Elke Jurandy Bran Nogueira Cardoso

José Leonardo de Moraes Gonçalves

Fabiano de Carvalho Balieiro
Avílio Antônio Franco Editors

Mixed Plantations
of Eucalyptus and
Leguminous Trees
Soil, Microbiology and Ecosystem
Services
Mixed Plantations of Eucalyptus and Leguminous
Trees
Elke Jurandy Bran Nogueira Cardoso
José Leonardo de Moraes Gonçalves
Fabiano de Carvalho Balieiro
Avílio Antônio Franco
Editors

Mixed Plantations
of Eucalyptus
and Leguminous Trees
Soil, Microbiology and Ecosystem Services
Editors
Elke Jurandy Bran Nogueira Cardoso José Leonardo de Moraes Gonçalves
Department of Soil Science Department of Forest Science
University of São Paulo University of São Paulo
“Luiz de Queiroz” College of Agriculture “Luiz de Queiroz” College of Agriculture
Piracicaba, SP, Brazil Piracicaba, SP, Brazil

Fabiano de Carvalho Balieiro Avílio Antônio Franco

EMBRAPA Soils EMBRAPA Agrobiology
Brazilian Agricultural Research Corporation (Retired Researcher)
Rio de Janeiro, RJ, Brazil Brazilian Agricultural Research Corporation
Seropédica, RJ, Brazil

ISBN 978-3-030-32364-6    ISBN 978-3-030-32365-3 (eBook)

https://doi.org/10.1007/978-3-030-32365-3

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Preface

Mixed Plantations of Eucalyptus and Acacia mangium

We indicate this book to foresters, entrepreneurs in forestry, producers of wood,

cellulose or other forest sub-products, agricultural engineers, agronomists, biolo-
gists, people working in Environmental Conservation and Natural Life Preservation,
as well as the graduate and post-graduate students in these areas and socio-­economic
planners.
Here, we present a compilation as complete as possible on research, themes
regarding eucalypt plantations, especially when in consortia with leguminous tropi-
cal trees. Such mixed stands generally can be productive and economically viable
and are ecologically sustainable and favorable for the social-economic guarantees
of rural workers and entrepreneurs. Eucalypt is one of the most cultivated forest
trees in Brazil. However, most of the time, it is produced as monoculture and needs
continuous fertilizer applications, including nitrogenous compounds, to maintain
productivity. These plantations, usually propagated by vegetative means, as clones,
receive criticism from various sectors of society for their low genetic diversity.
Among forest producers, the main concern is the high susceptibility of homoge-
neous stands to abiotic and biotic stress. In consequence, during the last decades,
several research teams all over the tropical countries have been investigating changes
in the eucalypt management system to provide a more attractive and sustainable
activity, achieving economic gains and diminishing its environmental impacts. Our
proposal is mostly restricted to the Brazilian research experience on this topic, with
special consideration of the need to diminish the use of industrial products as
­fertilizers and pesticides, but valuating soil health, biological gains, and ecosystem
services.
Considering those prerequisites, it becomes easy to answer the main question of
the first chapter: “Why mixed forest plantations?” Our response is as follows:
“Because, when comparing all investigated management systems, this one is socially
more advantageous and benefitting the rural entrepreneur economically, besides its
high sustainability.”

