology and pharmacology, 53(3),
ecological footprints of active pharmaceutical ingredients: an 205–208.
examination of risk factors in low-, middle-and high-income
Nash JP, Kime DE, van der Ven LTM,, Wester PW, Brion
countries. Philosophical Transactions of the Royal Society B:
F, Maack G, Stahlschmidt-Allner P, Tyler CR, (2004).
Biological Sciences, 369(1656), 20130586.
Environmental concentrations of the pharmaceutical
Kümmerer, K. (2009). The presence of pharmaceuticals in ethinyloestradiol cause reproductive failure in fish.
the environment due to human use–present knowledge and Environmental Health Perspectives, (112); 1725–1733.
future challenges. Journal of Environmental Management,
Oaks JL, Gilbert M, Virani MZ, Watson RT, Meteyer CU,
90(8), 2354–2366.
Rideout BA, et al. (2004). Diclofenac residues as the cause of
Küster, A., & Adler, N. (2014). Pharmaceuticals in the vulture population decline in Pakistan. Nature 427:630–633.
environment: scientific evidence of risks and its regulation.
Orlando, E. F., & Guillette Jr, L. J. (2007). Sexual dimorphic
Philosophical Transactions of the Royal Society B: Biological
responses in wildlife exposed to endocrine disrupting
Sciences, 369(1656), 20130587.
chemicals. Environmental Research, 104(1), 163–173.
Kyselková, M., Kotrbová, L., Bhumibhamon, G., Chroňáková,
Pruden, A., Arabi, M., & Storteboom, H. N. (2012). Correlation
A., Jirout, J., Vrchotová, N., ... & Elhottová, D. (2015).
between upstream human activities and riverine antibiotic
Tetracycline resistance genes persist in soil amended with
resistance genes. Environmental Science & Technology, 46(21),
cattle feces independently from chlortetracycline selection
11541–11549.
pressure. Soil Biology and Biochemistry, 81, 259–265.

Connecting Global Priorities: Biodiversity and Human Health 321

 Pruden, A. (2013). Balancing water sustainability and public Weinberger J, Klaper R, (2014). Environmental concentrations
health goals in the face of growing concerns about antibiotic of the selective serotonin reuptake inhibitor fluoxetine impact
resistance. Environmental Science & Technology, 48(1), 5–14. specific behaviors involved in reproduction, feeding and
predator avoidance in the fish Pimephales promelas (fathead
Radimersky, T., Frolkova, P., Janoszowska, D., Dolejska, M.,
minnow). Aquatic Toxicology 151; 77–83.
Svec, P., Roubalova, E., ... & Literak, I. (2010). Antibiotic
resistance in faecal bacteria (Escherichia coli, Enterococcus Wellington, E. M., Boxall, A. B., Cross, P., Feil, E. J., Gaze,
spp.) in feral pigeons. Journal of Applied Microbiology, 109(5), W. H., Hawkey, P. M., ... & Williams, A. P. (2013). The role
1687–1695. of the natural environment in the emergence of antibiotic
resistance in Gram-negative bacteria. The Lancet Infectious
Redshaw, C. H., Stahl-Timmins, W. M., Fleming, L. E.,
Diseases, 13(2), 155–165.
Davidson, I., & Depledge, M. H. (2013). Potential changes
in disease patterns and pharmaceutical use in response to Wickramsinghe LP, Harris S, Jones G, Vaughan Jennings N,
climate change. Journal of Toxicology and Environmental Health, (2004). Abundance and Species Richness of Nocturnal Insects
Part B, 16(5), 285–320. on Organic and Conventional Farms: Effects of Agricultural
Intensification on Bat Foraging. Conservation Biology, 18:
Rico A, Van den Brink PJ, (2014). Probabilistic risk assessment
1283–1292.
of veterinary medicines applied to four major aquaculture
species produced in Asia. Science of the Total Environment. World Health Organisation (WHO) (2011). Pharmaceuticals
468–469; 630–641. in Drinking Water. WHO, Geneva.
Santos, L. H., Araújo, A. N., Fachini, A., Pena, A., WHO (2012) The Evolving Threat of Antimicrobial Resistance –
Delerue-Matos, C., & Montenegro, M. C. B. S. M. (2010). Options for Action. WHO, Geneva, 120pp
Ecotoxicological aspects related to the presence of
WHO (2014). Antimicrobial Resistance: Global Report on
pharmaceuticals in the aquatic environment. Journal of
Surveillance. WHO, Geneva. 256pp
Hazardous Materials, 175(1–3), 45–95.
Schroeder, K., Thompson, T., Frith, K., & Pencheon, D.
(2013) A Vision for Sustainable Healthcare. (pp 72–91).
Chapter 11
In: Thompson, T., Frith, K., & Pencheon, D. Sustainable Alves, R. R., & Alves, H. N. (2011). The faunal drugstore:
Healthcare. John Wiley & Sons. Animal-based remedies used in traditional medicines in Latin
Smith J. S. (2014). Health Impact of Pharmaceuticals in the America. Journal of ethnobiology and ethnomedicine, 7(9):
Environment and in Drinking Water: Potential for Human 1–43.
and Environmental Risk. (pp. 91–102) In: Goldstein, W., (ed) Alves, R.R.N. and Rosa, I.M.L. (2007). Biodiversity, traditional
Pharmaceutical Accumulation in the Environment: Prevention, medicine and public health: Where do they meet? Journal of
Control, Health Effects, and Economic Impact, CRC Press, Baton Ethnobiology and Ethnomedicine, 3: 14–22.
Rouge. 262pp.
Alves, R.R.N. and Rosa, I.M.L. (2005). Why study the use
Stackelberg, P. E., Furlong, E. T., Meyer, M. T., Zaugg, S. D., of animal products in traditional medicines? Journal of
Henderson, A. K., & Reissman, D. B. (2004). Persistence of Ethnobiology and Ethnomedicine, 1, 5–9.
pharmaceutical compounds and other organic wastewater
contaminants in a conventional drinking-water-treatment Anonymous, (2008). A renaissance in primary health care. The
plant. Science of the Total Environment, 329(1), 99–113. Lancet, 372: 9642. Available online at: http://www.thelancet.
com/journals/lancet/article/PIIS0140–6736(08)61369–0/
Taylor, D. (2010). Ecopharmacostewardship – a fulltext#
pharmaceutical industry perspective. In: Kümmerer and
Hempel (eds) Green and Sustainable Pharmacy (pp. 105–126). Balabanova, D., Mills, A., Conteh, L., Akkazieva, B.,
Springer Berlin Heidelberg. 313pp Banteyerga, H., Dash, U,Gilson, L., Hammer, A., Ibraimova,
A., Islam, Z., Kidanu, A., Koehlmoos, T P., Limwattananon,
Taylor, N. G., Verner-Jeffreys, D. W., & Baker-Austin, C. S., Muraleedharan, VR. Murzalieva G., Palafox B.,
(2011). Aquatic systems: maintaining, mixing and mobilising Panichkriangkrai, W., Patcharanrumol, W., Penn-Kekana
antimicrobial resistance?. Trends in Ecology & Evolution, 26(6), L., Powell-Jackson, T. Tangcharoensathien, V and McKee,
278–284. M (2013). Good health at low cost 25 years on: lessons
Vatovec, C., Senier, L., & Bell, M. (2013). An ecological for the future of health systems strengthening. The Lancet,
perspective on medical care: environmental, occupational, and 381(9883), 2118–2133.
public health impacts of medical supply and pharmaceutical Balick, M. J., & Cox, P. A. (1996). Plants, people, and culture:
chains. EcoHealth, 10(3), 257–267. the science of ethnobotany. Scientific American Library.
Vickery JA, Tallowin JR, Feber RE., Asteraki EJ, Atkinson PW, Battiste, M. 2010. Indigenous knowledge and indigenous
Fuller RJ, Brown VK, (2001). The management of lowland peoples’ education. In: S.M. Subramanian and B.
neutral grasslands in Britain: effects of agricultural practices Pisupati, (Eds.) (2010). Traditional Knowledge in Policy and
on birds and their food resources. Journal of Applied Ecology, Practice:Approaches to Development and Human Well-being.
38: 647–664. Tokyo: UNU Press, pp.31–51.

322 Connecting Global Priorities: Biodiversity and Human Health

Bertrand Graz, Healing and prevention: How can we Etkin, N. L. (2001). Perspectives in ethnopharmacology:
study effectiveness and safety of traditional medicines, forging a closer link between bioscience and traditional
and their public health importance. An Online course on empirical knowledge. Journal of ethnopharmacology, 76(2),
“The Retrospective Treatment Outcome Study (RTO) for 177–182.
Traditional Medicines”, available at http://globalhealthtrials.
FairWild Foundation, (2010). FairWild Standard: Version 2.0.
tghn.org/elearning/the-retrospective-treatment-outcome-
FairWild Foundation, Weinfelden, Switzerland. Retrieved
study/ (accessed on 04 August 2014)
from http://www.fairwild.org/documents/
Bode, Maarten, and G. Hariramamurthi. “Integrating folk
Ford, J. D., Berrang-Ford, L., King, M., & Furgal, C. (2010).
healers in India’s public health: acceptance, legitimacy and
Vulnerability of Aboriginal health systems in Canada to
emancipation.” eJIM-eJournal of Indian Medicine 7.1 (2015):
climate change. Global Environmental Change, 20(4),
1–20.
668–680.
Bodeker, G., Ong, C.K., Grundy, C., Burford, G., Shein, K.
Foundation for Revitalisation of Local Health Traditions
(2005) WHO Global Atlas of Traditional, Complementary
(FRLHT), (1999). The Key Role of Forestry Sector in
and Alternative Medicine, World Health Organization, Kobe.
Conserving India’s Medicinal Plants: Conceptual and
Bodeker G & Burford G. (2007). Traditional, Comlementary Operational Features. Bangalore: FRLHT.
and Alternative Medicine: Policy and Public Health
Foundation for Revitalisation of Local Health Traditions
Perspectives. Imperial College Press, London.
(FRLHT), 2009.Overview. Available at: <http://envis.frlht.
Bodeker, G., Neumann, C., (2012). Revitalization and org/overview.htm> [Accessed 4 August 2014].
Development of Karen Traditional Medicine for Sustainable
Gadgil. M., Seshagiri Rao, P.R., Utkarsh, G., Pramod, P. and
Refugee Health Services at the Thai–Burma Border. Journal
Chhatre, A. 2000, New meanings for old knowledge: The
of Immigrant & Refugee Studies, 10:6–30.
people’s biodiversity register program. Ecological Applications,
Bodeker, G. Van ‘t Klooster, C. and E. Weisbord. (2014). Prunus 10(5), pp.1307–1317.
africana (Hook.f.) Kalkman: The Overexploitation of a
Hamilton, A. C. (2004). Medicinal plants, conservation and
Medicinal Plant Species and Its Legal Context. The Journal
livelihoods. Biodiversity & Conservation, 13(8), 1477–1517.
of Alternative and Complementary Medicine (in press). 
Hamilton, A. C, Hamilton, P. (2006) Plant Conservation: An
Bodeker, G., Weisbord E, Diallo, D., Byamukama, R., Sekagya,
Ecosystem Approach, Earthscan.
Y. van ‘t Klooster, C.I.E.A., (2015). ‘African medicinal plants
and traditional medical knowledge: Access & Benefit Sharing Hariramamurthi, G., Venkatasubramanian, P. Unnikrishnan,
in the context of R&D’, in: Charles Wambebe & Philippe P. M. and Shankar, D. (2006). Home Herbal Gardens  – A
Rafita Rasoanaivo (Eds.), African Indigenous Medical Knowledge Novel Health Security Strategy Based on Local Knowledge
and Human Health (in press). and Resources in ‘Traditional, Complementary & Alternative
Medicine: Policy & Public Health Perspectives’, G Bodeker&
Brewer, J. K. (2014). Indigenous Knowledge and Intellectual
G Burford, Imperial College Press, London.
Property: Drug Research and Development in Contemporary
Context. Intel Prop Rights, 2(120), 2. Haverkort, B., Van’tHooft, K. and Hiemstra, W. (Eds.), (2003).
Ancient Roots New Shoots. Leusden: ETC/COMPAS and Zed
Bussmann, R.W. (2013). The globalization of traditional
Books.
medicine in northern Peru – from shamanism to molecules.
Evidence Based Complementary and Alternative Medicine. Article Hawkins, B. (2008) Plants for life: Medicinal plant
ID 291903, 46 pages, doi:10.1155/2013/291903. conservation and botanic gardens Botanic Gardens
Conservation International (BGCI)
Chivian, E. and Bernstein, A. (Eds.), (2008). Sustaining Life:
How Human Health Depends on Biodiversity. New York: Oxford Jenkins, T.N., (2000). Putting Post modernity into Practice:
University Press. Endogenous Development and the Role of Traditional
Cultures in the Rural Development of Marginal Regions.
Cunningham, G., (2005). The Jambi Kiwa Story – Mobilizing
Ecological Economics, 34, pp.301–314.
Assets for Community Development. Antigonish: The Coady
International Institute. Available at: http:// Kathe, W., Pätzold, B., Leaman, D.,Timoshyna, A., Newton,
D., Khou, E., Kinhal, G.,Sapkota I.B., Pasha, M.K.S., Ndam,
coady.stfx.ca/tinroom/assets/file/JAMBIenglishfin1.pdf .
N.,Melisch, R.,Bundalo, S., Honnef, S., Osborn, T.,Buitrón,
Accessed 04 August 2014.
X., and Liu,X, (2010), Wild for a Cure ground-truthing a
Diallo, D., Diakite, C., Mounkoro, P.P., Sangare, D., Graz, B., Standard for Sustainable Management of wild plants in the
Falquet, J. and Giani, S., (2007). [Knowledge of traditional Field: TRAFFIC International.
healers on malaria in Kendi (Bandiagara) and Finkolo (Sikasso)
Kim, J, Y., Farmer, P., and Porter, M.E., (2013), Redefining
in Mali ]. Mali Medical 22, 1–8.Fabricant D.S., Farnsworth,
global health-care delivery, The Lancet 382 (9897),
N.R., (2001) The value of plants used in traditional medicine
1060–1069..
for drug discovery. Environ Health Perspect 109 (Suppl 1):
69–75.
Etkin, N. L. (1988). Ethnopharmocology: biobehavioral
approaches in the anthropological study of indigenous
medicines. Annual Review of Anthropology, 23–42.

Connecting Global Priorities: Biodiversity and Human Health 323

 Kitalong, C , Tadao, V.R., Hillmann, A., Balick, M., Kennelly, Reading, C. L., & Wien, F. (2009). Health inequalities and
E., (2012) Phytochemical analysis of Palauan traditional the social determinants of Aboriginal peoples’ health. Prince
medicinal plant Phaleria nisidai to determine therapeutic George, BC: National Collaborating Centre for Aboriginal
dosing of Mangiferin, A C-glucosylxanthone.Planta Medica. Health.
78(11): PF1.
Reid, A. M. (2014). Rastas on the road to healing:
Milliken, T. and Shaw, J. 2012. The South Africa – Viet plant-human mobilities in Cape Town, South Africa.
Nam Rhino Horn Trade Nexus: A deadly combination of University of Cape Town, Cape Town. Available at:
institutional lapses, corrupt wildlife industry professionals https://open.uct.ac.za/bitstream/handle/11427/6795/
and Asian crime syndicates. TRAFFIC, Johannesburg, South thesis_hum_2014_reid_am.pdf
Africa.
Reyes-García, V. (2010). The relevance of traditional
Miththapala, S. (Ed.), (2006). Conserving Medicinal Species: knowledge systems for ethnopharmacological research:
Securing a Healthy Future, Colombo: IUCN Ecosystems and theoretical and methodological contributions. Journal of
Livelihoods Group, Asia. ethnobiology and ethnomedicine, 6(1), 32.
Montenegro, R. A., & Stephens, C. (2006). Indigenous health Roe, D. ed., (2010). Linking Biodiversity Conservation and
in Latin America and the Caribbean. The Lancet, 367(9525), Poverty Alleviation: A State of Knowledge Review. CBD Technical
1859–1869. Series no. 55. Montreal: Secretariat of the Convention on
Biological Diversity.
Multi-disciplinary University Traditional Health Initiative.
(MUTHI). About the Project. (2013). Retrieved at: www. Saslis-Lagoudakis, C. H., Savolainen, V., Williamson, E. M.,
mn.uio.no/farmasi/english/research/projects/muthi. Forest, F., Wagstaff, S. J., Baral, S. R., Watson, M F., C A., &
Accessed 13 March 2014. Hawkins, J. A. (2012). Phylogenies reveal predictive power
of traditional medicine in bioprospecting. Proceedings of the
Newman, D. and Cragg, G., (2007). Natural Products as
National Academy of Sciences, 109(39), 15835–15840.
Sources of New Drugs over theLast 25 years. Journal of
Natural Products, 70(3): 461–477. Schippmann, U., Leamann, D. & Cunningham, A.B., (2006),
A comparison of cultivation and wild collection of medicinal
Ningthoujam, S. S., Talukdar, A. D., Potsangbam, K. S., &
and aromatic plants under sustainability aspects.  – In:
Choudhury, M. D. (2012). Challenges in developing medicinal
Bogers, R.J., Craker, L.E. &Lange, D (Ed): Medicinal and
plant databases for sharing ethnopharmacological knowledge.
aromatic plants. Agricultural, commercial, ecological, legal,
Journal of ethnopharmacology, 141(1), 9–32.
pharmacological and social aspects. pp. 75–95, Springer,
Nunkoo, D. H., & Mahomoodally, M. F. (2012). Dordrecht (Wageningen UR Frontis Series 17).  Retrieved
Ethnopharmacological survey of native remedies commonly from  http://library.wur.nl/frontis/medicinal_aromatic_
used against infectious diseases in the tropical island of plants/06_schippmann.pdf, (Accessed 04 August 2014).
Mauritius. Journal of ethnopharmacology, 143(2), 548–564.
Shankar, D., (1992) Indigenous Health Services the state of
Payyappalli, U. 2010 Knowledge and Practitioners – Is There the Art. State of India’s health. New Delhi: Voluntary Health
a Promotional Bias in Traditional Knowledge in Policy and Association of India.
Practice: Approaches to Development and Wellbeing Suneetha
Shankar, D., P.M. Unnikrishnan and Padma
Subramanian and Pisupati, B., (eds.), Tokyo: UNU Press.
Venkatasubramanian, (2007). Need to Develop Inter-Cultural
Payyappallimana, U. 2010 Role of Traditional Medicine Standards for Quality, Safety and Efficacy of Traditional
in Primary Health Care: An Overview of Perspectives and Indian Systems of Medicine. Current Science, 92 (11).
Challenges, Yokohama Journal of Social Sciences, Vol. 14 No.
Stephens, C., Porter, J., Nettleton, C., & Willis, R. (2006).
6, 57–77
Disappearing, displaced, and undervalued: a call to action
Petersen, L. M., Charman, A. J., Moll, E. J., Collins, R. J., & for Indigenous health worldwide. The lancet, 367(9527),
Hockings, M. T. (2014a). “Bush Doctors and Wild Medicine”: 2019–2028.
The Scale of Trade in Cape Town’s Informal Economy of
Timmermans, K. (2003). Intellectual property rights and
Wild-Harvested Medicine and Traditional Healing. Society
traditional medicine: policy dilemmas at the interface. Social
& Natural Resources, 27(3): 315–336.
Science & Medicine, 57(4), 745–756.
Petersen, L. M., Moll, E. J., Hockings, M. T., & Collins, R. J.
UN COMTRADE, (2013). Data analysed from http://
(2014b). Implementing value chain analysis to investigate
comtrade.un.org/
drivers and sustainability of Cape Town’s informal economy
of wild-harvested traditional medicine. Local Environment: UN 2010 A65/314, (2010). Report of the Secretary General
27(3) 1–22. of the United Nations, Harmony with Nature.
Posey, D (Ed), (2000). Cultural and Spiritual Values of United Nations (1993) Agenda 21: Earth Summit – The
Biodiversity. UNEP, Nairobi. United Nations Programme of Action from Rio, UN
Publications, USA.
Rai, J.S., Thorheim, C., Dorjderem, A. and Macer, D., (2010).
Universalism and Ethical Values for the Environment – Ethics and Unnikrishnan, P.M., Suneetha M.S., (2012), Biodiversity,
Climate Change in the Asia Pacific (ECCAP) Working Group 1 Traditional Knowledge and Community Health-Strengthening
Report. Bangkok: UNESCO. Linkages, UNU-IAS, Yokohama.

324 Connecting Global Priorities: Biodiversity and Human Health

Unnikrishnan, P.M., Prakash, B.N. (2007) Traditional Herbal Albrecht, G., Sartore, G. M., Connor, L., Higginbotham, N.,
Medicines for Malaria Prevention, Endogenous Development Freeman, S., Kelly, B, Stain, H., Tonna A. & Pollard, G. (2007).
Magazine, Leusden: Compas, No.1. Solastalgia: The distress caused by environmental change.
Australasian Psychiatry, 15(S1), S95-S98.
UNU-IAS (2012) Biodiversity and Community Health:
connecting and linking nature, knowledge and practices on Alexandra Health (2010). Unveiling a New Chapter: Annual
the ground, Tokyo: UNU-IAS. Report 09/10 [Online]. Singapore: Alexandra Health.
Accessed from: http://www.ktph.com.sg/uploads/report/
Vandebroek, I. (2013). Intercultural health and ethnobotany:
documents/8373_AR%202009–2010.pdf [Accessed 21 May
How to improve healthcare for underserved and minority
2015].
communities?. Journal of ethnopharmacology, 148(3),
746–754. Annerstedt, M., Ostergren, P.,O., Bjork, J., Grahn, P., Skarback,
E., Wahrborg, P. (2012) Green qualities in the neighbourhood
Vandebroek, I., & Balick, M. J. (2012). Globalization and loss
and mental health – Results from a longitudinal cohort study
of plant knowledge: challenging the paradigm. PloS one, 7(5),
in Southern Sweden. BMC Public Health 12: 337.
e37643.
Aspinall, P. A., Mavros, P., Coyne, R., Roe, J. J., (2013) Urban
Van Damme, W., Meessen, B., Por, I. and Kober, K., (2003).
Brain: Analyzing outdoor physical activity with mobile EEG,
Catastrophic health expenditure, The Lancet, 362 (9388): 996.
British Journal of Sports Medicine, 06.03.2013, p. 1–7.
Waage, J., Banerji, R., Campbell, O., Chirwa, E., Collender,
Astell-Burt, T., X. Feng, S. Mavoa, H. M. Badland, and B.
G., Dieltiens, V., Dorward, A., Godfrey-Faussett, P.,
Giles-Corti. 2014. Do low-income neighbourhoods have the
Hanvoravongchai, P., Kingdon, G., Little, A., Mills, A.,
least green space? A cross-sectional study of Australia’s most
Mulholland, K., Mwinga, A., North, A., Patcharanarumol,
populous cities. BMC Public Health 14:292.
W., Poulton, C., Tangcharoensathien, V., Unterhalter, E.,
(2010) The Millennium Development Goals: A cross-sectoral Axelsen, J.B., Manrubia, S.. (2014). River density and
analysis and principles for goal setting after 2015. Lancet landscape roughness are universal determinants of linguistic
and London International Development Centre Commission, diversity. Proc. R. Soc. B: 281
http://download.thelancet.com/flatcontentassets/pdfs/
Berkes, F. (2008). Sacred Ecology. Traditional ecological
S0140673610611968.pdf Accessed 18 August 2014.
knowledge and resource management. Taylor & Francis.
Willcox, M. L., & Bodeker, G. (2004). Traditional herbal Philadelphia, 2nd Edition
medicines for malaria. British Medical Journal, 329(7475),
Barton, J., Pretty, J. (2010) What is the best dose of nature
1156–1159.
and green exercise for improving mental health? A multi-
Willcox ML, G.B., Falquet J, Diakite C, Giani S, Diallo D., study analysis. Environ Sci Technol 44:3947–3955.
(2011). A “reverse pharmacology” approach for developing an
Bauman, A.E., (2004) Updating the evidence that physical
anti-malarial phytomedicine. Malaria Journal, 10(Suppl 1), S8.
activity is good for health: an epidemiological review 2000–
World Health Organization (WHO). (1998). The World Health 2003. J Sci Med Sport 7:6–19.
Report 1998: Life in the 21st century a vision for all. In The
Beaglehole, R., Bonita, R., Horton, R., Adams, C., Alleyne,
world health report 1998: life in the 21st century A vision for all;
G., Asaria, P., Baugh, V., Bekedam, H., Billo, N., Casswell, S.,
World Health Organization.
Cecchini, M., Colagiuri, R., Colagiuri, S., Collins, T., Ebrahim,
WHO, (2000). General Guidelines for Methodologies S. M. G Engelga, Galea, T., Gaziano ,T,. Geneau, R., Haines,
onresearch and evaluation of traditional medicine. World A., Hospedales, J., Jha, P., Keeling, A., Leeder, S., Lincoln,
Health Organisation, Geneva. P., McKee, M., Mackay, J., Magnusson, R., Moodie, M.,
Mwatsama, J., Nishtar, J.,Norrving, B., Patterson, D., Piot,
WHO (2002). WHO traditional medicine strategy 2002–
P., Ralston, J., Rani, M., Reddy, K.S., Sassi, F., Sheron, N.,
2005. World Health Organisation, Geneva.
Stuckler, D., Suh, I., Torode, J., Varghese, C., Watt, J. (2011)
WHO (2005) National policy on traditional medicine and Priority actions for the non-communicable disease crisis. The
regulation of herbal medicines: Report of a WHO global Lancet 377: 1438–1447.
survey. World Health Organisation, Geneva.
Beaglehole, R., & Bonita, R. (2008). Global public health: a
WHO, (2008). The Bamako Call to Action for Research on scorecard. The Lancet, 372(9654), 1988–1996.
Health. Retrieved from: http://www.who.int/rpc/news/
Bell, J.D., Kronen, M., Vunisea, A., Nash, W.J., Keeble, G.,
BAMAKO CALL TO ACTION FinalNov24.pdf?ua=1. Accessed
Demmke, A., Pontifex, S., Andrefouet, S. (2009) Planning
13 March 2014.
the use of fish for food security in the Pacific. Mar Policy 33
WHO, (2013). WHO Traditional Medicine Strategy 2014– (1) 64 -76.
2023, Geneva.
Berger, B.G., Motl, R.W., (2000) Exercise and mood: a selective
review and synthesis of research employing the Profile of
Chapter 12 Mood States. J Appl Sport Psychol , 12:69–92.

Agenda 21 for Culture (2004). An undertaking by cities and Bixler, R. D., and Floyd, M. F. (1997). Nature is scary,
local governments for cultural development. Accessed from disgusting, and uncomfortable. Environment and Behavior,
http://www.bcn.cat/cultura/agenda21cultura/index_en.htm 29(4), 443–467.

Connecting Global Priorities: Biodiversity and Human Health 325

 Björk, J., Albin, M., Grahn, P., Jacobsson, H., Ardö, J., Wadbro, Cohen, B. (2006). Urbanization in developing countries:
J., Östergren, P.O., Skärbäck, E. (2008) Recreational values Current trends, future projections, and key challenges for
of the natural environment in relation to neighbourhood sustainability. Technology in society, 28(1), 63–80.
satisfaction, physicalactivity, obesity and wellbeing. J.
Collins ,P.Y., Patel, V. Joestl S.S., March, D., Insel, T.R., Daar,
Epidemiol. Commun. Health 62: e2.
A.S., Bordin, I.A., Costello, E.J., Durkin, M., Fairburn, C.,
Blair, S.N., Morris J.N. (2009) Healthy hearts  – and the Glass, R.I., Hall, W., Huang, Y., Hyman, S.E., Jamison, K.,
universal benefits of being physically active: physical activity Kaaya, S., Kapur, S., Kleinman, A., Ogunniyi, A., Otero-
and health. Ann Epidemiol, 19:253–256. Ojeda, A., Poo, M.M., Ravindranath, V., Sahakian, B.J.,
Saxena, S., Singer, P.A., Stein, D.J., Anderson, W., Dhansay,
Bowler, D.E., Buyung-Ali, L.M., Knight, T.M., Pullin,
M.A., Ewart, W., Phillips, A., Shurin, S., Walport, M. (2011)
A.S., (2010) A systematic review of evidence for
Grand challenges in global mental health. Nature 475: 27–30.
the added benefits to health of exposure to
natural environments. BMC Public Health 10, 456, Crawford, D., Timperio, A., Giles-Corti, B., Ball, K., Hume,
doi: 10.1186/1471–2458–10–456. C., Roberts, R., Salmon, J. (2008). Do features of public open
spaces vary according to neighbourhood socio-economic
Branas C.C.,  Cheney,  R., MacDonald,  J.M., Tam,  V.M.,
status? Health & Place, 14(4), 889–893. doi: doi:10.1016/j.
Jackson, T.D. and Ten Have, T.R. (2011). A Difference-in-
healthplace.2007.11.002
Differences Analysis of Health, Safety, and Greening Vacant
Urban Space. Am. J. Epidemiol. 174:1296–1306. Cummins, S., Stafford, M., Macintyre, S., Marmot, M.,
Ellaway, A., (2005). Neighbourhood environment and its
Bringslimark T, Hartig T, Patil GG (2007) Psychological
association with self-rated health: Evidence from Scotland
benefits of indoor plants in workplaces: Putting experimental
and England. J. Epidemiol. Commun. Health 59: 207–213.
results into context. HortScience 42, 581–587.
Cutts, B. B., Darby, K. J., Boone, C. G. and Brewis, A., (2009).
Brown WJ, Burton NW, Rowan PJ (2007) Updating the
City structure, obesity, and environmental justice: an
evidence on physical activity and health in women. Am J Prev
integrated analysis of physical and social barriers to walkable
Med 33:404–411.
streets and park access. Soc. Sci. Med. 69 1314–22.
Byrne, J., J. Wolch, and J. Zhang. (2009). Planning for
Dadvand, P., de Nazelle, A., Figueras, F., Basagaña, X.,
environmental justice in an urban national park. Journal of
Su, J., Amoly, E., Jerrett, M., Vrijheid, M., Sunyer, J. and
Environmental Planning and Management 52:365–392.
Nieuwenhuijsen, M. J. (2012). Green space, health inequality
Cairns-Nagi, J. M., and C. Bambra. (2013). Defying the odds: and pregnancy. Environment international, 40, 110–115.
A mixed-methods study of health resilience in deprived areas
Dallimer, M., Irvine, K., Skinner, A., Davies, Z., Rouquette,
of England. Social Science & Medicine 91:229–237.
J., Maltby, L., Warren, P., Armsworth, P., Gaston, K. (2012)
Carter M, Horwitz P (2014) Beyond Proximity: The Biodiversity and the feel-good factor: Understanding
Importance of Green Space Useability to Self-Reported associations between self- reported human well-being and
Health. EcoHealth. DOI: 10.1007/s10393–014–0952–9 species richness. BioScience 62: 47–55.
Champion, P.D., Burns, N.M. (2001). Lake Omapere: Current Daw, T., Brown, K., Rosendo, S., and Pomeroy, R. (2011).
understanding of ecological condition with short- and long- Applying the ecosystem services concept to poverty
term management options. National Institute of Water alleviation: the need to disaggregate human well-being.
and Atmospheric Research (NIWA) Consultancy Report Environmental Conservation 38:370–379.
MFE01231. Hamilton, NIWA.
de Jong K., Albin, M., Skärbäck, E., Grahn, P., Björk, J. (2012)
Charron, D. F. (2012). Ecohealth Research in Practice: Innovative Perceived green qualities were associated with neighborhood
Applications of an Ecosystem Approach to Health. Springer, New satisfaction, physical activity, and general health: Results
York, NY, USA / International Development Research Centre, from a cross-sectional study in sub-urban and rural Scania,
Ottawa, Canada. southern Sweden. Health Place 18: 1374–1380.
Chawla, L. (1999). Life paths into effective environmental Derr, V., & Lance, K. (2012). Biophilic Boulder: Children’s
action. The Journal of Environmental Education, 31(1), 15–26. Environments That Foster Connections to Nature. Children
Youth and Environments, 22(2), 112–143.
Clark, N. E., R. Lovell, B. W. Wheeler, S. L. Higgins, M. H.
Depledge, and K. Norris. (2014). Biodiversity, cultural de Vries, S., Verheij, R. A., Groenewegen, P. P. and
pathways, and human health: a framework. Trends in Ecology Spreeuwenberg, P. (2003). Natural environments – healthy
& Evolution. environments? An exploratory analysis of the relationship
between greenspace and health. Environment and Planning A
Coen, S.E., & Ross, N.A. (2006). Exploring the material
35:1717–1731.
basis for health: Characteristics of parks in Montreal
neighbourhoods with contrasting health outcomes. Health Diaz S, Fargione J, Chapin FS, Tilman D (2006) Biodiversity
& Place, 12(4), 361–371. loss threatens human well-being. PLoS Biol. 4: e277.
Cohen, M., R. Baudoin, M. Palibrk, N. Persyn, and C. Rhein. Dutcher, D. D., Finley, J. C., Luloff, A. E., & Johnson,
(2012). Urban biodiversity and social inequalities in built-up J. B. (2007). Connectivity with nature as a measure of
cities: New evidences, next questions. The example of Paris, environmental values. Environment and Behavior, 39(4), 474–
France. Landscape and Urban Planning 106:277–287. 493. doi:10.1177/0013916506298794