v
vi Preface

Considering some of these advantages, we want to present the main line of

thought of the sequence of the book chapters. Thus, regarding growth and produc-
tivity of the trees, the most outstanding combination is Eucalypt in consortium with
Acacia mangium, an exotic species, already known for its expressive productivity.
Although, in biology, one always gets some variation, the best responses occur with
mixed ­plantations in deep and sandy soils of low fertility, with a hot and rainy cli-
mate, which corresponds to most of the Brazilian regions used for eucalypt
production.
The main reason for these superior results is that most legumes present a natural
association with soil bacteria, generically known as rhizobia, which nodulate the
roots of these trees and have a high potential of fixing atmospheric nitrogen, trans-
forming it into ammonia in the root nodules. The forthcoming fixed nitrogenous
compounds cycle throughout the whole tree and generally are exported and divided
with other plants in their neighborhood. During litterfall, some of the fixed N
reaches the soil causing its enrichement in N. The symbiotically fixed N can supply
nitrogen needs of all plants, at the same time retaining nutrient reserves for the next
tree rotation. Thus, the enriched soil in C and N turns the nutrient cycling much
more dynamic.
Chapters 5–10 are all dedicated to discussing biological aspects of this kind of
management, providing us with a constant increase in knowledge on the most
­adequate strategies to be applied to better soil health and plant growth. The perfect
functioning of the soil as producer correlates directly with the size and diversity of
the soil bacterial community structure, with each plant recruiting in its rhizosphere
the most helpful bacteria, with functions of mineralizing the soil organic matter,
acting on enzymes related to plant nutrition and on biological control of pathogens,
among others. Right thereafter, we present the processes inherent to biological N
fixation (BNF), selection of the most adequate rhizobial strains, and the transfer
from soil to plant or from plant to plant mediated by mycorrhizal fungi, having a
synergic interaction with BNF. Mycorrhizal fungi transport all kinds of nutrients to
plants but are more active regarding the ones with slow mobility in soil, as phospho-
rus (P). Here, it is important to highlight another trait of Eucalyptus and Acacia:
both host plants form symbioses with both kinds of mycorrhiza, the arbuscular
(AM) and the ectomycorrhiza (ECM), which is exceptional among plants, that nor-
mally associate only with one kind of mycorrhiza, if at all.
Following the chapters, we now come to the important contribution of insects
and other soil invertebrates to soil health, nutrient cycling and organic matter
decomposition, showing how they influence the plants and how they become
affected, in numbers and diversity, besides the influence of the climate. Right
­afterwards, there follows a chapter on bio-indicators of soil health, showing many
recent results on the extreme relevance of the microbiological phenomena and the
innumerable ecosystem services derived from the ecologically correct management,
with benefits to soil, plants, and workers, still contributing to economic gains.
Chapter 11 discusses the problems that may derive from the introduction of
exotic possible biological species into any ecosystem different from its origin,
which resides in its invasiveness, sometimes causing severe ecological and
Preface vii

e­ conomic problems, a phenomenon that has been occurring regarding specimens of

plants and animals of most categories. Although most of our researchers did not
perceive such behavior regarding A. mangium, we feel ethically compromised to
tell what a few other researchers have reported, and it is always worthwhile to use
prevention and caution in such situations. Generally, however, our experience says
that the danger of this species becoming invasive should be neglected, when being
used adequately. We belief that invasiveness may only occur in open lands and not
when used in forests.
Chapter 12 presents the use of Brazilian leguminous trees to substitute A. man-
gium. So far, the best choice has always been this species (A. mangium), and it is the
only one about which we have already compiled a great amount of experimental
reports and practical experience, as well in Brazil as in many other countries. The
approval of employing this species was almost unanimous by all researchers or
farmers who had the opportunity of following its performance in the field, and for
many decades.
Nevertheless, nothing impedes to test other species, as, for example, the national
leguminous trees, which are available in great numbers. Maybe in the future, we can
select some of them, which present the same advantages or are even better in such a
consortium, as indicated by the author of this chapter, one of the very few scientists
who worked in this area.
Finally, all this information is complemented by the last chapter, which describes
the Brazilian legal structure and presents the regulations for the exploration of
­forests, either Eucalypt plantations in monoculture or in consortia, which we hope,
will help the interested people to make the best choices on this activity.

Piracicaba, SP, Brazil  Elke Jurandy Bran Nogueira Cardoso

Piracicaba, SP, Brazil   José Leonardo de Moraes Gonçalves
Rio de Janeiro, RJ, Brazil   Fabiano de Carvalho Balieiro
Seropédica, RJ, Brazil   Avílio Antônio Franco
Contents

1 Why Mixed Forest Plantation? ��������������������������������������������������������������    1

Ranieri Ribeiro Paula, Ivanka Rosado de Oliveira,
José Leonardo de Moraes Gonçalves,
and Alexandre de Vicente Ferraz
2 Growth Patterns at Different Sites and Forest
Management Systems������������������������������������������������������������������������������   15
Carolina Braga Brandani, Felipe Martini Santos,
Ivanka Rosado de Oliveira, Bruno Bordon, Maurel Bheling,
Eduardo Vinicius Silva, and José Leonardo de Moraes Gonçalves
3 Nutrient Cycling in Mixed-Forest Plantations��������������������������������������   45
José Henrique Tertulino Rocha,
José Leonardo de Moraes Gonçalves,
and Alexandre de Vicente Ferraz
4 Litter Decomposition and Soil Carbon Stocks in Mixed
Plantations of Eucalyptus spp. and Nitrogen-Fixing Trees������������������   57
Fabiano de Carvalho Balieiro, Fernando Vieira Cesário,
and Felipe Martini Santos
5 Soil Bacterial Structure and Composition in Pure and Mixed
Plantations of Eucalyptus spp. and Leguminous Trees������������������������   91
Caio Tavora Coelho da Costa Rachid
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations ������ 103
Sergio Miana de Faria, Fabiano de Carvalho Balieiro,
Ranieri Ribeiro Paula, Felipe Martini Santos, and Jerri Edson Zilli

ix
x Contents

7 Mycorrhiza in Mixed Plantations���������������������������������������������������������� 137

Maiele Cintra Santana, Arthur Prudêncio de Araujo Pereira,
Bruna Andréia de Bacco Lopes, Agnès Robin,
Antonio Marcos Miranda Silva,
and Elke Jurandy Bran Nogueira Cardoso
8 Mesofauna and Macrofauna in Soil and Litter
of Mixed Plantations�������������������������������������������������������������������������������� 155
Maurício Rumenos Guidetti Zagatto,
Luís Carlos Iuñes Oliveira Filho, Pâmela Niederauer Pompeo,
Cintia Carla Niva, Dilmar Baretta,
and Elke Jurandy Bran Nogueira Cardoso
9 Bioindicators of Soil Quality in Mixed Plantations
of Eucalyptus and Leguminous Trees ���������������������������������������������������� 173
Arthur Prudêncio de Araujo Pereira, Daniel Bini,
Emanuela Gama Rodrigues, Maiele Cintra Santana,
and Elke Jurandy Bran Nogueira Cardoso
10 Ecosystem Services in Eucalyptus Planted Forests
and Mixed and Multifunctional Planted Forests���������������������������������� 193
Fabiano de Carvalho Balieiro, Luiz Fernando Duarte de Moraes,
Rachel Bardy Prado, Ciro José Ribeiro de Moura,
Felipe Martini Santos, and Arthur Prudêncio de Araujo Pereira
11 The Risk of Invasions When Using Acacia spp. in Forestry���������������� 221
Ciro José Ribeiro de Moura, Nina Attias,
and Helena de Godoy Bergallo
12 Multifunctional Mixed-Forest Plantations:
The Use of Brazilian Native Leguminous Tree Species
for Sustainable Rural Development ������������������������������������������������������ 241
Antonio Carlos Gama-Rodrigues
13 The Brazilian Legal Framework on Mixed-­Planted Forests��������������� 257
Luiz Fernando Duarte de Moraes, Renata Evangelista de Oliveira,
Maria Jose Brito Zakia, and Helena Carrascosa Von Glehn

Index������������������������������������������������������������������������������������������������������������������ 271
Contributors

Nina Attias Department of Animal Biology, Federal University of Mato Grosso do

Sul, Campo Grande, MS, Brazil
Dilmar Baretta Santa Catarina State University, Chapecó, SC, Brazil
Maurel Bheling Embrapa Agrosilvopastoral, Brazilian Agricultural Research
Corporation, Sinop, MT, Brazil
Daniel Bini State University of the Central West, Guarapuava, PR, Brazil
Bruno Bordon Department of Forest Sciences, University of São Paulo, “Luiz de
Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Elke Jurandy Bran Nogueira Cardoso Department of Soil Science, University of
São Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Carolina Braga Brandani College of Agricultural, Consumer and Environmental
Sciences - Animal and Range Sciences, New Mexico State University, Las Cruces,
NM, USA
Fernando Vieira Cesário Fluminense Federal University, Niterói, RJ, Brazil
Caio Tavora Coelho da Costa Rachid Institute of Microbiology, Federal
University of Rio de Janeiro, Ilha do Fundão, RJ, Brazil
Arthur Prudêncio de Araujo Pereira Department of Soil Science, University of
São Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Soil Science Department (Pici Campus), Federal University of Ceará, Fortaleza,
Ceará, Brazil
Bruna Andréia de Bacco Lopes Department of Soil Science, University of São
Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Fabiano de Carvalho Balieiro EMBRAPA Soils, Brazilian Agricultural Research
Corporation, Rio de Janeiro, RJ, Brazil