326 Connecting Global Priorities: Biodiversity and Human Health

Ellett, L., Freeman, D., Garety, P.A.(2008) The psychological Hamer, M., & Chida, Y. (2008). Active commuting and
effect of an urban environment on individuals with persecutory cardiovascular risk: a meta-analytic review. Preventive
delusions: The Camberwell walk study, Schizophrenia Research medicine, 46(1), 9–13.
99: 77–84
Han K (2009) Influence of limitedly visible leafy indoor plants
Ernstson, H. (2013). The social production of ecosystem on the psychology, behaviour, and health of students at a
services: A framework for studying environmental justice and junior high school in Taiwan. Environ. Behav. 41, 658–692.
ecological complexity in urbanized landscapes. Landscape and
Hankey, S., Lindsey, G., Wang, X., Borah, J., Hoff, K., Utecht,
Urban Planning 109:7–17.
B., & Xu, Z. (2012). Estimating use of non-motorized
Fjeld, T., Veiersted, B., Sandvik, L., Riise, G., Levy, F. (1998). infrastructure: Models of bicycle and pedestrian traffic in
The effect of indoor foliage plants on health and discomfort Minneapolis, MN. Landscape and Urban Planning, 107(3),
symptoms among office workers. Indoor Built Environ. 2, 307–316. doi:10.1016/j.landurbplan.2012.06.005.
204–209.
Hansmann, R,, Hug, S., Seeland, K. (2007). Restoration and
Francis, J., Wood, L. J., Knuiman, M., Giles-Corti, B. (2012). stress relief through physical activities in forests and parks.
Quality or quantity? Exploring the relationship between Urban Forestry Urban Greening 6, 213–225.
Public Open Space attributes and mental health in Perth,
Henwood, R., & Henwood, W. (2011). Mana whenua
Western Australia. Social Science & Medicine, 74 1570–1577.
kaitiakitanga in action: Restoring the mauri of Lake Ōmāpere.
doi: 10.1016/j.socscimed.2012.01.032
AlterNative: An International Journal of Indigenous Peoples, 7(3).
Fuller, R.A., Irvine, K.N., Devine- Wright, P., Warren, P.H.,
Hope, D., Gries, C., Zhu, W., Fagan, W. F., Redman, C. L.,
Gaston, K.J. (2007) Psychological benefits of green space
Grimm, N. B., Nelson, A.l., Martin, C. & Kinzig, A. (2003).
increase with biodiversity. Biol. Lett. 3: 390–394.
Socioeconomics drive urban plant diversity. Proceedings of the
Gavin MC, Sibanda N. (2012). The island biogeography of national academy of sciences, 100(15), 8788–8792.
languages. Global Ecology and Biogeography 21: 958–967.
Horwitz, P. and Finlayson, C.M. (2011). Wetlands as settings:
Garvin, E.C., Cannuscio, C.C., and Branas, C.C. (2013). using ecosystem services and health impact assessment for
Greening vacant lots to reduce violent crime: a randomised wetland and water resource management. BioScience 61:
controlled trial. Injury Prevention 19(3): 198–203. 678–688
Gee, K., and Burkhard, B., (2010). Cultural ecosystem services Hou, L., Ji, B. T., Blair, A., Dai, Q., Gao, Y. T., & Chow, W. H.
in the context of offshore wind farming: a case study from (2004). Commuting physical activity and risk of colon cancer
the west coast of Schleswig-Holstein. Ecological Complexity in Shanghai, China. American journal of epidemiology, 160(9),
7:349–358. 860–867.
Giles-Corti, B., Broomhall, M. H., Knuiman, M., Collins, Huynen, M. M. T. E., Martens, P., & De Groot, R. S. (2004).
C., Douglas, K., Ng, K., Lange, A. & Donovan, R. J. Linkages between biodiversity loss and human health: a global
(2005). Increasing walking: how important is distance to, indicator analysis. International Journal of Environmental
attractiveness, and size of public open space?. American Health Research, 14(1), 13–30.
journal of preventive medicine, 28(2), 169–176.
Jarrett, J., Woodcock, J., Griffiths, U. K., Chalabi, Z., Edwards,
Godbey, G. (2009). Outdoor recreation, health, and wellness: P., Roberts, I., & Haines, A. (2012). Effect of increasing active
Understanding and enhancing the relationship. RFF travel in urban England and Wales on costs to the National
Discussion Paper No. 09–21, May 6, 2009. Health Service. The Lancet, 379(9832), 2198–2205.
Goličnik, B., & Thompson, C. W. (2010). Emerging Jenkins, A.P., Jupiter, S.D. (2011) Spatial and seasonal
relationships between design and use of urban park spaces. patterns in freshwater ichthyofaunal communities of a
Landscape and Urban Planning, 94(1), 38–53.doi: 10.1016/j. tropical high island in Fiji. Environ Biol Fish 91(3):261–274.
landurbplan.2009.07.016
Jenkins, A.P., Jupiter, S.D., Qauqau, I., Atherton, J. (2010) The
Gorenflo, L. J., Romaine, S., Mittermeier, R. A., & Walker- importance of ecosystem-based management for conserving
Painemilla, K. (2012). Co-occurrence of linguistic and migratory pathways on tropical high islands: A case study
biological diversity in biodiversity hotspots and high from Fiji. Aquat Conserv 20(2):224–238.
biodiversity wilderness areas. Proceedings of the National
Jennings, V., Johnson Gaither, C., & Gragg, R. S. (2012).
Academy of Sciences, 109(21), 8032–8037.
Promoting environmental justice through urban green space
Gray, T. (2012). Review of the Lake Ōmāpere Restoration and access: a synopsis. Environmental Justice, 5(1), 1–7.
Management Project. Report prepared for Northland Regional
Jones, A., Hillsdon, M., & Coombes, E. (2009). Greenspace
Council. TEC Services. 87 p. Accessed from: http://www.nrc.
access, use, and physical activity: understanding the effects of
govt.nz/
area deprivation. Preventive medicine, 49(6), 500–505.
Grabow, M. L., Spak, S. N., Holloway, T., Stone Jr, B.,
Kabisch, N., & Haase, D. (2014). Green justice or just green?
Mednick, A. C., & Patz, J. A. (2012) Air quality and exercise-
Provision of urban green spaces in Berlin, Germany. Landscape
related health benefits from reduced car travel in the
and Urban Planning, 122, 129–139.
midwestern United States. Env Health Perspect. 120(1):68–
76. doi:10.1289/ehp.1103440. 

Connecting Global Priorities: Biodiversity and Human Health 327

 Kahn Jr, P. H., & Kellert, S. R. (2002). Children and nature: Lovell R, Wheeler BW, Higgins SL , Irvine KN, Depledge MH
Psychological, sociocultural, and evolutionary investigations. (2014) A Systematic Review of the Health and Well-Being
Cambridge, MA: MIT Press. Benefits of Biodiverse Environments, Journal of Toxicology
and Environmental Health, Part B: Critical Reviews, 17:1,
Kaplan R, Kaplan S (1989) The experience of nature: A
1–20.
psychological perspective New York, Cambridge University
Press. Luck GW, Davidson P, Boxall D, Smallbone L (2011) Relations
between urban bird and plant communities and human well-
Kaplan S (1995) The restorative benefits of nature: toward
being and connection to nature. Conserv. Biol. 25: 816–826.
an integrative framework. J Environ Psychol 15:169–182.
Maas, J., Verheij, R. A., Groenewegen, P. P., De Vries, S.,
Keller, H.A. 2001. “Etnobotánica de los guaraníes que habitan
& Spreeuwenberg, P. (2006). Green space, urbanity, and
la selva misionera”. Reunión de Comunicaciones Científicas y
health: how strong is the relation?. Journal of epidemiology
Tecnológicas 2001, UNNE, Corrientes, Argentina, Accessed
and community health, 60(7), 587–592.
from: http://www.unne.edu.ar/cyt/2001/6-biológicas/b-008.
pdf Maffi, L. (2005). Linguistic, Cultural and Biological Diversity.
Annu. Rev. Anthropol. 34:599–617.
Keniger, L. E., Gaston, K. J., Irvine, K. N., & Fuller, R. A.
(2013). What are the Benefits of Interacting with Nature?. Maller C, Townsend M, St Leger L, Henderson-Wilson C,
International journal of environmental research and public health, Pryor A, Prosser L, Moore M (2008). Healthy parks, healthy
10(3), 913–935, doi:10.3390/ijerph10030913 people: The health benefits of contact with nature in a park
context. A review of current literature (2nd ed.) Melbourne:
Kessel, A., Green, J., Pinder, R., Wilkinson, P., Grundy, C.,
Deakin University and Parks Victoria.
Lachowycz, K. (2009). Multidisciplinary research in public
health: A case study of research on access to green space. Maizlish N, Woodcock J, Co S, Ostro B, Fanai A, Fairley D.
Public Health, 123 32–38. doi: 10.1016/j.puhe.2008.08.005 Health cobenefits and transportation-related reductions
in greenhouse gas emissions in the San Francisco Bay
Kinzig, A. P., Warren, P., Martin, C., Hope, D., & Katti, M.
area. Am J Public Health. 2013;103(4):703–9. doi:10.2105/
(2005). The effects of human socioeconomic status and
ajph.2012.300939.
cultural characteristics on urban patterns of biodiversity.
Ecology and Society, 10(1), 23. Markevych, I., Tiesler, C. M., Fuertes, E., Romanos, M.,
Dadvand, P., Nieuwenhuijsen, M. J., et al. (2014). Access
Kuo, F. E., & Faber Taylor, A. (2004). A potential natural
to urban green spaces and behavioural problems in
treatment for attention-deficit/hyperactivity disorder:
children: Results from the GINIplus and LISAplus studies.
evidence from a national study. American journal of public
Environment international, 71, 29–35.
health, 94(9), 1580–1586.
Martin, C. A., Warren, P. S., & Kinzig, A. P. (2004).
Kuo, F.E. and Sullivan, W.C. (2001). Aggression and violence
Neighborhood socioeconomic status is a useful predictor of
in the inner city. Effects of environment via mental fatigue.
perennial landscape vegetation in residential neighborhoods
Environment and Behaviour 33: 543–571.
and embedded small parks of Phoenix, AZ. Landscape and
Lachowycz K, Jones AP (2011) Green space and obesity: Urban Planning, 69(4), 355–368.
A systematic review of the evidence. Obesity Rev. 12:
Mayer, F.S. and C. Frantz. (2004). The connectedness to
e183–e189.
nature scale: A measure of individuals’ feeling in community
Lee ACK, Maheswaran R (2010) The health benefits of urban with nature. Journal of Environmental Psychology. 24(4), 503–
green spaces: A review of the evidence. J. Public Health 33: 515. doi:10.1016/j.jenvp.2004.10.001
212–222.
McCurdy, L. E., Winterbottom, K. E., Mehta, S. S., & Roberts,
Lee, J., Park, B. J., Tsunetsugu, Y., Ohira, T., Kagawa, T., & J. R. (2010). Using nature and outdoor activity to improve
Miyazaki, Y. (2011). Effect of forest bathing on physiological children’s health. Current problems in pediatric and adolescent
and psychological responses in young Japanese male subjects. health care, 40(5), 102–117.
Public Health, 125(2), 93–100.
McGregor, D. P., Morelli, P. T., Matsuoka, J. K., Rodenhurst,
Lim, S. S., Vos, T., Flaxman, A. D., Danaei, G., Shibuya, R., Kong, N., & Spencer, M. S. (2003). An ecological model
K., Adair-Rohani, H., .et al. (2013). A comparative risk of Native Hawaiian well-being. Pacific health dialog, 10(2),
assessment of burden of disease and injury attributable to 106–128.
67 risk factors and risk factor clusters in 21 regions, 1990–
Milcu, A. I., Hanspach, J., Abson, D., & Fischer, J. (2013).
2010: a systematic analysis for the Global Burden of Disease
Cultural ecosystem services: a literature review and prospects
Study 2010. The Lancet, 380(9859), 2224–2260.
for future research. Ecol. Soc, 18(3), 44.
Little, B. R. (1983) ‘Personal projects: a rationale and method
Millennium Ecosystem Assessment. (2005). Ecosystems and
for investigation’ in Environment and Behavior, 15: 273–309.
Human Well-being: Synthesis., Washington, DC.
Logan, A. C. (2015). Dysbiotic drift: mental health,
Mitchell, R., Popham, F. (2007) Green space, urbanity and
environmental grey space, and microbiota. dementia, 8, 9.
health: Relationships in England. J. Epidemiol. Commun.
Louv, R. (2008). Last child in the woods: Saving our children from Health 61: 681–683.
nature-deficit disorder. Algonquin Books.

328 Connecting Global Priorities: Biodiversity and Human Health

Mitchell, R., Popham, F. (2008) Effect of exposure to natural Pretty, J, Adams, B., Berkes, F., de Athayde, S.F., Dudley,
environment on health inequalities: An observational N., Hunn, E., Maffi, L., Milton, K., Rapport, D., Robbins, P.,
population study. The Lancet 372: 1655–1660. Samson, C., Sterling, E., Stolton, S., Takeuchi, K., Tsing, A.,
Vintinner, E. and Pilgrim, S. (2008). How Do Biodiversity and
Mlambo M (2012) The urgent need for human well-being
Culture Intersect? Plenary paper for Conference “Sustaining
elements in biodiversity research. Biodivers. Conserv. 21:
Cultural and Biological Diversity In a Rapidly Changing World:
1149–1151.
Lessons for Global Policy”. Organized by American Museum of
Montenegro, R.A. 1992. “Ecodiversity or biodiversity? Natural History’s Center for Biodiversity and Conservation,
Towards new concepts”. In: “Biodiversity and International IUCN-The World Conservation Union/Theme on Culture and
Environmental Law”, S. Bilderbeck Ed., Ed. IOS Press-IUCN, Conservation, and Terralingua. April 2–5th 2008.
Amsterdam, pp. 47–48.
Pretty, J., Barton, J., Colbeck, I., Hine, R., Mourato, S.,
Montenegro, R.A. 2004. “Latin American experiences in Mackerron, G. and Wood, C. (2011). Health Values from
community based assessments. Joint works with the Mbya Ecosystems. Chapter 23 in UK National Ecosystem
indigenous communities of Tekoa Yma and Tekoa Kapi’i Assessment: Technical Report.
Yvate in the rainforest of Misiones (Argentina)”. Abstracts,
Pucher J, Buehler R, Bassett DR, Dannenberg AL. Walking and
3rd. International Conference on Children’s Health and
Cycling to Health: A Comparative Analysis of City, State, and
Environment, London School of Hygiene and Tropical
International Data. Am J Public Health. 2010;100(10):1986–
Medicine, University of London, p. 31.
1992. doi:10.2105/AJPH.2009.189324.
Montenegro, R.A. 2006. “El silencioso genocidio de los Mbya
Raudsepp-Hearne, C., Peterson, G. D., Tengö, M., Bennett, E.
Guarani”. Ed. FUNAM, Córdoba, Argentina, 231 p. To be
M., Holland, T., Benessaiah, K., MacDonald, G. K. and Pfeifer,
re published by Université de Franche Comté in France (in
G. K. (2010). Untangling the Environmentalist’s Paradox:
press).
Why Is Human Well-being Increasing as Ecosystem Services
Montenegro, R.A. and Stephens, C. (2006). Indigenous Degrade? BioScience 60:576–589.
Health in Latin America and the Caribbean. The Lancet,
Rethorst CD, Wipfli BM, Landers DM (2009) The
367:1859–1869.
antidepressive effects of exercise: a meta-analysis of
Montgomery, M. R. (2008). The urban transformation of the randomized trials. Sports Med 39:491–511.
developing world. Science, 319(5864), 761–764.
Richardson EA, Mitchell R (2010). Gender differences in
Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. relationships between urban green space and health in the
D., Michaud, C. et al. (2012). Disability-adjusted life years United Kingdom. Soc. Sci. Med. 71, 568–575.
(DALYs) for 291 diseases and injuries in 21 regions, 1990–
Roe, J. and Aspinall, P A. (2011a): The restorative outcomes
2010: a systematic analysis for the Global Burden of Disease
of forest versus indoor settings in young people with varying
Study 2010. The Lancet, 380(9859), 2197–2223.
behaviour states. Urban Forestry and Urban Greening, issue
Mustapa, Nor Diyana, Nor Zarifah Maliki, and Aswati 3, Volume 10.
Hamzah. (2015). Repositioning Children’s Developmental
Roe, J. and Aspinall, P A (2011b): The restorative benefits of
Needs in Space Planning: A Review of Connection to Nature.
walking in urban and rural settings in adults with good and poor
Procedia – Social and Behavioral Sciences 170 : 330–339.
mental health; Health and Place, 17: 103–113.
Nisbet, E. K., Zelenski, J. M., & Murphy, S. A. (2009).
Roe J, Ward Thompson C, Aspinall PA, Brewer MJ, Duff E,
The nature relatedness scale: Linking individuals’
Miller D, Mitchell R, Angela Clow (2013), Green Space and
connection with nature to environmental concern and
Stress: Evidence from Cortisol Measures in Deprived Urban
behavior. Environment and Behavior, 41(5), 715–740.
Communities, International Journal of Environmental
doi:10.1177/0013916508318748
Research and Public Health, 10(9): 4086–4103.
O’Brien, L., Townsend, M. & Ebden, M. (2008), ‘I like to think
Rook, G. A. W. (2013). Regulation of the immune system
when I’m gone I will have left this a better place’ – Environmental
by biodiversity from the natural environment: An ecosystem
volunteering: motivations, barriers and benefits, Report to the
service essential to health. Proc. Natl. Acad. Sci. U.S.A.,
Scottish Forestry Trust and Forestry Commission.
110(46): 18360–18367.
O’Campo P, Salmon C, Burke J (2009) Neighbourhoods and
Rydin, Y., Bleahu, A., Davies, M., Dávila, J. D., Friel, S., De
mental well-being: What are the pathways? Health & Place,
Grandis, G., Groce, N., et al. (2012). Shaping cities for health:
15(1), 56–68.
complexity and the planning of urban environments in the
Parks Canada. (2011, April). The VALUE of Visiting National 21st century. The Lancet, 379(9831), 2079–2108.
Parks. Social Science Branch (ERVE).
Sandifer, P. A., Sutton-Grier, A. E., & Ward, B. P. (2015).
Pereira G, Christian H, Foster S, Boruff B J, Bull F, Knuiman M, Exploring connections among nature, biodiversity, ecosystem
Giles-Corti B (2013). The association between neighborhood services, and human health and well-being: Opportunities
greenness and weight status: an observational study in Perth to enhance health and biodiversity conservation. Ecosystem
Western Australia. Environmental Health, 12, 49. doi: http:// Services, 12, 1–15.
www.ehjournal.net/content/12/1/49