xi
xii Contributors

Sergio Miana de Faria EMBRAPA Agrobiology, Brazilian Agricultural Research

Corporation, Seropédica, RJ, Brazil
Helena de Godoy Bergallo Department of Ecology, Institute of Biology Roberto
Alcântara Gomes, Rio de Janeiro State University, Rio de Janeiro, RJ, Brazil
José Leonardo de Moraes Gonçalves Department of Forest Sciences, University
of São Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Luiz Fernando Duarte de Moraes EMBRAPA Agrobiology, Brazilian
Agricultural Research Corporation, Seropédica, RJ, Brazil
Ciro José Ribeiro de Moura Federal University of Rio de Janeiro, Rio de Janeiro,
RJ, Brazil
Ivanka Rosado de Oliveira Department of Forest Sciences, University of São
Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Renata Evangelista de Oliveira Department of Rural Development, Federal
University of São Carlos, Araras, SP, Brazil
Alexandre de Vicente Ferraz Institute of Forest Science and Research (IPEF),
Piracicaba, SP, Brazil
Avílio Antônio Franco EMBRAPA Agrobiology (Retired Researcher), Brazilian
Agricultural Research Corporation, Seropédica, RJ, Brazil
Antonio Carlos Gama-Rodrigues Darcy Ribeiro State University of Norte
Fluminense, Campos dos Goytacazes, RJ, Brazil
Cintia Carla Niva Embrapa Cerrados, Brazilian Agricultural Research
Corporation, Planaltina, DF, Brazil
Luís Carlos Iuñes Oliveira Filho Santa Catarina State University, Chapecó, SC,
Brazil
Ranieri Ribeiro Paula Center for Agricultural Sciences and Engineering, Federal
University of Espirito Santo, Alegre, ES, Brazil
Pâmela Niederauer Pompeo Santa Catarina State University, Chapecó, SC, Brazil
Rachel Bardy Prado EMBRAPA Soils, Brazilian Agricultural Research
Corporation, Rio de Janeiro, RJ, Brazil
Agnès Robin Department of Soil Science, University of São Paulo, “Luiz de
Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Eco & Sols, Univ. Montpellier, CIRAD, INRA, IRD, Montpellier SupAgro,
Montpellier, France
José Henrique Tertulino Rocha Agriculture and Forest Engineering College
(FAEF), Garça, SP, Brazil
Contributors xiii

Emanuela Gama Rodrigues North Fluminense State University, Campos dos

Goytacazes, RJ, Brazil
Maiele Cintra Santana Department of Soil Science, University of São Paulo,
“Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Felipe Martini Santos Federal Rural University of Rio de Janeiro, Seropédica, RJ,
Brazil
Antonio Marcos Miranda Silva Department of Soil Science, University of São
Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Eduardo Vinicius Silva Federal Rural University of Rio de Janeiro, Seropédica,
RJ, Brazil
Helena Carrascosa Von Glehn São Paulo Environmental System, São Paulo, SP,
Brazil
Maurício Rumenos Guidetti Zagatto Department of Soil Science, University of
São Paulo, “Luiz de Queiroz” College of Agriculture, Piracicaba, SP, Brazil
Maria Jose Brito Zakia Department of Forest Sciences, São Paulo State
University, Botucatu, SP, Brazil
Jerri Edson Zilli EMBRAPA Agrobiology, Brazilian Agricultural Research
Corporation, Seropédica, RJ, Brazil
About the Editors

Elke Jurandy Bran Nogueira Cardoso holds a PhD degree in Plant Pathology
from the Ohio State University (USA) and a post doc from Göttingen University
(Germany). She is currently senior professor of Soil Microbiology and
Biotechnology in the Department of Soil Science at the University of São Paulo
(Brazil), where she has been working since 1971 and has supervised more than 100
post-graduate and post-doctoral students. Her research interests are focused on
ecology and agricultural sustainability, forestry, plant growth-promoting microor-
ganisms, plant microbiomes, organic residues in agriculture and forestry, and soil
remediation. She has published more than 130 scientific articles in international
journals, about 20 books and book chapters, many in cooperation with colleagues
from other countries.