Connecting Global Priorities: Biodiversity and Human Health 329

 Schizophrenia Commission (2012) The abandoned illness: a Townsend, M., Henderson-Wilson, C., Warner, E. and Weiss,
report from the Schizophrenia Commission. London: Rethink L. (2015). Healthy Parks Healthy People: the state of the evidence
Mental Illness. http://www.recoverydevon.co.uk/download/ 2015. Parks Victoria, Melbourne.
schizophrenia_commission_report.pdf last accessed 28.06.12
Ulrich RS (1981) Natural versus urban scenes: Some
Schultz, P. W. (2002). Inclusion with Nature: The Psychology psychophysiological effects. Environ Behav 13, 523–556.
Of Human-Nature Relations. In P. Schmuck & P.W. Schultz
Ulrich RS (1983) Aesthetic and affective response to natural
(Eds.), Psychology of Sustainable Development (pp. 61–78).
environment. Behavior and the natural environment New
Springer US.
York, Plenum Press 1983, 85–125.
Shin WS, Jaakson R, Kim EI (2001) Benefits-based analysis
Ulrich RS (1984). View through a window may influence
of visitor use of Sorak-San National Park in Korea. Environ
recovery from surgery. Science 224, 420–421.
Manage 28, 413–419.
UN-habitat, & United Nations Human Settlements
Shwartz A, Turbe A, Simon L, Julliard R. (2014). Enhancing
Programme. (2010). State of the World’s Cities 2010/11:
urban biodiversity and its influence on city-dwellers: an
Bridging the Urban Divide. Earthscan.
experiment. Biol Conservat. 171: 82–90.
Van den Berg AE, Custers MHG (2011) Gardening promotes
Skevington, S. (2009). Quality of Life, Biodiversity and
neuroendocrine and affective restoration from stress. J Health
Health: Observations and Applications. In Sala OE, Meyerson
Psychol 16, 3–11.
LA, & Parmesan C, 2009. Sala, O. E., Meyerson, L. A., &
Parmesan, C. (Eds.). (2012). Biodiversity change and human van Dillen SME., de Vries S, Groenewegen PP, Spreeuwenber
health: from ecosystem services to spread of disease, Island Press, P (2012) Green space in urban neighbourhoods and residents’
Washington DC, USA. health: Adding quality to quantity. J. Epidemiol. Commun.
Health 66: e8.
Speldewinde PC, Cook A, Davies P, Weinstein P (2009)
A relationship between environmental degradation and Veitch J, Ball K, Crawford D, Abbott GR, Salmon J. (2012).
mental health in rural Western Australia. Health and Place Park Improvements and Park Activity: A Natural Experiment.
15: 880–887. American Journal of Preventive Medicine, 42(6), 616–619. doi:
doi: 10.1016/j.amepre.2012.02.015.
Street, G., James, R., & Cutt, H. (2007). The relationship
between organised physical recreation and mental health. Veitch, J., Salmon, J., Carver, A., Timperio, A., Crawford, D.,
Health Promotion Journal of Australia, 18(3), 236–239. Fletcher, E., & Giles-Corti, B. (2014). A natural experiment
to examine the impact of park renewal on park-use and park-
Strohbach, M. W., Haase, D., & Kabisch, N. (2009). Birds and
based physical activity in a disadvantaged neighbourhood:
the city: urban biodiversity, land use, and socioeconomics.
the REVAMP study methods. BMC public health, 14(1), 600.
Ecology and Society, 14(2), 31.
Waltner-Toews, D. 2004. Ecosystem Sustainability and Health:
Sugiyama, T., Leslie, E., Giles-Corti, B., & Owen, N. (2008).
A Practical Approach. Cambridge University Press.
Associations of neighbourhood greenness with physical and
mental health: do walking, social coherence and local social Thompson, C. W., Roe, J., Aspinall, P., Mitchell, R., Clow, A.,
interaction explain the relationships? Journal of Epidemiology & Miller, D. (2012). More green space is linked to less stress
and Community Health, 62, 9. in deprived communities: Evidence from salivary cortisol
patterns. Landscape and Urban Planning, 105(3), 221–229.
Tanner CC, Clayton JS, Harper LM 1986. Observations on
Doi:10.1016/j.landurbplan.2011.12.015
aquatic macrophytes in 26 northern New Zealand lakes. New
Zealand Journal of Botany 24: 539–551. Webb, J., Mergler, D., Parkes, M. W., Saint-Charles, J., Spiegel,
J., Waltner-Toews, D., et al. (2010). Tools for Thoughtful
Taylor, A. F., Kuo, F. E., Spencer, C., & Blades, M. (2006). Is
Action: the role of ecosystem approaches to health in
contact with nature important for healthy child development?
enhancing public health. Canadian Journal of Public Health,
State of the evidence. Children and their environments:
101, 439–441.
Learning, using and designing spaces, 124.
Wellman, J. D., Roggenbuck, J. W., & Smith, A. C. (1982).
Thompson-Coon J, Boddy K, Stein RW, Barton J, Depledge
Recreation specialization and norms of depreciative behaviour
MH (2011) Does participating in physical activity in outdoor
among canoeists. Journal of Leisure Research, 14(4), 323–340.
natural environments have a greater effect on physical and
mental wellbeing than physical activity indoors? A systematic Wells, N. M. (2014). The Role of Nature in Children’s
review. Environ. Sci. Technol. 45: 1761–1772 Resilience: Cognitive and Social Processes. In Greening in
the Red Zone (pp. 95–109). Springer Netherlands.
Tilt J, Unfried T, Roca B (2007) Using objective and subjective
measures of neighborhood greenness and accessible Werner, P., & Zahner, R. (2010). Urban patterns and biological
destinations for understanding walking trips and BMI in diversity: a review. Urban biodiversity and design, (7), 145.
Seattle, Washington. Am. J. Health Promotion 21: 371–379.
Wilcox, B. A., Aguirre, A. A., & Horwitz, P. 2012) Connecting
Townsend, M. & Ebden, M. (2006), Feel Blue, Touch Green, Ecology, Health, and Sustainability. In A. A. Aguirre, R. S.
Final Report, Deakin University. Ostfeld, & P. Daszak (Eds.), New directions in conservation
medicine: Applied cases of ecological health. New York, NY:
Oxford University Press.

330 Connecting Global Priorities: Biodiversity and Human Health

Williams, D. R., & Huffman, M. G. (1986). Recreation Bandyopadhyay, J; Kraemer, D; Kattelmann, R and
specialization as a factor in backcountry trail choice. General Kundzewicz, ZW (1997) ‘Highland waters: A resource of
Technical Report, Intermountain Research Station, USDA Forest global signi_cance.’ In Messerli, B; Ives, JD (eds), Mountains
Service, (INT-212), 339–344. of the World: A Global Priority, pp 131–155. New York, USA:
Parthenon.
Wilson, E. O. (1984). Biophilia. Harvard University Press.
Barlow, J. and Peres, C.A. (2008) Fire-mediated dieback and
World Health Organization (WHO). (2001). Strengthening
compositional cascade in an Amazonian forest. Philosophical
mental health promotion (Fact Sheet No. 220). World Health
Transactions of the Royal Society B: Biological Sciences, 363 ,
Organisation. Geneva, Switzerland.
1787–1794.
Woodcock, J., Edwards, P., Tonne, C., Armstrong, B. G.,
Barriopedro, D., Fischer, E.M., Luterbacher, J., Trigo, R.M.
Ashiru, O., Banister, D., et al. (2009). Public health benefits
& García-Herrera, R. (2011). The hot summer of 2010:
of strategies to reduce greenhouse-gas emissions: urban land
redrawing the temperature record map of Europe. Science,
transport. The Lancet, 374(9705), 1930–1943.
332, 220–224.
World Health Organization (WHO). (2013). Mental health
Bausch, D.G. & Schwarz, L. (2014). Outbreak of Ebola virus
action plan 2013–2020. World Health Organization. Geneva,
disease in Guinea: where ecology meets economy. PLoS
Switzerland.
Neglected Tropical Diseases, 8, e3056.
World Health Organisation Quality of Life Assessment
Beaumont, L. J., Pitman, A., Perkins, S., Zimmermann, N. E.,
Group (WHOQOL) (1994). Development of the WHOQOL:
Yoccoz, N. G., & Thuiller, W. (2011). Impacts of climate change
Rationale and current status. International Journal of Mental
on the world’s most exceptional ecoregions. Proceedings of the
Health 23(3); 24–26
National Academy of Sciences, 108(6), 2306–2311.
Yamaguchi M, Deguchi M, Miyazaki Y (2006) The effects of
Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., &
exercise in forest and urban environments on sympathetic
Courchamp, F. (2012). Impacts of climate change on the
nervous activity of normal young adults. J. Int. Med. Res. 34,
future of biodiversity. Ecology letters, 15(4), 365–377.
152–159.
Birkmann, J., Garschagen, M., Kraas, F., & Quang, N. (2010).
Zelenski, J. M., & Nisbet, E. K. (2014). Happiness and
Adaptive urban governance: new challenges for the second
feeling connected: The distinct role of nature relatedness.
generation of urban adaptation strategies to climate change.
Environment and Behavior, 46(1), 3–23.
Sustainability Science, 5(2), 185–206.
Zylstra, M. (2014). Exploring meaningful nature experience
Bogardi, J. J., Dudgeon, D., Lawford, R., Flinkerbusch, E.,
connectedness with nature and the revitalization of transformative
Meyn, A., Pahl-Wostl, C., Vielhauer, K., & Vörösmarty,
education for sustainability (Dissertation). Stellenbosch
C. (2012). Water security for a planet under pressure:
University, South Africa.
interconnected challenges of a changing world call for
sustainable solutions. Current Opinion in Environmental
Chapter 13 Sustainability, 4(1), 35–43.

Ahmed, M., & Suphachalasai, S. (2014). Assessing the Costs of Boyden, S. (2004). The Biology of Civilisation: Understanding
Climate Change and Adaptation in South Asia, Mandaluyong Human Culture as a Force in Nature, Sydney; UNSW Press.
City, Philippines: Asian Development Bank. Bush,M. B., Silman,M. R.,McMichael, C. and Saatchi, S.
Ali, M., Lopez, A. L., You, Y., Kim, Y. E., Sah, B., Maskery, B., (2008) Fire, climate change and biodiversity in Amazonia:
& Clemens, J. (2012). The global burden of cholera. Bulletin a Late-Holocene perspective. Philosophical Transactions of the
of the World Health Organization, 90(3), 209–218. Royal Society B-Biological Sciences, 363, 1795–1802.

Altizer, S., Ostfeld, R.S., Johnson, P.T.J., Kutz, S. & Harvell, Butler, C.D. (2014a). Climate change and global health: a new
C.D. (2013). Climate change and infectious diseases: from conceptual framework – Mini Review. CAB Reviews, 9, 027.
evidence to a predictive framework. Science, 341, 514–519. Butler, C.D. (ed.) (2014b). Climate Change and Global Health,
Anonymous 1989. Health in the greenhouse. The Lancet, 333, Wallingford UK, Boston, US: CABI.
819–820. Butler, C.D. (2000). Inequality, global change and the
Armstrong, R. L. (2010). The glaciers of the Hindu Kush- sustainability of civilisation. Global Change and Human Health,
Himalayan region: a summary of the science regarding glacier 1, 156–172.
melt/retreat in the Himalayan, Hindu Kush, Karakoram, Pamir, Callendar, G.S. (1958). On the amount of carbon dioxide in
and Tien Shan mountain ranges. International Centre for the atmosphere. Tellus, 10, 243–248.
Integrated Mountain Development (ICIMOD).
Campbell, A., Kapos, V., Scharlemann, J. P.W., Bubb, P.,
Bajracharya, S. R., & Shrestha, B. (2011). The status of glaciers Chenery, A., Coad, L., Dickson, B., Doswald, N., Khan, M. S.
in the Hindu Kush-Himalayan region. International Centre for I., Kershaw, F. and Rashid, M. (2009). Review of the Literature
Integrated Mountain Development (ICIMOD). on the Links between Biodiversity and Climate Change: Impacts,
Adaptation and Mitigation. Secretariat of the Convention on
Biological Diversity, Montreal. Technical Series No. 42, 124
pages.

Connecting Global Priorities: Biodiversity and Human Health 331

 Carpenter, K. E., Abrar, M., Aeby, G., Aronson, R. B., Banks, Convention on Biological Diversity (CBD) (2003).
S., Bruckner, A., Chiriboga, A., Cortes, J., Delbeek, J., De Interlinkages between biological diversity and climate change.
Vantier, L., Edgar, G., Edwards, A., Fenner, D., Guzman, Advice on the integration of biodiversity considerations into the
H., Hoeksema, B., Hodgson, G., Johan, O., Licuanan, W., implementation of the United Nations Framework Convention on
Livingstone, S., Lovell, E., Moore, J., Obura, D., Ochavillo, D., Climate Change and its Kyoto protocol. Montreal, SCBD, 154 pp.
Polidoro, B., Precht, W., Quibilan, M., Reboton, C., Richards, (CBD Technical Series no. 10).
Z., Rogers, A., Sanciangco, J., Sheppard, A., Sheppard, C.,
Corvalán, C., Hales, S., McMichael, A.J., Butler C.D., Campbell-
smith, J., Stuart, S., Turak, E., Veron, J., Wallace, C., Weil,
Lendrum D., Confalonieri U., Leitner, K., Lewis, N., Patz, J.,
E., & Wood, E. (2008). One-third of reef-building corals
Polson, K., Scheraga, J., Woodward, A., Younes, M., & MA
face elevated extinction risk from climate change and local
authors. (2005). Ecosystems and Human Well-Being. Health
impacts. Science, 321(5888), 560–563.
Synthesis. Geneva, Switzerland: World Health Organization.
Castree, N., Adams, W.M., Barry, J., Brockington, D., Buscher,
Costello, A., Abbas, M., Allen, A., Ball, S., Bell, S., Bellamy,
B., Corbera, E., Demeritt, D., Duffy, R., Felt, U., Neves, K.,
R., Friel, S., Groce, N., Johnson, A., Kett, M., Lee, M., Levy.,
Newell, P., Pellizzoni, L., Rigby, K., Robbins, P., Robin, L.,
C., Maslin, M., McCoy, D., McGuire, B., Montgomery, H.,
Bird Rose, D., Ross, A., Schlossberg, D., Soerlin, S., West, P.,
Napier, D., Pagel, C., Patel, J., Puppim de Oliveira, J.A.,
Whitehead, M., & Wynne, B. (2014). Changing the intellectual
Redclift, N., Rees, H., Rogger, D., Scott, J., Stephenson,
climate. Nature Clim. Change, 4, 763–768.
J., Twigg, J., Wolff, J., Patterson, C. (2009). Managing the
Cavaliere, C. (2009). The effects of climate change on health effects of climate change: lancet and University College
medicinal and aromatic plants. Herbal Gram, 81, 44–57. London Institute for Global Health Commission. The Lancet,
373(9676), 1693–1733.
Center for International Forestry Research (CIFOR). (2007).
Reducing Emissions from Deforestation. Carbon Forestry Research Cramer, W., Bondeau, A., Woodward, F. I., Prentice, I. C.,
Program. Available at: www.cifor.cgiar.org/carbofor. Betts, R. A., Brovkin, V., Cox, P.M., Fisher, V., Foley, J.A.,
Friend, A.D., Kucharik, C., Lomas, M., Ramankutty, N., Sitch,
Chapin, F.S. III, Callaghan, T.V., Bergeron, Y., Fukuda, M.,
S., Smith, B., White, A., Young-Molling, C. (2001). Global
Johnstone, J.F., Juday, G. & Zimov, S. (2004). Global Change
response of terrestrial ecosystem structure and function to
and the Boreal Forest: Thresholds, Shifting States, or Gradual
CO2 and climate change: results from six dynamic global
Change. Ambio, 33: 361–365.
vegetation models. Global change biology, 7(4), 357–373.
Chaudhary, P., & Aryal, K. P. (2009). Global Warming in
Das, S. & Vincent, J.R. (2009). Mangroves protected villages
Nepal: Challenges and Policy Imperatives. Journal of Forest
and reduced death toll during Indian super cyclone. Proceedings
and Livelihood, 8(1), 4–13.
of the National Academy of Sciences, 106, 7357–7360.
Chettri, N., Bandana Shakya, B., and Sharma, E. (2011).
Destouni, G., F. Jaramillo, and C. Prieto C. 2013. Hydro-
Enhancing Ecological And People’s Resilience: Implementing
climatic shifts driven by human water use for food and energy
the CBD’s Ecosystem Approach in the Hindu Kush-Himalayan
production. Nature Climate Change 3:213–217.
Region. In CBD, Secretariat (2011). Contribution of Ecosystem
Restoration to the Objectives of the CBD and a Healthy Planet Doney, S. C., Fabry, V. J., Feely, R. A., & Kleypas, J. A. (2009).
for All People. Abstracts of Posters Presented at the 15th Ocean acidification: the other CO2 problem. Marine Science, 1.
Meeting of the Subsidiary Body on Scientific, Technical
Dora, C., Haines, A., Balbus, J., Fletcher, E., Adair-Rohani,
and Technological Advice of the Convention on Biological
H., Alabaster, G., Hossain, R., de Onis, M., Branca, F., Neira,
Diversity, 7–11 November 2011, Montreal, Canada. Technical
M. (2014). Indicators linking health and sustainability in
Series No. 62. Montreal, SCBD, 116 pp.
the post-2015 development agenda. The Lancet, published
Chua, K.B. (2003). Nipah virus outbreak in Malaysia. Journal on-line. DOI: 10.1016/S0140–6736(14)60605-X.
of Clinical Virology 26, 265–275.
Doswald, N., & Osti, M. (2011). Ecosystem-based Approaches
Convention on Biological Diversity (CBD) (2014) Global to Adaptation and Mitigation: Good Practice Examples and
Biodiversity Outlook 4. Secretariat of the Convention on Lessons Learned in Europe. BfN, Federal Agency for Nature
Biological Diversity, Montreal. Conservation.
Convention on Biological Diversity (CBD) (2012). CBD, Ebi, K. L., Woodruff, R., von Hildebrand, A., & Corvalan, C.
Secretariat. (2012). Report of the expert group on maintaining (2007). Climate change-related health impacts in the Hindu
the ability of biodiversity to continue to support the water cycle. Kush–Himalayas. EcoHealth, 4(3), 264–270.
UNEP/CBD/COP/11/INF/2.
Elmhagen, B., Destouni, G., Angerbjörn, A., Borgström, S.,
Convention on Biological Diversity (CBD) (2010) Global Boyd, E., Cousins, S. A et al.(2015). Interacting effects of
Biodiversity Outlook 3. Secretariat of the Convention on change in climate, human population, land use, and water
Biological Diversity, Montreal. use on biodiversity and ecosystem services. Ecology and
Society, 20(1), 23.
Convention on Biological Diversity (2009). Connecting
Biodiversity and Climate Change Mitigation and Adaptation: Epstein, P. R. (2001). Climate change and emerging infectious
Report of the Second Ad Hoc Technical Expert Group on diseases. Microbes and infection, 3(9), 747–754.
Biodiversity and Climate Change. Montreal, Technical Series
No. 41, 126 pages.