José Leonardo de Moraes Gonçalves is full professor in the Department of Forest

Sciences at the University of São Paulo. He has undertaken extensive research on
soil fertility, site preparation, and plant nutrition, focusing on the tropical and sub-
tropical eucalyptus and pine plantations, including genotypic adaptation and pheno-
typic acclimatization of plantations in regions with high water, thermal, and
nutritional stresses. Ecosystem management and sustained production of wood and
non-wood products from planted forests always were among his main objectives,
having been a pioneer in forest research with minimum tilling in the early 1990s. He
has edited three books and published more than one hundred ­scientific articles in
journals of wide dissemination and international impact. He supervised 25 masters,
24 doctors, and 5 post-doctorates.

Fabiano de Carvalho Balieiro holds a PhD in Soil Science from the Federal Rural
University of Rio de Janeiro (Brazil), where he also was a post doc fellow. He cur-
rently works as a researcher at the National Center for Soil Research at Embrapa
Solos (Brazil), and his research is focused on nutrient cycling, soil organic matter
dynamics and soil ecology in different crop systems (eucalyptus, mixed forest
­plantations, and sugarcane), and native vegetation (Amazon and Atlantic Forests

xv
xvi About the Editors

and Cerrado biomes). Dr. Balieiro has published 27 articles in high impact factor
journals over the past 5 years and edited the book Manual of Fertilization and
Liming for the State Rio de Janeiro (in Portuguese), a publication on the sustainable
­agricultural development in Rio de Janeiro State (Brazil).

Avílio Antônio Franco is a graduated Agricultural Engineer from the Federal

Rural University of Rio de Janeiro (Brazil) (UFRRJ), and he obtained an MSc in
Microbiology from the University of New South Wales (Australia), a PhD in Soil
Science from the University of California-Davis (USA), and a post doc from the
University of Queensland (Australia). He is retired scientist from the Center for
Agrobiology at Embrapa (Brazil) after 40 years of activity. He has supervised 33
graduate students at URRJ and Federal University of Rio de Janeiro (UFRJ) and
published 92 scientific articles and 25 books and book chapters. His research
­interests are soil microbiology (Biological Nitrogen Fixation), plant nutrition, land
reclamation, and agroforestry. He is an effective member of the Brazilian Academy
of Science (ABC) and the Third World Academy of Sciences (TWAS). He has
received the Brazilian National Scientific Award.
Chapter 1
Why Mixed Forest Plantation?

Ranieri Ribeiro Paula, Ivanka Rosado de Oliveira,

José Leonardo de Moraes Gonçalves , and Alexandre de Vicente Ferraz

1.1 Introduction

Although relevant to Brazilian gross domestic product (GDP), forest plantations

currently occupy only a small fraction of Brazilian land with 9.8 million hectares
(Bacha 2008; IBGE 2017). Approximately 96% of these lands are occupied by
monocultures of species of Eucalyptus (75.2%) and Pinus (20.6%), and only a few
forest species occupy another 400,000 hectares (IBGE 2017). These plantations
have expanded over the past 30–40 years on land abandoned by agriculture and
livestock, especially in the Atlantic Forest (South, Southeast, Coastal area of Bahia),
Cerrado (Southeast, Midwest, and North), and Pampa (South) (Gonçalves et al.
2013; IBGE 2017).
Pastures planted with “African” grass occupy at least 80 million hectares in tropi-
cal regions of Brazil, and at least half of those are considered degraded (Boddey
et al. 2004). Additionally, current estimates by the Brazilian Government indicate
that 4.5 million ha of permanent preservation areas of native vegetation need to be
recovered throughout Brazil. In addition, approximately 7.2 million ha of legal
reserve should be recovered mainly in the Amazon, 4.8 million ha in the Atlantic

R. R. Paula (*)
Center for Agricultural Sciences and Engineering, Federal University of Espirito Santo,
Alegre, ES, Brazil
I. R. de Oliveira · J. L. M. Gonçalves
Department of Forest Sciences, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
A. de Vicente Ferraz
Institute of Forest Science and Research (IPEF), Piracicaba, SP, Brazil

© Springer Nature Switzerland AG 2020 1

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_1
2 R. R. Paula et al.