332 Connecting Global Priorities: Biodiversity and Human Health

Eriksson, M., Jianchu, X., Shrestha, A. B., Vaidya, R. A., Nepal, Heller, N. E., & Zavaleta, E. S. (2009). Biodiversity
S., & Sandström, K. (2009). The changing Himalayas: impact of management in the face of climate change: a review of 22
climate change on water resources and livelihoods in the greater years of recommendations. Biological conservation, 142(1),
Himalayas. International centre for integrated mountain 14–32.
development (ICIMOD).
Hoberg, E. P., & Brooks, D. R. (2015). Evolution in action:
Fabre, B., Piou, D., Desprez-Loustau, M.-L., & Marçais, B. climate change, biodiversity dynamics and emerging
(2011). Can the emergence of pine Diplodia shoot blight in infectious disease. Philosophical Transactions of the Royal
France be explained by changes in pathogen pressure linked Society of London B: Biological Sciences, 370(1665),
to climate change? Global Change Biology, 17, 3218–3227. 20130553.
Feachem, R., Phillips, A.A., Hwang, J., Cotter, C., Wielgosz, Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck,
B., Greenwood, B.M., Sabot, O., Rodriguez, M., Abeyasinghe, R. S., Greenfield, P., Gomez, E., Harvell, C., Sale, P., Edwards,
R., Ghebreyesus, T., Snow, R. (2010). Shrinking the malaria A., Caldeira, K., Knowlton, N., Eakin, C., Iglesias-Prieto,
map: progress and prospects. The Lancet, 376, 1566–1578. R., Muthiga, N., Bradbury, R., Dubi, A., & Hatziolos, M. E.
(2007). Coral reefs under rapid climate change and ocean
February, E. C.,West,A. G. and Newton, R. J. (2007) The
acidification. Science, 318(5857), 1737–1742.
relationship between rainfall, water source and growth for
an endangered tree. Austral Ecology, 32 , 397–402. Horton, R. (2013). Offline: Planetary health – a new vision
for the post-2015 era. The Lancet, 382, 1012.
Fleurbaey, M. & Blanchet, D. (2013). Beyond GDP: Measuring
Welfare and Assessing Sustainability, New York, Oxford Huq, A., Small, E. B., West, P. A., Huq, M. I., Rahman, R., &
University Press. Colwell, R. R. (1983). Ecological relationships between Vibrio
cholerae and planktonic crustacean copepods. Applied and
Food and Agriculture Organization (FAO). FAO World Food
Environmental Microbiology, 45(1), 275–283.
Summit: Factsheet Water and Food Security. Available online:
www.fao.org/worldfoodsummit/english/fsheets/water.pdf. Intergovernmental Panel on Climate Change (IPCC).
(2014a). Chapter 1, In: Climate Change 2014, Mitigation of
Gething, P.W., Smith, D.L., Patil, A.P., Tatem, A.J., Snow, R.W.
Climate Change. Contribution of Working Group III to the
& Hay, S.I. (2010). Climate change and the global malaria
Fifth Assessment Report of the Intergovernmental Panel
recession. Nature, 465, 342–346.
on Climate Change [Edenhofer, O., R. Pichs-Madruga, Y.
Goulden, M., Naess, L.O., Vincent, K., Adger, W.N. (2009). Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I.
Accessing diversification, networks and traditional resource Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen,
management as adaptations to climate extremes. In: Adapting S. Schl.mer, C. von Stechow, T. Zwickel and J.C. Minx (eds.)].
to Climate Change: Thresholds, Values, Governance; Adger, W.N., Cambridge University Press, Cambridge, United Kingdom
Lorenzoni, I., O’Brien, K.L., Eds.; University of Cambridge: and New York, NY, USA.
Cambridge, UK; pp. 448–463.
Intergovernmental Panel on Climate Change (IPCC). (2014b).
Haines, A., Kovats, R. S., Campbell-Lendrum, D., & Corvalán, Technical Summary, In: Climate Change 2014, Mitigation of
C. (2006). Climate change and human health: Impacts, Climate Change. Contribution of Working Group III to the
vulnerability and public health. Public health, 120(7), Fifth Assessment Report of the Intergovernmental Panel
585–596. on Climate Change [Edenhofer, O., R. Pichs-Madruga, Y.
Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I.
Haines, A., Alleyne, G., Kickbusch, I. & Dora, C. (2012).
Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen,
From the Earth Summit to Rio+20: integration of health
S. Schl.mer, C. von Stechow, T. Zwickel and J.C. Minx (eds.)].
and sustainable development. The Lancet, 379, 2189–2197.
Cambridge University Press, Cambridge, United Kingdom
Haines, A., McMichael, A.J., Smith, K.R., Roberts, I., and New York, NY, USA.
Woodcock, J., Markandya, A.,Armstrong, B., Campbell-
Intergovernmental Panel on Climate Change (IPCC).
Lendrum, D., Dangour, A., Davies, M., Bruce, N., Tonne, C.,
(2014c). Chapter 11: Agriculture, Forestry and Other
Barrett, M., Wilkinson, P.. (2009). Public health effects of
Land Use (AFOLU), In: Climate Change 2014, Mitigation of
strategies to reduce greenhouse-gas emissions: overview and
Climate Change. Contribution of Working Group III to the
implications for policy makers. The Lancet, 374, 2104–2114.
Fifth Assessment Report of the Intergovernmental Panel
Hales, S., Edwards, S., Kovats, R. (2003). Impacts on on Climate Change [Edenhofer, O., R. Pichs-Madruga, Y.
health of climate extremes. In:McMichael, A., ed. Climate Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I.
change and health: risks and responses. Geneva, World Health Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen,
Organization. S. Schl.mer, C. von Stechow, T. Zwickel and J.C. Minx (eds.)].
Cambridge University Press, Cambridge, United Kingdom
Harley, C. D., Randall Hughes, A., Hultgren, K. M., Miner, B.
and New York, NY, USA.
G., Sorte, C. J., Thornber, C. S., Rodriguez, L., Tomanek, L.,
& Williams, S. L. (2006). The impacts of climate change in
coastal marine systems. Ecology letters, 9(2), 228–241.
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson,
A. P., Ostfeld, R. S., & Samuel, M. D. (2002). Climate warming
and disease risks for terrestrial and marine biota. Science,
296(5576), 2158–2162.

Connecting Global Priorities: Biodiversity and Human Health 333

 Intergovernmental Panel on Climate Change (IPCC). McMichael, T., Montgomery, H. and Costello, A. (2012).
(2014d). Summary for policymakers. In: Climate Change Health risks, present and future, from global climate change.
2014: Impacts, Adaptation, and Vulnerability. Part A: Global British Medical Journal, 344, e1359-e1363.
and Sectoral Aspects. Contribution of Working Group II to the
McMichael, A.J. & Wilcox, B.A. (2009). Climate change,
Fifth Assessment Report of the Intergovernmental Panel on
human health, and integrative research: a transformative
Climate Change [Field, C.B., V.R. Barros, D.J. Dokken, K.J.
imperative. EcoHealth, 6, 163–165.
Mach, M.D. Mastrandrea, T.E. Bilir, M. Chatterjee, K.L. Ebi,
Y.O. Estrada, R.C. Genova, B. Girma, E.S. Kissel, A.N. Levy, McMichael, A. J., Campbell-Lendrum, D. H., Corvalán, C.
S. MacCracken, P.R. Mastrandrea, and L.L. White (eds.)]. F., Ebi, K. L., Githeko, A. K., Scheraga, J. D., & Woodward,
Cambridge University Press, Cambridge, United Kingdom A. (2003). Climate change and human health: risks and
and New York, NY, USA, pp. 1–32. responses. World Health Organization.
Jeger, M. J., & Pautasso, M. (2008). Plant disease and McMichael, A.J., Smith, K.R. & Corvalan, C.F. (2000). The
global change – the importance of long-term data sets. New sustainability transition: a new challenge [editorial]. Bulletin
Phytologist, 177, 8–11. of the World Health Organization, 78, 1067.
Johnstone, S. & Mazo, J. 2011. Global Warming and the Arab McMichael, A.J., Haines, A., Slooff, R. & Kovats, S. (eds.)
Spring. Survival, 53, 11–17. 1996. Climate Change and Human Health, Geneva: World
Health Organization.
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk,
D., Gittleman, J. L., & Daszak, P. (2008). Global trends in Millennium Ecosystem Assessment (MA). (2005), Ecosystems
emerging infectious diseases. Nature, 451(7181), 990–993. and Human Well-being: Biodiversity Synthesis, Washington, DC
(World Resources Institute).
Lafferty, K.D. 2009. The ecology of climate change and
infectious diseases. Ecology, 90, 888–900. Munang, R., Thiaw, I., Alverson, K., Mumba, M., Liu, J.,
& Rivington, M. (2013). Climate change and Ecosystem-
Lambin, E. F., Turner, B. L., Geist, H. J., Agbola, S. B.,
based Adaptation: a new pragmatic approach to buffering
Angelsen, A., Bruce, J. W., Coomes, O., Dirzo, R., Fischer, G.,
climate change impacts. Current Opinion in Environmental
Folke, C., George, P., Homewood, K., Imbernon, J., Leemans,
Sustainability, 5(1), 67–71.
R., Li, X., Moran, E., Mortimore, M., Ramakrishnan, P.,
Richards, J., Skanes, H., Steffen, W., Stone, G., Svedin, U., Naumann, Sandra, Gerardo Anzaldua, Pam Berry, Sarah
Veldkamp, T., Vogel, C., & Xu, J. (2001). The causes of land- Burch, McKenna Davis, Ana Frelih-Larsen, Holger Gerdes
use and land-cover change: moving beyond the myths. Global and Michele Sanders (2011): Assessment of the potential of
environmental change, 11(4), 261–269. ecosystem-based approaches to climate change adaptation and
mitigation in Europe. Final report to the European Commission,
Lancet-Rockefeller Foundation Commission on Planetary
DG Environment, Contract no. 070307/2010/580412/SER/
Health (2015) forthcoming
B2, Ecologic institute and Environmental Change Institute,
Lapola, D. M., Oyama, M. D., & Nobre, C. A. (2009). Exploring Oxford University Centre for the Environment
the range of climate biome projections for tropical South
Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C.,
America: the role of CO2 fertilization and seasonality. Global
Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos,
Biogeochemical Cycles, 23(3).
F., Key, R., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray,
Leaf, A. 1989. Potential health effects of global climatic and P., Mouchet, A., Najjar, R., Plattner, G., Rodgers, K., Sabine,
environmental changes. The New England Journal of Medicine, C., Sarmiento, J., Schlitzer, R., Slater, R., Totterdell, I., Weirig,
321, 1577–1583. M., Yamanaka, Y., & Yool, A. (2005). Anthropogenic ocean
acidification over the twenty-first century and its impact on
Lipp, E. K., Huq, A., & Colwell, R. R. (2002). Effects of global
calcifying organisms. Nature, 437(7059), 681–686.
climate on infectious disease: the cholera model. Clinical
microbiology reviews, 15(4), 757–770. Padulosi, S., Heywood, V., Hunter, D., & Jarvis, A. (2011).
Underutilized species and climate change: current status
Luis, A.D., Hayman, D.T.S., O’Shea, T.J., Cryan, P.M., Gilbert,
and outlook. Crop Adaptation to Climate Change. Blackwell
A.T., Pulliam, J.R.C.,Mills, J., Timonin, M., Willis, C.,
Publishing Ltd, UK, 507–521.
Cunningham, A., Fooks, A., Rupprecht, C., Wood, J., & Webb,
C. 2013. A comparison of bats and rodents as reservoirs of Parmesan, C., & Yohe, G. (2003). A globally coherent
zoonotic viruses: are bats special? Proceedings of the Royal fingerprint of climate change impacts across natural systems.
Society B: Biological Sciences, 280. Nature, 421(6918), 37–42.
Martínez, R., Hemming, D., Malone, L., Bermudez, N., Parmesan, C. (2006). Ecological and evolutionary responses
Cockfield, G., Diongue, A., Hansen, J., Hildebrand, A., Ingram, to recent climate change. Annual Review of Ecology, Evolution,
K., Jakeman, G., Kadi, M., McGregor, G., Mushtag, S., Rao, P., and Systematics, 637–669.
Pulwarty, R., Ndiaye, O., Srinavasan, G., Seck, Eh., White, N.
Parmesan, C., & Matthews, J. (2006). Biological impacts of
& Zougmoré, R. (2012). Improving climate risk management
climate change. Principles of Conservation Biology. Sinauer
at local level–techniques, case studies, good practices and
Associates, Inc. Sunderland, Massachusetts, 333–374.
guidelines for World Meteorological Organization members.

334 Connecting Global Priorities: Biodiversity and Human Health

Parmesan, C., & Martens, P. (2009). Climate change, wildlife, Rockström, J., Steffen, W., Noone, K., Persson, Å., F. Stuart
and human health. In SCOPE / DIVERSITAS Assessment: Chapin, I., Lambin, E.F., Lenton, T., Scheffer, M., Folke1, C.,
Biodiversity Change and Human Health: From Ecosystem Schellnhuber, H., J., Nykvist, B., de Wit, C., Hughes, T., van
Services to Spread of Disease, Island Press. der Leeuw, S., Rodhe, H., Sörlin, S., Snyder, P., Costanza, R.,
Svedin, U., Falkenmark, M., Karlberg, L., Corell, R., Fabry, V.,
Parmesan, C., Duarte, C., Poloczanska, E., Richardson, A.J.
Hansen, J., Walker, B., Liverman, D., Richardson, K., Crutzen,
& Singer, M.C. (2011). Overstretching attribution. Nature
P. & Foley, J. 2009. A safe operating space for humanity.
Climate Change, 1, 2–4.
Nature, 461, 472–475.
Patz, J. A. (2001). Public health risk assessment linked to
Roy, B. A., Güsewell, S., & Harte, J. (2004). Response of plant
climatic and ecological change. Human and Ecological Risk
pathogens and herbivores to a warming experiment. Ecology,
Assessment: An International Journal, 7(5), 1317–1327.
85(9), 2570–2581.
Patz, J. A., Campbell-Lendrum, D., Holloway, T., & Foley, J. A.
Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield,
(2005). Impact of regional climate change on human health.
J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson,
Nature, 438(7066), 310–317.
R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A.,
Pautasso, M., Döring, T. F., Garbelotto, M., Pellis, L., & Jeger, Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker,
M. J. (2012). Impacts of climate change on plant diseases – M., Wall, D.H., 2000. Biodiversity – global biodiversity
opinions and trends. European Journal of Plant Pathology, scenarios for the year 2100. Science 287, 1770–1774.
133(1), 295–313.
Salazar, L. F., Nobre, C. A., & Oyama, M. D. (2007). Climate
Pereira, H. M., Leadley, P. W., Proença, V., Alkemade, R., change consequences on the biome distribution in tropical
Scharlemann, J. P., Fernandez-Manjarrés, J. F., Araújo, M., South America. Geophysical Research Letters, 34(9).
Balvanera, P., Biggs, R., Cheung, W.,W., L., Chini, L., Cooper,
Santamouris, M. (Ed.). (2013). Energy and climate in the
H., D., Gilman, E., L., Guénette, S., Hurtt,G., Huntington,
urban built environment. Routledge.
H., Mace, G., Oberdorff, T., Revenga, C., Rodrigues, P.,
Scholes, R., Sumaila, U. & Walpole, M. (2010). Scenarios for Schiedek, D., Sundelin, B., Readman, J. W., & Macdonald,
global biodiversity in the 21st century. Science, 330(6010), R. W. (2007). Interactions between climate change and
1496–1501. contaminants. Marine Pollution Bulletin, 54(12), 1845–1856.
Plowright, R.K., Foley, P., Field, H.E., Dobson, A.P., Foley, Seinfeld, J. H., & Pandis, S. N. (2012). Atmospheric chemistry
J.E., Eby, P., & Daszak, P. 2011. Urban habituation, ecological and physics: from air pollution to climate change. John Wiley
connectivity and epidemic dampening: the emergence of & Sons.
Hendra virus from flying foxes (Pteropus spp.). Proceedings
Selwood KE, McGeoch MA, & Mac Nally R (2014) The effects
of the Royal Society B, 278, 3703–12
of climate change and land-use change on demographic rates
Price, M. F. (1998). Mountains: globally important ecosystems. and population viability. Biological Reviews; doi: 10.1111/
UNASYLVA-FAO-, 3–12. brv.12136
Pulliam, J.R.C., Epstein, J.H., Dushoff, J., Rahman, S.A., Siraj, A.S., Santos-Vega, M., Bouma, M.J., Yadeta, D.,
Bunning, M., Jamaluddin, A.A., Hyatt, A.D., Field, H.E., Carrascal, D.R. & Pascual, M. 2014. Altitudinal changes in
Dobson, A.P., Daszak, P.; Henipavirus Ecology Research malaria incidence in highlands of Ethiopia and Colombia.
Group (HERG). 2012. Agricultural intensification, priming Science, 343, 1154–1158.
for persistence and the emergence of Nipah virus: a lethal
Steffen, W., Grinevald, J., Crutzen, P. & McNeill, J. 2011.
bat-borne zoonosis. Journal of the Royal Society Interface, 9,
The Anthropocene: conceptual and historical perspectives.
89–101.
Philosophical Transactions of the Royal Society A, 369, 842–867.
Puppim de Oliveira, J.A., Balaban, O., Doll, C., Moreno-
Stott, R. 2006. Healthy response to climate change. BMJ, 332,
Penaranda, R., Gasparatos, A., Iossifova, C., Aki, S. 2010.
1385–1387.
Cities, Biodiversity and Governance: Perspectives and challenges
of the implementation of the convention on biological diversity at Syvitski, J.P.M., Kettner, A.J., Overeem, I., Hutton, E.W.H.,
the city level, Yokohama: United Nations University. Hannon, M.T., Brakenridge, G.R Day, J., Vörösmarty, C., Saito,
Y., Giosan, L., & Nicholls, R. (2009). Sinking deltas due to
Purse, B. V., Mellor, P. S., Rogers, D. J., Samuel, A. R.,
human activities. Nature Geoscience, 2, 681–686.
Mertens, P. P., & Baylis, M. (2005). Climate change and the
recent emergence of bluetongue in Europe. Nature Reviews Tamplin, M. L., Gauzens, A. L., Huq, A., Sack, D. A., & Colwell,
Microbiology, 3(2), 171–181. R. R. (1990). Attachment of Vibrio cholerae serogroup O1
to zooplankton and phytoplankton of Bangladesh waters.
Randolph, S.E. 2009. Perspectives on climate change impacts
Applied and Environmental Microbiology, 56(6), 1977–1980.
on infectious diseases. Ecology, 90, 927–931.
Templeton, A. R., Shaw, K., Routman, E., & Davis, S. K.
Raskin, P., Gallopin, G., Gutman, P., Hammond, A., Kates, R.
(1990). The genetic consequences of habitat fragmentation.
& Swart, R. 2002. Great Transition: The Promise and Lure of
Annals of the Missouri Botanical Garden, 13–27.
the Times Ahead, Boston: Stockholm Environment Institute.
Reid, H. (2015). Ecosystem-and community-based
adaptation: learning from community-based natural resource
management. Climate and Development, (ahead-of-print), 1–6.