Forest, and 3.7 million ha in the Cerrado—Brazilian savannah (Soares-Filho et al.

2014; Brazil 2017). Public policies are foreseen in the National Plan for the
Recovery of Native Vegetation for the recovery of at least 12 million ha until 2030
(Brazil 2017).
The expansion of highly productive monospecific forest plantations faces several
challenges. Species are recommended for a given site according to edaphoclimatic
adaptation, productivity, quality of wood, and resistance to pests and diseases,
among others. In the case of Eucalypt, higher wood yields (e.g., annual average
increment >40 m3 ha−1 year−1) have been achieved by integrating improved genetic
material, suitable edaphoclimatic conditions, and good silvicultural practices
(Gonçalves et al. 2013). However, breeding programs exist only for a limited num-
ber of species, notably Eucalyptus, Corymbia, Pinus, and Hevea, and for commer-
cial fruit trees. Several potential native and introduced tree species for forest
plantations with economic purposes have little or no level of genetic improvement
(Carvalho 2003).
Most of the soils located in the tropical and warm subtropical portions are gener-
ally deep and well drained, with high acidity and low fertility, mostly classified as
Oxisols and Ultisols (Gonçalves et al. 2013; Guerra et al. 2014). The chemical,
physical, and biological characteristics of soils intended for forest plantations will
be increasingly limiting as plantations occupy lands degraded by agriculture and
livestock. The availability of water is in most cases the main limiting factor for for-
est production, since other edaphic factors can be overcome through mechanization
and fertilization (Stape et al. 2010; Gonçalves et al. 2013). The availability of water
may be a limiting factor for the expansion of highly productive forest plantations in
the regions with predominance of the tropical and subtropical climates, whose dry
season varies between 3 and 7 months. Moreover, the effects of climate change on
forest plantations need better understanding. The mortality induced by lack of water
in native and exotic trees has been detected in several regions of the world, includ-
ing Brazil (Laclau et al. 2013; Rowland et al. 2015). To minimize the risks of tree
mortality due to water shortage, it is indicated to plant species that are adapted and
efficient in the use of resources (Gonçalves et al. 2013). The impacts of highly pro-
ductive trees and plantations on water resources need to be well understood to pro-
mote the sustainable expansion of plantations (Christina et al. 2011; Nouvellon
et al. 2011).
Nitrogen is a nutrient commonly limiting the productivity of forest plantations
with non-nitrogen-fixing species (Gonçalves et al. 2003; Rennenberg et al. 2009;
Laclau et al. 2010; Bouillet et al. 2013; Gonçalves et al. 2013). Although N is natu-
rally available in the soil through the mineralization of organic matter, this is reduced
in degraded soils because of the low content and quality of the organic matter
(Gonçalves et al. 2003). And availability of N is conditioned by the microbial activ-
ity that is regulated by soil moisture content (Rennenberg et al. 2009; Voigtlaender
et al. 2019). Nitrogen fertilizer application in forest plantation may be recommended
according to organic matter concentrations in soil (Gonçalves 1995). For example,
values of 60 kg ha−1 and 30 kg ha−1 of total nitrogen are indicated for commercial
plantations of Eucalyptus and Pinus, respectively, when the concentration of soil
1 Why Mixed Forest Plantation? 3

organic matter is less than 1.5%. These amounts decrease to 20 kg ha−1 if the con-
centration of soil organic matter is higher than 4%. For native species of Brazil with
a medium and high nitrogen demand 50 kg ha−1 of total nitrogen is recommended
(Gonçalves 1995). The production and use of N fertilizers involve environmental
risks of water pollution and greenhouse gas emissions, as well as being increasingly
costly for Brazilian planters due to the fluctuation of the dollar and the influence of
the value of oil (Galloway 1998; Dias and Fernandes 2006).
A growing scientific interest in the establishment of more biodiverse forest plan-
tations has been observed around the world and Brazil (Paquette and Messier 2010;
Brancalion et al. 2012; Bouillet et al. 2013; Del Río et al. 2016; Dai et al. 2018;
Marron and Epron 2019). These plantations may involve only trees and/or trees with
agricultural crops and/or livestock pastures. The call for the establishment of mixed
forests is mainly associated with the possibility of higher productivity and greater
provision of products (e.g., wood for multiple uses, non-timber forest products,
fibers, and proteins) and ecosystem services (e.g., soil and water conservation, car-
bon storage, wildlife feeding). Mixed forest plantations involving N2-fixing legume
species and non-N2-fixing species such as eucalypt have been proposed to increase
productivity and ecosystem services in regions with N-deficient soils (Balieiro et al.
2002; Chaer et al. 2011; Bouillet et al. 2013; Santos et al. 2016; Voigtlaender et al.
2019; Marron and Epron 2019). Tree legumes inoculated with specific bacteria can
fix most of the N demanded for growth and transfer the fixed N to the soil and plants
in companion, as detailed in Chap. 6. Results of research in Brazil testing inter-
cropped Eucalyptus sp. with Acacia mangium (Fig. 1.1) increased the nutrient
cycling rate, contributing to the soil a large amount of N from the biological nitro-
gen fixation (FBN) in only one crop rotation (Santos et al. 2016; Voigtlaender et al.
2019), as detailed in Chap. 3.

Fig. 1.1 Mixed forest of Eucalyptus grandis and Acacia mangium at spacing of 3 m by 3 m (pro-
portion 1:1): (a) 5 months and (b) 30 months after planting, at the Experimental Station of Forest
Sciences of Itatinga, São Paulo, Brazil
4 R. R. Paula et al.

In a recent meta-analysis, Marron and Epron (2019) showed that mixed forest
plantations involving at least equal proportions of N2-fixing and non-N2-fixing spe-
cies are generally more productive than monospecific plantations when established
in sites with low productive capacity. In these sites, poorer in nutrients or water,
positive interactions (e.g., facilitation and complementarity) over negative ones
(e.g., intraspecific competition) are expected to prevail. Sites with lower growth
resource limitations tend to favor fast-growing species more adapted, leading to
greater intraspecific competition (Kelty 2006; Forrester et al. 2006; Bouillet et al.
2013). Thus, the zoning of the productive capacity of the forest sites is a necessary
measure for the best use of the sites destined to the mixed and monospecific planta-
tions. Even when yield is not increased the benefit of long-term sustainability and
other ecosystem services should be considered (see the Chap. 10).
The choice of the right species to minimize the effects of site quality also is
important. According to authors such as Gonçalves et al. (2003) and Kelty (2006),
the success in terms of production and ecosystem service delivery is obtained more
easily by combining species that differ in growth rates, in growth resource require-
ments, and in the form they obtain resources. The combination of these functional
characteristics of the species is necessary to promote a better capture of the resources
to maximize nutrient cycling and the recovery of degraded soils in Brazil (Gonçalves
et al. 2003).

1.2 Socioeconomic Benefits

The increase in forest cover promoted by forest plantations with economic objec-
tives and recovery of ecosystem functions is an urgent need pointed out by several
authors (Ab’Sáber et al. 1990; Machado and Bacha 2002; Bacha 2008; Brancalion
et al. 2011; Chaer et al. 2011; Guerra et al. 2014; Soares-Filho et al. 2014; Brazil
2017). There are numerous public and private actions in the Brazilian forestry pro-
duction and conservation program aimed at the sustainability of the development of
this sector: for example, the ABC Plan (Low Carbon Emissions Agriculture), and
the Native Vegetation Protection Law (Law 12.651, of May 25, 2012), which defines
the proportions of areas for protection of native vegetation and for forestry, agricul-
ture, and livestock in rural properties, as well as the process of restoration of native
vegetation in degraded areas. More recent legislation, called National Policy for the
Recovery of Native Vegetation, was created to promote the revegetation of Brazilian
biomes with mixed forest plantations and agroforestry. Moreover, other initiatives
involving nongovernmental organizations, such as the Atlantic Forest Restoration
Pact, bring new approaches to reconcile restoration of the biome with economic
returns (Brancalion et al. 2011; Amazonas et al. 2018).
One of the great novelties of the Law 12.651 is the possibility, according to pre-­
established criteria, in mixing a 1:1 proportion of exotic and native species includ-
ing fruit trees, in the legal reserve area (i.e., forest area of rural property intended for
forest management and biodiversity conservation). This mechanism allows the
1 Why Mixed Forest Plantation? 5