Connecting Global Priorities: Biodiversity and Human Health 335

 Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Chapter 14
Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira,
M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Adger, W.N., J.M. Pulhin, J. Barnett, G.D. Dabelko, G.K.
Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Hovelsrud, M. Levy, Ú. Oswald Spring, and C.H. Vogel,
Peterson, A.T., Phillips, O.L., Williams, S.E., 2004. Extinction 2014: Human security. In: Climate Change 2014: Impacts,
risk from climate change. Nature 427, 145–148. Adaptation, and Vulnerability. Part A: Global and Sectoral
Aspects. Contribution of Working Group II to the Fifth Assessment
Tirado M.C. et al. (2010) Climate change and food safety: a Report of the Intergovernmental Panel on Climate Change [Field,
review. Food Research International 43: 1745 – 1765. C.B., V.R. Barros, D.J. Dokken, K.J. Mach, M.D. Mastrandrea,
Tucker, C. J., Wilson, J. M., Mahoney, R., Anyamba, A., T.E. Bilir, M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova,
Linthicum, K., & Myers, M. F. (2002). Climatic and ecological B. Girma, E.S. Kissel, A.N. Levy, S. MacCracken, P.R.
context of the 1994–1996 Ebola outbreaks. Photogrammetric Mastrandrea, and L.L. White (eds.)]. Cambridge University
engineering and remote sensing, 68(2), 147–152. Press, Cambridge, United Kingdom and New York, NY, USA.

Türkeş, M. (2014). Impacts of the Climate Change on Ahlsten, N., T. Giang, T. Hwang , K. Lam, H. Mathews, et
Agricultural Food Security, Traditional Knowledge and al. (2005). Protracted Refugee Situations: A Case Analysis of
Agroecology. Turkish Journal of Agriculture-Food Science and Kakuma Camp, Kenya. Conducted by the Princeton Refugee
Technology, 2(2). Initiative of the Woodrow Wilson School of Public and
International Affairs, Princeton University.
Vineis, P., Chan, Q. & Khan, A. (2011). Climate change
impacts on water salinity and health. Journal of Epidemiology Alliance Development Works (ADW), 2012. World Risk Report
and Global Health, 1, 5–10. 2012. ADW, Berlin, Germany.

Vörösmarty, C. J., Green, P., Salisbury, J., & Lammers, R. B. Alongi, D.M. 2008. Mangrove Forests: Resilience, Protection
(2000). Global water resources: vulnerability from climate from Tsunamis, and Responses to Global Climate Change.
change and population growth. Science, 289(5477), 284–288. Estuarine, Coastal and Shelf Science, 76: 1–13.

Welbergen, J., Klose S, Markus N & Eby, P. 2008. Climate ARC, 2014. REWARD Project Report Updates, January-April
change and the effects of temperature extremes on Australian 2014. American Refugee Committee.
flying-foxes. Proc. R. Soc. B 275, 419–425. Badola, R. and Hussain, S.A. 2005. Valuing ecosystem
World Commission on Environment and Development (ed.) functions: an empirical study on the storm protection
1987. Our Common Future, Oxford: Oxford University Press. function of Bhitarkanika mangrove ecosystem, India.
Environmental Conservation 32:1, 85–92
World Health Organization (WHO). World Health Assembly
resolution 61.19: climate change and health. Geneva: WHO. Barnett CP, 2003. Mozambican Refugees in Malawi:
2008. Available at: http://www.who.int/phe/news/wha/en/ Livelihoods and their Impact on the Natural Resource Base.
index.html. ITAD Ltd., West Sussex, UK. Published on-line, available at:
http://www.unhcr.org/4132e45c4.pdf (accessed 1 July 2014)
World Health Organization (WHO). (2012). Our Planet, Our
Health, Our Future. Human Health and the Rio Conventions. Barraclough, S.L. and Finger-Stich, A. 1996. Some Ecological
Discussion paper. Geneva: World Health Organization. and Social Implications of Commercial Shrimp Farming in Asia.
http://www.who.int/globalchange/publications/reports/ United Nations Research Institute for Social Development.
health_rioconventions.pdf. Accessed June 5, 2014. Available at: http://www.rrojasdatabank.org/shenv.htm#HD_
NM_23 (accessed 11 October 2013)
World Health Organization (WHO). (2005) Human health
impacts from climate variability and climate change in the Hindu BP, 2014. Fighting Nature with Nature. Bangkok Post, 12
Kush-Himalaya region. Report of an Inter-Regional Workshop. March 2014. Available at: http://www.raksthai.org/new/hot-
Mukteshwar: WHO Regional Office for South-East Asia. topic-detail.php?option=&task=&tr_id=181&cat=&lang=en
(accessed 13 July 2014)
World Health Organization (WHO) & UN-HABITAT 2010.
Hidden Cities: Unmasking and Overcoming Health Inequities in Bunch, M. J. (2011). Promoting health and well-being by
Urban Settings, Kobe, WHO Centre for Health Development managing for social–ecological resilience: the potential of
and UN Human Settlements Programme. integrating ecohealth and water resources management
approaches.
Wilson, M. E. (1991). [Infectious diseases in the era of the global
village]. Salud publica de Mexico, 34(3), 352–356. Cavaillé P, Dommanget, Daumergue N, Loucougaray G,
Spiegelberger T, Tabacchi E, Evette A, 2013. Biodiversity
assessment following a naturality gradient of riverbank
protection structures in French prealps rivers. Ecol
Engineering 53; 23–30
Cutter, S. L., Barnes, L., Berry, M., Burton, C., Evans,
E., Tate, E., & Webb, J. (2008). A place-based model for
understanding community resilience to natural disasters.
Global environmental change, 18(4), 598–606.

336 Connecting Global Priorities: Biodiversity and Human Health

Das, S. and Crépin, A-S. 2013. Mangroves can Provide Guha-Sapir D, D’aoust O, 2011. Demographic and health
Protection against Wind Damage during Storms. Estuarine, consequences of civil conflict: background paper. In: World
Coastal and Shelf Science, 134: 98–107. development report 2011: conflict, security, and development.
Washington, DC: World Bank.
Deoja B, Dhital M, Thapa B, Wagner A, 1991, Mountain Risk
Engineering Handbook, Part I & II, International Centre for Guha-Sapir D, Hoyois P, Below R., 2013. Annual Disaster
Integrated Mountain Development, Kathmandu, Nepal, 875 Statistical Review 2012: The Numbers and Trends. Brussels:
pp Centre for Research on the Epidemiology of Disasters
(CRED), Université catholique de Louvain, Brussels, Belgium.
Du, W., FitzGerald, G. J., Clark, M., & Hou, X. Y. 2010. Health
impacts of floods. Prehospital and Disaster Medicine, 25(03), Guha-Sapir D, Hoyois Ph., Below. R., 2014 Annual Disaster
265–272. Statistical Review 2013: The Numbers and Trends. Brussels.
CRED
Enright, J. and Kaewmahanin, J. 2012. Feasibility Study for
Climate Smart Mangrove Restoration Activities for Developing Hanson T, 2011. War and Biodiversity Conservation: The Role
Resilient Livelihoods to Reduce Climate Change Impacts. Report of Warfare Ecology. In: Warfare Ecology. NATO Science for
for Raks Thai Foundation, Thailand. Peace and Security Series C: Environmental Security 2011, pp
125–132.
Enright, J. and Nakornchai, P. 2014. Best Practices of Mangrove
Restoration in Adopting to Climate Change in Coastal Areas under Huxham M, Kumara MP, Jayatissa LP, Krauss KW, Kairo J,
BCRCC in Thailand. Building Coastal Resilience to Reduce Langat J, Mencuccini M, Skov MW, Kirui B, 2010. Intra- and
Climate Change Impact in Thailand and Indonesia (BCRCC) interspecific facilitation in mangroves may increase resilience to
Assessment Team. Mangrove Action Project. climate change threats. Phil Trans R Soc B, 365; 2127–2135.
Fattet M, Fu Y, Ghestem M, Ma W, Foulonneau M, Nespoulous Hyndman, J. 2009. Refugees, in Gregory, D. et al. (Eds.) The
J, Le Bissonnais Y, Stokes A, 2011. Effects of vegetation type Dictionary of Human Geography. 5th Edition, pp. 628–629.
on soil resistance to erosion: relationship between aggregate
Jambiya, G., S. Milledge, and N. Mtango. 2007. ‘Night time
stability and shear strength. Catena 87:60–69
spinach’: conservation and livelihood implications of wild meat use
Feagin, R.A., Mukherjee, N., Shanker, K., Baird, A.H., Cinner, in refugee situations in north-western Tanzania. TRAFFIC East/
J., Kerr, A.M., Koedam, N., Sridhar, A., Arthur, R., Jayatissa, Southern Africa, Dar es Salaam , Tanzania
L.P., Seen, D.L., Monon, M., Rodriguez, S., Shamsuddoha, M.
Jayakody, S., Jayasinghe, J.M.P.K. and Wijesundara, A. 2012.
and Dahdouh-Guebas, F. 2010. Shelter from the Storm? Use
Active vs. Passive Restoration of Mangroves: Developing
and Misuse of Coastal Vegetation Bioshields for Managing
Models for Sustainable Rejuvenation of Mangrove Ecosystems
Natural Disasters. Conservation Letters, 3: 1–11.
used for Shrimp Farming in North-Western Province of
Ghestem M, Sidle RC, and Stokes A, 2011. The Influence of Sri Lanka. In MFF, 2012. Sharing Lessons on Mangrove
Plant Root Systems on Subsurface Flow: Implications for Restoration. Proceedings and a Call for Action from an MFF
Slope Stability. BioScience 61(11); 869–879 Regional Colloquium. 30–31 August 2012, Mamallapuram,
India. pp. 179–188.
Gitau GC, 2011. The GIZ Dadaad household energy project:
Presentation during an improved cookstove colloquium Jayasurya, P.K. 2007. Global Warming: The Severe Threat to
at Nairobi Sarova Panaftic, 7th June 2011. GIZ (Deutsche Mangrove Ecosystems in Future. Science India, 37–41.
Gesellschaft für Internationale Zusammenarbeit (GIZ)
Kathiresan, K. 2008. Global Policies: Role of Institutions. UN
GmbH), Bonn, Germany.
Universities.
Giri, C., Zhu, Z., Tieszen, L.L., Singh, A., Gillette, S. &
Kathiresan, K. and Rajendran, N. 2005. Coastal Mangrove
Kelmelis, JA, 2008. Mangrove forest distributions and
Forests Mitigated Tsunami. Estuarine, Coastal and Shelf
dynamics (1975–2005) of the tsunami-affected region of
Science, 65: 601–606.Ke C, Feng Z, Wu X, Tu F, 2003.
Asia. Journal of Biogeography 35; 519–528
Design Principles and Engineering Samples of Applying Vetiver
Global Risks Perception Surveys 2013 and 2014, World Eco-engineering Technology for Steep Slope and River Bank
Economic Forum. Stabilisation. Paper presented at ICV3, Guangzhou, China,
October 2003.
Gonzalez, B. 2006. No, They’re not Magic, but Mushrooms
help Refugees in Rwanda. 13 June 2006. Available at: http:// Keim, M. E., 2008. Building human resilience: the role of
www.unhcr.org/448eb37f4.html (accessed 6 July 2014) public health preparedness and response as an adaptation
to climate change. American Journal of Preventive Medicine,
Gouzerh, A., Laize, A., Assangono, M., Wilson, M. and
35(5), 508–516.
Nespoulous, J. 2013. Ecological Engineering for Protecting
Against Shallow Landslides in China: Rehabilitation of a Kouadio, I. K., Aljunid, S., Kamigaki, T., Hammad, K., &
Mountain Slope in China’s Southeast. Ecological Engineering Oshitani, H., 2012. Infectious diseases following natural
Module, Training GEEFT 2012/2013. disasters: prevention and control measures
Green, W.G., 2008 Resistance and Resilience: Some Basic Leaning J, Guha-Sapir D, 2013. Natural Disasters, Armed
Postulates… Disaster Theory Series No. 4. Conflict, and Public Health. N Eng J Med 369(19); 1836–1842

Connecting Global Priorities: Biodiversity and Human Health 337

 Lyytinen, E., 2009. Household energy in refugee and IDPs Raks Thai, 2014. Adaptation for Secured Human Settlement
camps – challenges and solutions for UNHCR. New Issues in Bamboo Fences for Mangrove Restoration, Tambon Klong
Refugee Research, UNHCR, Geneva. Prasong, Amphur Muang, Krabi Province. Raks Thai
Foundation.
Mao, Z., Bourrier, F., Stokes, A. and Fourcaud, T. 2014. Three-
Dimensional Modelling of Slope Stability in Heterogeneous Reubens B, Poesen J, Danjon F, Geudens G, Muys B, 2007.
Montane Forest Ecosystems. Ecological Modelling, 273: 11–22. The role of fine and coarse roots in shallow slope stability and
soil erosion control with a focus on root system architecture:
MAP, 2012. Mangrove Action Project Annual Review 2012
a review. Trees 21(4); 385–402
McIvor, A., Spencer, T., Möller, I. and Spalding, M. 2012.
Sarnsamak, P. 2014. Krabi Villagers Build Bamboo Barriers
Storm Surge Reduction by Mangroves. Natural Coastal
to Protect the Coast. 4 March 2014. Available at: http://
Protection Series: Report 2. Cambridge Coastal Research Unit
www.nationmultimedia.com/national/Krabi-villagers-build-
Working Paper 41.
bamboo-barriers-to-protect-t-30228277.html (accessed 13
McIvor AL, Moller I, Spencer T, Spalding M, 2013. Mangroves July 2014)
as a sustainable coastal defence. Paper presented at the 7th
Sena, A., Corvalan, C., & Ebi, K., 2014. Climate Change,
International Conference on Asian and Pacific Coasts, Bali,
Extreme Weather and Climate Events, and Health Impacts.
Indonesia, September 2013. Available at: http://repository.
In: Freedman, B., Global Environmental Change: Handbook
unhas.ac.id/handle/123456789/7666
of Global Environmental Pollution Volume 1, pp 605–613,
Mercy Corps, 2014. Tapped Out: Water Scarcity and Refugee Springer.Shi, P. and Li, W. 1999. Rehabilitation of degraded
Pressures in Jordan. Mercy Corps, Portland, Oregon, USA. mountain ecosystems in southwestern China: An integrated
approach. Ambio, 28(5): 390–97.
Neria, Y., Nandi, A., & Galea, S. 2008. Post-traumatic stress
disorder following disasters: a systematic review. Psychological Smith, K.R., A. Woodward, D. Campbell-Lendrum, D.D.
Medicine, 38(04), 467–480. Chadee, Y. Honda, Q. Liu, J.M. Olwoch, B. Revich, and R.
Sauerborn, 2014: Human health: impacts, adaptation, and
Oucho, J.O. 2007. Environmental Impact of Refugees and
co-benefits. In: Climate Change 2014: Impacts, Adaptation, and
Internally Displaced Persons in Sub-Saharan Africa. Keynote
Vulnerability. Part A: Global and Sectoral Aspects. Contribution
Address to the African Migration Alliance Biennial Workshop on
of Working Group II to the Fifth Assessment Report of the
Climate Change, Environment and Migration, East London, South
Intergovernmental Panel on Climate Change [Field, C.B., V.R.
Africa, 15–16 November 2007 Available at: http://www2.
Barros, D.J. Dokken, K.J. Mach, M.D. Mastrandrea, T.E. Bilir,
warwick.ac.uk/fac/soc/crer/afrobrain/oucho/publications/
M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova, B. Girma,
environmental_impact_of_refugees_and_internally_di.pdf
E.S. Kissel, A.N. Levy, S. MacCracken, P.R. Mastrandrea, and
(accessed 1 July 2014)
L.L. White (eds.)]. Cambridge University Press, Cambridge,
PEDRR, 2013. PEDRR Input into Post-2015 Global United Kingdom and New York, NY, USA.
Framework on Disaster Risk Reduction. PEDRR Secretariat,
Stapleton J, (ed), 2014. Dispatches No. 353. Jesuit Refugee
Geneva. Published online, available at: http://www.unep.org/
Services International. Published on-line, available at: https://
disastersandconflicts/Portals/155/dnc/docs/GlobalPlatform/
en.jrs.net/newsletters_detail?ITN=MC-20140514083120
Framework.pdf (accessed 1 July 2014)
(accessed 1 July 2014).
Pohl M, Alig D, Körner C, Rixen C, 2009. Higher plant diversity
Stokes A, Spanos I, Norris JE, Cammeraat E (eds.), 2004.
enhances soil stability in disturbed alpine ecosystems. Plant
Eco- and Ground Bio-Engineering: The Use of Vegetation to
Soil 324:91–102
Improve Slope Stability, Proceedings of the First International
Post WM, Kwon, KC, 2000. Soil carbon sequestration and Conference on Eco-Engineering, 13–17 September 2004, Series:
land-use change: processes and potential. Global Change Developments in Plant and Soil Sciences, vol. 103, Springer
Biology, 6: 317–327. (2007) ISBN: 978–1-4020–5592–8
ProAct, 2008. The Role of Environmental Management and Stokes A, Norris JE, Greenwood J, 2008. Introduction to
Eco-engineering in Disaster Risk Reduction and Climate Change ecotechnological solutions. In: J.E. Norris, A. Stokes, S.B.
Adaptation. ProAct Network, Gland, Switzerland. Mickovski, L.H. Cammeraat, L.P.H. van Beek, B. Nicoll,
A. Achim (eds), 2008. Slope Stability and Erosion Control:
Promper C, Puissant A, Malet J-P, Glade T, 2014. Analysis of
Ecotechnological Solutions, Springer (2008), pp. 1–8.
land cover changes in the past and the future as contribution
to landslide risk scenarios. Applied Geography 53; 11–19 Stokes A, Atger C, Bengough AG, Fourcaud T, Sidle RC,
2009. Desirable plant root traits for protecting natural and
Quartel, S., Kroon, A., Augustinus, P.G.E.F., Van Santen, P.
engineered slopes against landslides. Plant Soil 324:1–30.
and Tri, N.H. 2007. Wave Attenuation in Coastal Mangroves
in the Red River Delta, Vietnam. Journal of Asian Earth Stokes A, Sotir RB, ChenW, GhestemM, 2010. Soil bio-
Sciences, 29: 576–584. and ecoengineering in China, past experience and present
priorities. Ecol Eng 36:247–257
Quarto, A. 2012. Ecological Mangrove Restoration (EMR):
Re-establishing a more Biodiverse and Resilient Coastal Stokes A, Douglas GB, Forcaud T, Giadrossich F, Gillies C,
Ecosystem with Community Participation. Mangrove Action Hubble T et al, 2014. Ecological mitigation of hillslope
Project. instability: ten key issues facing researchers and practitioners.
Plant Soil, 377:1–23.

338 Connecting Global Priorities: Biodiversity and Human Health

Sudmeier-Rieux, K. and Ash, N. (2009) Environmental Bongaarts, J. (2015, January). Global fertility and population
Guidance Note for Disaster Risk Reduction: Healthy Ecosystems trends. In Seminars in reproductive medicine (Vol. 33, No. 1,
for Human Security. IUCN, Gland, Switzerland. pp. 5–10).
Unite for Sight (UfS), 2013. Refugee Health – Module 7: Refugee Boserup, Ester. 1965. The Conditions of Agricultural Growth:
and Host Community Relationships. Unite for Sight. Published The Economics of Agrarian Change under Population
online, available at: http://www.uniteforsight.org/refugee- Pressure, Chicago: Aldine.
health/module7 (accessed 1 July 2014)
Bongaarts, J. (2013) Demographic trends and implications
United Nations High Commissioner for Refugees (UNHCR), for development, paper presented at the International Union
2002. A critical time for the environment. In: Refugees. for the Scientific Study of Population 2013 Meeting, Busan,
no.127, p 2 Republic of Korea, 26 to 31 August 2013. Downloaded from
http://iussp.org/ sites/default/files/event_call_for_papers/
UNHCR, 2014. United Nations High Commissioner for
Session_071_01_Bongaarts.pdf.
Refugees Website. Available at: http://www.unhcr.org/
cgi-bin/texis/vtx/home (accessed 1 July 2014) Bowen, K. J., Ebi, K., & Friel, S. (2014). Climate change
adaptation and mitigation: next steps for cross-sectoral action
United Nations International Strategy for Disaster reduction
to protect global health. Mitigation and Adaptation Strategies
(UNISDR), 2009: Global assessment report on disaster risk
for Global Change, 19(7), 1033–1040.
reduction. Geneva: UNISDR Secretariat.
Brown, L. R. (2004). Outgrowing the earth: The food
van Slobbe E, de Vriend HJ, Aarnikhof S, Lulofs K, de Vries
security challenge in an age of falling water tables and rising
M, Dircke P, 2013. Building with Nature: in search of resilient
temperatures. W. W. Norton & Company, Inc.
storm surge protection strategies. Natural Hazards 66(3);
1461–1480 Burkle, F. M. (2010). Future humanitarian crises: challenges
for practice, policy, and public health. Prehospital and disaster
Watson JT, Gayer M, Connoly MA. Epidemics after natural
medicine, 25(03), 191–199.
disasters. Emerg. Infect. Dis. 13, 11 (2007)
Campbell, A., Kapos, V., Scharlemann, J. P.W., Bubb, P.,
Weingärtner, L., 2005. The concept of food and nutrition
Chenery, A., Coad, L., Dickson, B., Doswald, N., Khan, M. S.
security. Achieving Food and Nutrition Security, 3, 21–52. In:
I., Kershaw, F. and Rashid, M. (2009). Review of the Literature
Klaus Klennert (ed) Achieving Food and Nutrition Security
on the Links between Biodiversity and Climate Change: Impacts,
Actions to Meet the Global Challenge A Training Course Reader.
Adaptation and Mitigation. Secretariat of the Convention on
InWEnt – Capacity Building International, Germany
Biological Diversity, Montreal. Technical Series No. 42, 124
Wisner B, Blaikie P, Cannon T, Davis I., 2008. At risk: natural pages.
hazards, people’s vulnerability and disasters (2nd ed.) Routledge,
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U.,
New York 275 pp
Perrings, C., Venail, P., et al. (2012). Biodiversity loss and its
World Bank, 2009. Convenient Solutions to an Inconvenient impact on humanity. Nature, 486 (7401), 59–67.
Truth: Ecosystem-Based Approaches to Climate Change. World
CBD (2014). Global Biodiversity Outlook, fourth edition,
Bank, Washington.
Secretariat for the Convention on Biological Diversity.
World Confederation for Physical Therapy (WCPT) (2014)
CBD (2013). The identification of scientific and technical
What is Disaster Management? World Confederation for
needs for the attainment of the targets under Strategic
Physical Therapy. Available at: http://www.wcpt.org/disaster-
Goal A of the Strategic Plan For Biodiversity 2011–2020.
management/what-is-disaster-management (accessed 30
Submitted to the 17th meeting of the SBSTTA, 30 August
June 2014).
2013. Document UNEP/CBD/SBSTTA/17/2/Add.1.

Chapter 15 Costello, A., Abbas, M., Allen, A., Ball, S., Bell, S., Bellamy, R.,
et al. (2009). Managing the health effects of climate change:
Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J. S., lancet and University College London Institute for Global
Nakashizuka, T., Raffaelli, D., and Schmid, B. (2006). Health Commission. The Lancet, 373(9676), 1693–1733.
Quantifying the evidence for biodiversity effects on ecosystem Das Gupta, M., Bongaarts, J., & Cleland, J. (2011). Population,
functioning and services. Ecology letters, 9(10), 1146–1156. Poverty, and Sustainable Development: A Review of the
Barnosky A.D., et al. (2012). Approaching a state shift in Evidence.
Earth’s biosphere. Nature, 486, 52–8. Ellis E.C., Ramankutty, N., (2008) Putting people in the
Bogardi, J. J., Dudgeon, D., Lawford, R., Flinkerbusch, E., map: anthropogenic biomes of the world. Front Ecol Environ
Meyn, A., Pahl-Wostl, C., Vielhauer, K., & Vörösmarty, 6:439–447.
C. (2012). Water security for a planet under pressure: Ezeh, A. C., Bongaarts, J., & Mberu, B. (2012). Global
interconnected challenges of a changing world call for population trends and policy options. The Lancet, 380(9837),
sustainable solutions. Current Opinion in Environmental 142–148.
Sustainability, 4(1), 35–43.

Connecting Global Priorities: Biodiversity and Human Health 339

 Flora, C. B. (2010). Food security in the context of energy McMichael, A. J. (2013). Globalization, climate change, and
and resource depletion: Sustainable agriculture in developing human health. New England Journal of Medicine, 368(14),
countries. Renewable agriculture and food systems, 25(02), 1335–1343.
118–128.
McMichael, A. J., & Butler, C. D. (2011). Promoting global
Flora, C. B. (2010). Food security in the context of energy population health while constraining the environmental
and resource depletion: Sustainable agriculture in developing footprint. Annual review of public health, 32, 179–197.
countries. Renewable agriculture and food systems, 25(02),
McMichael, T., Montgomery, H. and Costello, A. (2012).
118–128.
Health risks, present and future, from global climate change.
Freya A., Edwards-Jones, G., & Jones, J. P. (2011) British Medical Journal, 344, e1359-e1363.
Conservation and human behaviour: lessons from social
Millennium Ecosystem Assessment (MA). (2005). Ecosystems
psychology. Wildlife Research, 37(8), 658–667.
and human well-being: Synthesis. Washington, DC: Island
Fulton, E. A., Smith, A. D., Smith, D. C., & van Putten, I. E. Press.
(2011) Human behaviour: the key source of uncertainty in
Moon K and Cocklin C (2011) Participation in biodiversity
fisheries management. Fish and Fisheries, 12(1), 2–17.
conservation: Motivations and barriers of Australian
Gerland P, Raftery AE, Ševčíková H, Nan Li, Danan Gu, landholders. Journal of Rural Studies 27:331–342.
Spoorenberg T, Alkema L, Fosdick BK, Chunn J, Lalic N,
Neff, R. A., Parker, C. L., Kirschenmann, F. L., Tinch, J., &
Bay G, Buettner T, Heilig KK, and Wilmoth J. (2014) World
Lawrence, R. S. (2011). Peak oil, food systems, and public
population stabilization unlikely this century. Science:
health. American Journal of Public Health, 101(9), 1587.
234–237
Netto, G., Bhopal, R., Lederle, N., Khatoon, J., & Jackson,
Global Footprint Network, 2015. http://footprintnetwork.
A. (2010) How can health promotion interventions be
org/en/index.php/GFN/page/at_a_glance/
adapted for minority ethnic communities? Five principles
Godfray, H. C. J., Beddington, J. R., Crute, I. R., Haddad, L., for guiding the development of behavioural interventions.
Lawrence, D., Muir, J. F., et al. (2010). Food security: the Health Promotion International, daq012.
challenge of feeding 9 billion people. science, 327(5967),
Newson RS, Lion R, Crawford R, Curtis V, Elmadfa I, et al.
812–818.
(2013) Behaviour change for better health: nutrition, hygeine
Hirschman, C. (1994). Why fertility changes. Annual review and sustainability. BMC Public Health 13(Suppl 1): S1.
of sociology, 203–233.
Parmesan, C. (2008, October). Impacts of Climate Change
Horton, R. (2007). Righting the balance: energy for health. on Biodiversity and Human Health. In 2008 Joint Meeting of
The Lancet, 370(9591), 921–921. The Geological Society of America, Soil Science Society of America,
American Society of Agronomy, Crop Science Society of America,
IEA (2011). World Energy Outlook 2011. Available
Gulf Coast Association of Geological Societies with the Gulf Coast
from http://www.worldenergyoutlook.org/publications/
Section of SEPM.
weo-2011/
Parry M, Canziani, O., Palutikof, J., van der Linden, P.,
IEA (2012). World Energy Outlook 2012. Available
Hanson, C., eds. (2007). Contribution of Working Group II to
from http://www.worldenergyoutlook.org/publications/
the fourth assessment report of the Intergovernmental Panel
weo- 2012/
on Climate Change. Cambridge and New York, Cambridge
IEA (2013). World Energy Outlook 2013. Available University Press.
from http://www.worldenergyoutlook.org/publications/
PBL, 2010. Rethinking global biodiversity strategies. PBL
weo- 2013/
Netherlands Environmental Assessment Agency, Bilthoven/
Kok, M., Alkemende, R. et al. (2014). How sectors can The Hague, the Netherlands, 500197001.
contribute to the sustainable use and conservation of
Pereira HM, Leadley P et al. (2010) Scenarios for Global
biodiversity. CBD Technical Series 79. PBL/Netherlands
Biodiversity in the 21st Century, Science 330, 1496 (2010);
Environmental Assessment Agency and Secretariat,
Convention on Biological Diversity Peterson HB, Darmstadt GL, Bongaarts J (2013) Meeting
the unmet need for family planning: Now is the time. Lancet
Leadley, P.W., Krug, C.B., Alkemade, R., Pereira, H.M., Sumaila
381, 1696–1699
U.R., Walpole, M., Marques, A., Newbold, T., Teh, L.S.L, van
Kolck, J., Bellard, C., Januchowski-Hartley, S.R. and Mumby, Pollan M (2008) “Farmer in chief”. New Times, October
P.J. (2014): Progress towards the Aichi Biodiversity Targets: 9, 2008. http://www.nytimes.com/2008/10/12/
An Assessment of Biodiversity Trends, Policy Scenarios and magazine/12policy-t.html?pagewanted=all&_r=0
Key Actions. Secretariat of the Convention on Biological
Population and Environment, (2007), Volume 28 Number 4–5:
Diversity, Montreal, Canada. Technical Series 78, 500 pages.
Special Issue on Population and Conservation, May 2007.
Marmot, M., Friel, S., Bell, R., Houweling, T. A., & Taylor, S.
Pretty, J., O’Riordan, T., & Stoll-Kleemann, S. (2002) People,
(2008). Closing the gap in a generation: health equity through
livelihoods and collective action in biodiversity management,
action on the social determinants of health. The Lancet,
pp. 61–86. In O’Riordan, T., & Stoll-Kleemann, S. (Eds.)
372(9650), 1661–1669.
Biodiversity, sustainability and human communities: protecting
beyond the protected. Cambridge University Press.

340 Connecting Global Priorities: Biodiversity and Human Health

Robbins, P. (2011). Political ecology: A critical introduction Tukker, A., Bulavskaya, T., Giljum, S., de Koning, A., Lutter,
(Vol. 16). John Wiley & Sons. S., Simas, M., et al. (2014). The global resource footprint of
nations. Carbon, water, land and materials embodied in trade
Rockström, J., Steffen, W., Noone, K., Persson, Å., Chapin,
and final consumption calculated with EXIOBASE, 2, 8.
F. S., Lambin, E. F., et al. (2009). A safe operating space for
humanity. Nature, 461(7263), 472–475. UN Department of Economic and Social Affairs (UN
DESA) (2015) http://www.un.org/en/development/desa/
Royal Society of London (2009) Reaping the Benefits: Science
population/commission/pdf/48/DESA%20Fact%20Sheet_
and the Sustainable Intensification of Global Agriculture
Final.pdf
(Royal Society, London, 2009).
UNEP (2015a) Developing effective off-grid lighting policy:
Sachs, J. D. (2008) Common wealth: economics for a crowded
guidance note for governments in Africa. Available from:
planet. New York: Penguin Press.
http://www.enlighten-initiative.org/portals/0/documents/
Satterthwaite, D (2009) The implications of population Resources/publications/OFG-publication-may-BDef.pdf
growth and urbanization for climate change.
UNEP (2015b) Off Grid Country Lighting Assessments.
Environment & Urbanization, Vol 21(2): 545–567. DOI:
UNEP/GEF en.lighten initiative. Paris. Available from: http://
10.1177/0956247809344361.
map.enlighten-initiative.org/
Schusser, C. (2013). Who determines biodiversity? An
Viala, E. (2008). Water for food, water for life a comprehensive
analysis of actors’ power and interests in community forestry
assessment of water management in agriculture. Irrigation
in Namibia. Forest Policy and Economics, 36, 42–51.
and Drainage Systems, 22(1), 127–129.
Schwartz, B. S., Parker, C. L., Hess, J., & Frumkin, H. (2011).
Wackernagel, M. (1994). Ecological Footprint and
Public Health and Medicine in an Age of Energy Scarcity:
Appropriated Carrying Capacity: A Tool for Planning Toward
The Case of Petroleum. American Journal of Public Health,
Sustainability (PhD thesis). Vancouver, Canada: School of
101(9).
Community and Regional Planning. The University of British
Schwarzenbach, R. P., Escher, B. I., Fenner, K., Hofstetter, Columbia.
T. B., Johnson, C. A., Von Gunten, U., & Wehrli, B. (2006).
Waylen, Kerry A., Fischer, Anke, McGowan, Philip J.K.,
The challenge of micropollutants in aquatic systems. Science,
Thirgood, Simon, J.,& Milner-
313(5790), 1072–1077.
Wilkinson and Pickett (2009) The Spirit Level: Why More
Sen A (1999) Development as Freedom. Random House
Equal Societies Almost Always Do Better. Penguin.
Books
World Economic Forum (WEF), 2011. Water Security. The
Speidel, J. J., Weiss, D. C., Ethelston, S. A., & Gilbert, S. M.
water-food-energy-climate nexus. Island Press, Washington
(2007). Family planning and reproductive health: the link to
DC, Covelo, London.
environmental preservation. Population and Environment,
28(4–5), 247–258.
Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O., & Ludwig,
Chapter 16
C. (2015). The trajectory of the Anthropocene: The Great Allegrante, J. P. (2015). Policy and Environmental Approaches
Acceleration. The Anthropocene Review, 2053019614564785. in Health Promotion What Is the State of the Evidence?.
Health Education & Behavior, 42(1 suppl), 5S-7S.
The Earth Institute, Colombia University. (2006). “It’s 2025.
Where Do Most People Live?”, 7 November, 2006. Retrieved Alleyne, G., Binagwaho, A., Haines, A., Jahan, S., Nugent,
from http://www.earth.columbia.edu/news/2006/story07– R., Rojhani, A., & Stuckler, D. (2013). Embedding non-
11–06.php.html communicable diseases in the post-2015 development
agenda. The Lancet, 381(9866), 566–574.
The Lancet (2012), Volume 380, Issue 9837, Pages 75–186,
(14–20 July 2012). Barnosky A.D., et al. (2012). Approaching a state shift in
Earth’s biosphere. Nature, 486: 52–8.
The Lancet (2015) Protecting human health in the Anthropocene
era, Report of the Lancet Commission on Planetary Health. Barrett, C. B., Travis, A. J., & Dasgupta, P. (2011) On
Forthcoming. (TITLE TBC) biodiversity conservation and poverty traps. Proceedings of
the National Academy of Sciences, 108(34), 13907–13912.
Tilman, D., & Clark, M. (2014). Global diets link
environmental sustainability and human health. Nature, Beaglehole, R., Bonita, R., Horton, R., Adams, C., Alleyne,
515(7528), 518–522. G., Asaria, P., et al. (2011). Priority actions for the non-
communicable disease crisis. The Lancet, 377(9775),
Tilman, D., Balzer C., Hill, J. and B.L. Befort (2011)
1438–1447.
Global food demand and the sustainable intensification of
agriculture. Proc. Natl. Acad. Sci. 108: 20260–4. Biglan, A., Flay, B.R., Embry, D.D., & Sandler, I. (2012). The
Critical Role of Nurturing Environments for Promoting
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson,
Human Wellbeing. American Psychology 67(4): 257–271.
A., Howarth, R., Schindler, D., Schlesinger, W., Simberloff,
D., Swackhamer, D. & Swackhamer, D. (2001). Forecasting
agriculturally driven global environmental change. Science,
292(5515), 281–284.

Connecting Global Priorities: Biodiversity and Human Health 341

 Biodiversity Indicators Partnership (BIP). (2010). Biodiversity Costanza, R., Wilson, M. A., Troy, A., Voinov, A., Liu, S., &
indicators and the 2010 Target: Experiences and lessons D’Agostino, J. (2006). The value of New Jersey’s ecosystem
learnt from the 2010 Biodiversity Indicators Partnership. services and natural capital.
Secretariat of the Convention on Biological Diversity,
De Bourdeaudhuij, I., Van Cauwenberghe, E., Spittaels, H.,
Montréal, Canada. Technical Series No. 53, 196 pages.
Oppert, J. M., Rostami, C., Brug, J., et al. (2011). School.
Brauman, K. A., Daily, G. C., Duarte, T. K. E., & Mooney, based interventions promoting both physical activity and
H. A. (2007). The nature and value of ecosystem services: healthy eating in Europe: a systematic review within the
an overview highlighting hydrologic services. Annu. Rev. HOPE project. Obesity Reviews, 12(3), 205–216.
Environ. Resour., 32, 67–98.
Díaz, S., Demissew, S., Joly, C., Lonsdale, W. M., &
Bridgewater, P., Régnier, M, and Wang Zhen. (2012). Healthy Larigauderie, A. (2015a). A Rosetta Stone for nature’s benefits
Planet, Healthy People. A Guide to Human Health and to people. PLoS biology, 13(1).
Biodiversity. Montreal: Secretariat of the Convention on
Díaz, S., Demissew, S., Carabias, J., Joly, C., Lonsdale, M.,
Biological Diversity.
Ash, N., Larigauderie, A., Adhikari, J.R., Ariko, S., Baldi,
Brouwer, R., Brander, L., Kuik, O., Papyrakis, E., & Bateman, A. Bartuska, A., et al. (2015b). The IPBES Conceptual
I. (2013). A synthesis of approaches to assess and value Framework – connecting nature and people. Current Opinion
ecosystem services in the EU in the context of TEEB. VU in Environmental Sustainability, 14, 1–16.
University Amsterdam.
Dora, C., Haines, A., Balbus, J., Fletcher, E., Adair-Rohani, H.,
Butchart, S. H., Walpole, M., Collen, B., van Strien, A., Alabaster, G., Hossain, R., de Odnis, M. Branca, F. & Neira,
Scharlemann, J. P., Almond, R. E., et al. (2010). Global M. (2014). Indicators linking health and sustainability in the
biodiversity: indicators of recent declines. Science, 328(5982), post-2015 development agenda. The Lancet.
1164–1168.
Duraiappah, A.K., Asah, S.T., Brondizio, E.S., Kosoy, N.,
Campbell-Lendrum, D. (2005). How much does the health O’Farrell, P.J., Prieur-Richard, A-H., Subramanian, S.M., &
community care about global environmental change?. Global Tacheuchi, K. (2014). Managing the Mismatches to Provide
Environmental Change, 15(4), 296–298. Ecosystem Services for Human Well-being: A Conceptual
Framework for Understanding the New Commons. Current
Carlsson, G., & Nordström, A. (2012). Global engagement for
Opinion in Environmental Sustainability 7: 94–100.
health could achieve better results now and after 2015. The
Lancet, 380(9853), 1533–1534. French J., Blair-Stevens C., McVey, D., & Merritt, R. (2009).
Social marketing and public health: Theory and practice.
CBD (2014). Global Biodiversity Outlook, fourth edition,
Oxford University Press, USA.
Secretariat for the Convention on Biological Diversity.
Freudenberg, N., Franzosa, E., Chisholm, J., & Libman, K.
CBD (2013). Biodiversity and Sustainable Development
(2015). New Approaches for Moving Upstream How State
– The Relevance of the Strategic Plan for Biodiversity 2011–
and Local Health Departments Can Transform Practice to
2020 and the Aichi Biodiversity Targets for the Post-2015
Reduce Health Inequalities. Health Education & Behavior, 42(1
Development Agenda and the Sustainable Development
suppl), 46S-56S.
Goals. Submitted to the 17th meeting of the SBSTTA, 30
August 2013. Document UNEP/CBD/SBSTTA/17/INF/2. Freya A., Edwards-Jones, G., & Jones, J. P. (2010).
Conservation and human behaviour: lessons from social
CBD, Secretariat. (2013a). The identification of scientific
psychology. Wildlife Research, 37(8), 658–667.
and technical needs for the attainment of the targets under
Strategic Goal A of the Strategic Plan For Biodiversity 2011– Fulton, E. A., Smith, A. D., Smith, D. C., & van Putten, I. E.
2020. Submitted to the 17th meeting of the SBSTTA, 30 (2011). Human behaviour: the key source of uncertainty in
August 2013. Document UNEP/CBD/SBSTTA/17/2/Add.1. fisheries management. Fish and Fisheries, 12(1), 2–17.
CBD, Secretariat. (2013b). The Identification of Scientific and Gaventa, J., & Barrett, G. (2012). Mapping the outcomes of
Technical Needs for the Attainment of Targets 14 And 15 citizen engagement. World Development, 40(12), 2399–2410.
under Strategic Goal D of The Strategic Plan For Biodiversity
Gielen, Green L. W. (2015). The impact of policy,
2011–2020. Submitted to the 17th meeting of the SBSTTA,
environmental, and educational interventions: A synthesis
30 August 2013. Document UNEP/CBD/SBSTTA/17/Add.4.
of the evidence from two public health success stories. Health
Chivian, E. and Bernstein, A. (Eds.). (2008). Sustaining life: Education & Behavior, 42(Suppl. 1), 20S-34S.
How human health depends on biodiversity. New York: Oxford
Gimona, A., & van der Horst, D. (2007). Mapping hotspots
University Press.
of multiple landscape functions: a case study on farmland
Christie, M., Fazey, I., Cooper, R., Hyde, T., & Kenter, J. afforestation in Scotland. Landscape Ecology, 22(8),
O. (2012). An evaluation of monetary and non-monetary 1255–1264.
techniques for assessing the importance of biodiversity and
Glanz, K., & Bishop, D. B. (2010). The role of behavioral
ecosystem services to people in countries with developing
science theory in development and implementation of
economies. Ecological Economics, 83, 67–78.
public health interventions. Annual review of public health,
Corvalan, C., Hales, S., & McMichael, A. J. (2005). Ecosystems 31, 399–418.
and human well-being: health synthesis. World health
organization.

342 Connecting Global Priorities: Biodiversity and Human Health

Golden S. D., Earp J. A. (2012). Social ecological approaches Lewis, D., Bell, S. D., Fay, J., Bothi, K. L., Gatere, L., Kabila,
to individuals and their contexts: Twenty years of health M., et al. (2011). Community Markets for Conservation
education & behavior health promotion interventions. Health (COMACO) links biodiversity conservation with sustainable
Education & Behavior, 39, improvements in livelihoods and food production. Proceedings
of the National Academy of Sciences, 108(34), 13957–13962.
Gómez-Baggethun, E., & Muradian, R. (2015). In markets we
trust? Setting the boundaries of Market-Based Instruments Lieberman, L., Golden, S. D., & Earp, J. A. L. (2013). Structural
in ecosystem services governance. Ecological Economics. Approaches to Health Promotion What Do We Need to Know
About Policy and Environmental Change? Health Education &
Gómez-Baggethun, E., Martín-López, B., Barton, D., Braat,
Behavior, 40(5), 520–525.
L., Kelemen, E., García-Llorente, M., et al. (2014). State-of-
the-art report on integrated valuation of ecosystem services. Lomazzi, M., Borisch, B., & Laaser, U. (2014). The Millennium
European Commission, EU FP7 OpenNESS Project Deliverable, 4. Development Goals: experiences, achievements and what’s
next. Global health action, 7.
Haines, A., Alleyne, G., Kickbusch, I., & Dora, C. (2012).
From the Earth Summit to Rio+ 20: integration of health Lucas, P. L., Kok, M. T., Nilsson, M., & Alkemade, R. (2013).
and sustainable development. The Lancet, 379(9832), Integrating Biodiversity and Ecosystem Services in the Post-
2189–2197. 2015 Development Agenda: Goal Structure, Target Areas and
Means of Implementation. Sustainability, 6(1), 193–216.
Hargreaves, T. (2011). Practice-ing behaviour change:
Applying social practice theory to pro-environmental Marmot, M., Friel, S., Bell, R., Houweling, T. A., & Taylor, S.
behaviour change.” Journal of Consumer Culture 11.1: 79–99. (2008). Closing the gap in a generation: health equity through
action on the social determinants of health. The Lancet,
Horwitz, P., Morrison, K., Parkes, M., Patz, J., Zinsstag, J.
372(9650), 1661–1669.
(2012). Integrating health, sustainability and ecosystems
in the post-2015 Development Agenda. Think Piece for MacDonald, K. I., & Corson, C. (2012). ‘TEEB Begins Now’:
Health in the Post-2015 Development Agenda.http://www. a virtual moment in the production of Natural Capital.
worldwewant2015.org/health. Accessed June 5, 2014. Development and Change, 43(1), 159–184.
Kelemen, E., García-Llorente, M., Pataki, G., Martín-López, B., McKenzie-Mohr D., Schultz P.W., Kotler P. & Lee N.R. (2011)
& Gómez-Baggethun, E. (2014). Non-monetary techniques Social marketing to protect the environment: What works. Sage
for the valuation of ecosystem services. In OpenNESS Publications, Incorporated.
Reference Book. EC FP7 Grant Agreement No. 308428.
McMichael, A. J. (2013). Globalization, climate change, and
Khun, S., & Manderson, L. (2007). Community and school- human health. New England Journal of Medicine, 368(14),
based health education for dengue control in rural Cambodia: 1335–1343.
a process evaluation. PLoS neglected tropical diseases 1(3), e143.
Moon, K., and Cocklin, C. (2011). Participation in biodiversity
Kickbusch, I., Brindley, C. (2013). Health in the Post-2015 conservation: Motivations and barriers of Australian
Development Agenda. An Analysis of the UN-led thematic landholders. Journal of Rural Studies 27:331–342.
consultations, High-Level Panel report and sustainable
Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A.
development debate in the context of health. Geneva: World
D., Michaud, C., et al. (2012). Disability-adjusted life years
Health Organization.
(DALYs) for 291 diseases and injuries in 21 regions, 1990–
Lee, N. R., & Kotler, P. (2011). Social marketing: Influencing 2010: a systematic analysis for the Global Burden of Disease
behaviors for good. Sage. Study 2010. The Lancet, 380(9859), 2197–2223.
Kuhnlein, H. V., Erasmus, B., Spigelski, D., & Burlingame, Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford,
B. (2013). Indigenous peoples’ food systems and well-being: K. H., Ricketts, T. H., et al. (2013). Human health impacts of
interventions and policies for healthy communities. Food and ecosystem alteration. Proceedings of the National Academy of
Agriculture Organization of the United Nations (FAO). Sciences, 110(47), 18753–18760.
Langlois E.V., Campbell, K., Prieur-Richard, A.H, Karesh, Nelson, E., Mendoza, G., Regetz, J., Polasky, S., Tallis, H.,
W.B., Daszak, P. (2012). Towards a better integration of global Cameron, D., et al. (2009). Modeling multiple ecosystem
health and biodiversity in the new sustainable development services, biodiversity conservation, commodity production,
goals beyond Rio +20. EcoHealth. 2012;9(4):381–385. doi: and tradeoffs at landscape scales. Frontiers in Ecology and the
10.1007/s10393–012–0800–8. Environment, 7(1), 4–11.
Leadley, P.W., Krug, C.B., Alkemade, R., Pereira, H.M., Sumaila Netto, G., Bhopal, R., Lederle, N., Khatoon, J., & Jackson,
U.R., Walpole, M., Marques, A., Newbold, T., Teh, L.S.L, van A. (2010). How can health promotion interventions be
Kolck, J., Bellard, C., Januchowski-Hartley, S.R. and Mumby, adapted for minority ethnic communities? Five principles
P.J. (2014): Progress towards the Aichi Biodiversity Targets: for guiding the development of behavioural interventions.
An Assessment of Biodiversity Trends, Policy Scenarios and Health Promotion International, daq012.
Key Actions. Secretariat of the Convention on Biological
Newson, R. S., Lion, R., Crawford, R., Curtis, V., Elmadfa, I.,
Diversity, Montreal, Canada. Technical Series 78, 500 pages.
et al. (2013). Behaviour change for better health: nutrition,
hygeine and sustainability. BMC Public Health 13(Suppl 1): S1.

Connecting Global Priorities: Biodiversity and Human Health 343

 Nunes, P. A., & van den Bergh, J. C. (2001). Economic Shin A., Surkan P. J., Coutinho A., Suratkar S. R., Campbell
valuation of biodiversity: sense or nonsense?. Ecological R. K., Rowan M., et al. (2015). Impact of Baltimore Healthy
economics, 39(2), 203–222. Eating Zones: An environmental intervention to improve diet
among African American youth. Health Education & Behavior,
Open Working Group (OWG). (2013). “TST Issues Brief:
42 (Suppl. 1), 97S-105S.
Biodiversity”. Technical Support Team Issues Briefs,
Available at: http://sustainabledevelopment.un.org/index. Smith, J., & Taylor, E. M. (2013). MDGs and NTDs: Reshaping
php?menu=1528 the Global Health Agenda. PLoS neglected tropical diseases, 7(12).
Panel, UN High Level. (2013). A new global partnership: Sunderlin, W. D. (2006). Poverty alleviation through
Eradicate poverty and transform economies through community forestry in Cambodia, Laos, and Vietnam: An
sustainable development. Final Report of the UN High-Level assessment of the potential. Forest Policy and Economics,
Panel of Eminent Persons on the Post-2015 Development 8(4), 386–396.
Agenda, 30.
Talbot, L., & Verrinder, G. (2009). Promoting health: the
Panter-Brick, C., Clarke, S. E., Lomas, H., Pinder, M., & primary health care approach. Elsevier Australia.
Lindsay, S. W. (2006). Culturally compelling strategies for
The Economics of Ecosystems and Biodiversity. (2010).
behaviour change: a social ecology model and case study
Mainstreaming the Economics of Nature: A Synthesis of
in malaria prevention. Social science & medicine, 62(11),
the Approach, Conclusions and Recommendations of TEEB.
2810–2825.
Malta: Progress Press.
PBL. (2010). Rethinking global biodiversity strategies. PBL
Trickett, E. J., Beehler, S., Deutsch, C., Green, L. W., Hawe,
Netherlands Environmental Assessment Agency, Bilthoven/
P., McLeroy, K., et al. (2011). Advancing the science of
The Hague, the Netherlands, 500197001.
community-level interventions. American journal of public
PEDRR, (2013). PEDRR Input into Post-2015 Global health, 101(8), 1410–1419.
Framework on Disaster Risk Reduction. PEDRR Secretariat,
United Nations Development Group (UNDG). (2013).
Geneva. Published online, available at: http://www.unep.org/
The global conversation begins: Emerging views for a New
disastersandconflicts/Portals/155/dnc/docs/GlobalPlatform/
Development Agenda. 20 March 2013. Retrieved from:
Framework.pdf
http://www.undp.org/content/undp/en/home/librarypage/
Pelletier, N., Maas, R., Goralczyk, M., & Wolf, M. A. mdg/global-conversation-begins/
(2014). Conceptual basis for development of the European
United Nations, (2012). Rio+20 The future we want: outcome
Sustainability Footprint. Environmental Development, 9,
document adopted at Rio+20. Available from http://www.
12–23.
un.org/en/Sustainablefuture
Pons-Vigués, M., Diez, È., Morrison, J., Salas-Nicás, S.,
Vaughan P.W., Encalada H. R. R., Torres S. C., & Campos,
Hoffmann, R., Burstrom, et al. (2014). Social and health
B. (2013). Impact of the “My Community” Communications
policies or interventions to tackle health inequalities in
Intervention in Loja Province Ecuador on Changing
European cities: a scoping review. BMC public health, 14(1),
Human Behaviors related to Surface Water Contamination.
198.
Conservation Evidence, 10: 53–56.
Pretty, J., O’Riordan, T., & Stoll-Kleemann, S. (2002). People,
Verissimo, D. (2013). Influencing human behaviour: an
livelihoods and collective action in biodiversity management,
underutilised tool for biodiversity management. Conservation
pp. 61–86. In O’Riordan, T., & Stoll-Kleemann, S. (Eds.)
Evidence, 29–31.
Biodiversity, sustainability and human communities: protecting
beyond the protected. Cambridge University Press. Wakefield, M.A., Loken, B., and Hornick, R. C. (2010). Use
of mass media campaigns to change health behaviour. Lancet
Raks, T. (2014). Adaptation for Secured Human Settlement
376:1261–71.
Bamboo Fences for Mangrove Restoration, Tambon Klong
Prasong, Amphur Muang, Krabi Province. Raks Thai Waylen, K. A., Fischer, A., McGowan, P. J. K., Thirgood, S.
Foundation. J., & Milner-Gulland, E. J. (2010). The effect of local cultural
context on community-based conservation interventions:
Romanelli, C., Corvalan, C., Cooper, H. D., Manga, L., Maiero,
evaluating ecological, economic, attitudinal and behavioural
M., & Campbell-Lendrum, D. (2014b). From Manaus to
outcomes. CEE review 09–019 (SR80). Collaboration for
Maputo: Toward a Public Health and Biodiversity Framework.
Environmental Evidence: www.environmentalevidence.org/
EcoHealth, 11(3), 292–299.
SR80.html
Sachs, J. D. (2012). From millennium development goals
WHO. (2012). Our Planet, Our Health, Our Future.
to sustainable development goals. The Lancet, 379(9832),
Human Health and the Rio Conventions. Discussion paper.
2206–2211.
Geneva: World Health Organization. http://www.who.int/
Sandifer, P. A., Sutton-Grier, A. E., & Ward, B. P. (2015). globalchange/publications/reports/health_rioconventions.pdf.
Exploring connections among nature, biodiversity, ecosystem
WHO. (2008). Report to the WHO Commission on Social
services, and human health and well-being: Opportunities
Determinants of Health from the Knowledge Network on
to enhance health and biodiversity conservation. Ecosystem
Urban Settings: Our cities, our health, our future: Acting
Services, 12, 1–15.
on social determinants of health equity in urban settings.
Kobe, Japan: World Health Organization Centre for Health
Development.

344 Connecting Global Priorities: Biodiversity and Human Health

Secretariat of the Convention on Biological Diversity Department of Public Health, Environmental
World Trade Centre and Social Determinants of Health (PHE)
413 St. Jacques Street, Suite 800 World Health Organization (WHO)
Montreal, Quebec, Canada H2Y 1N9 Avenue Appia 20 – CH-1211 Geneva 27 – Switzerland
Phone: 1 (514) 288 2220 www.who.int/phe/en/
Fax: 1 (514) 288 6588 ISBN 978 92 4 150853 7
E-mail: secretariat@cbd.int
Website: http://www.cbd.int