formation of mixed multipurpose forests, as well as reduction of planting costs.

Another relevant aspect is the legal reserve having a minimum area set at 20% in
relation to the total size of the property for all regions of the country except the
Amazon. In the Amazon region, legal reserve areas range around 80% (forest
region), 35% (Cerrado region), and 20% (general field region). Chapter 13 details
the Brazilian legal framework of multifunctional mixed forest plantations.
Mixed forest plantations provide a greater diversity of products and ecosystem
services than monospecific forest plantations (Bouillet et al. 2013; Del Río et al.
2016; Dai et al. 2018; Voigtlaender et al. 2019). The mixture of two species with
high timber value, with one being a N-fixer, has been the model most studied and
recommended by researchers working with forest for timber production (Forrester
et al. 2006; Bouillet et al. 2013; Del Río et al. 2016; Marron and Epron 2019). Pairs
of mixtures of fast-growing exotic species such as Eucalyptus sp. or Pinus sp. with
legumes such as Acacia mangium or A. mearnsii have the potential to offer a wide
range of products in the same area, including timber, firewood, coal, tannins, resins,
and essential oils. Such mixtures also contribute with the addition of ecosystem
services, including the reduction of surface runoff and consequent more water infil-
tration, carbon sequestration, and biological fixation of N, culminating in the reduc-
tion of nitrogen fertilization use (see also Chap. 10).
Forest plantations carried out by companies on their own area or via forest out
grower schemes use high-technology equipment with variation of techniques in
function of the terrain slope (Malinovski et al. 2006; Gonçalves et al. 2013). The use
of heavy machinery (e.g., tractors and harvesters) during planting and harvesting
has restrictions because of local topography, and the alternatives for harvesting
machinery in steep areas are even more expensive. Among the main limitations for
the establishment of mixed forests with high technology, we cite the increase in the
operational cost during harvesting. This limitation may not occur in plantations car-
ried out in slope areas where cutting is done primarily by chainsaws. Moreover, the
increase in the cost of harvesting in steep areas, in comparison to flat areas, may
render unfeasible forest plantations with low value added (e.g., firewood and char-
coal). Under these conditions, the planting of mixed forests with species of higher
value, such as fruit trees or trees for seed production, noble wood, resins, and latex,
among others, would be an interesting alternative.
The increase in income generated by the supply of both timber and non-timber
products and ecosystem services (e.g., water increase, conservation of plant and
animal diversity) could be much higher with mixed plantations with a greater diver-
sity of species (Brancalion et al. 2012). Forestry production participated in the econ-
omy of 87% of Brazilian municipalities in 2017; 77.3% of revenue generation was
derived from forestry (e.g., logs, firewood, and charcoal) and 22.7% from vegetable
extraction (e.g., fruits, nuts, waxes, latex, resins) (IBGE 2017). Mixed forest planta-
tions are an alternative to land use by small- and medium-sized producers who are
interested in obtaining multiple forest products, and to increase ecosystem services
on their properties (Brancalion et al. 2012; Brazil 2017). Species of the families
Fabaceae, Myrtaceae, Arecaceae, and Lecythidaceae, among many others, can
function both as a source of income and as a source of food for the fauna. Mixed
6 R. R. Paula et al.

plantation composed of groups of trees capable of producing wood, fruits, nuts, and
extractives planted side by side allows to maintain a forest cover of sloping areas for
a long term and, in this way, could reduce the surface runoff of water after rain
events, and promote the infiltration of water into the soil (Gonçalves et al. 2003).
One of the main barriers to planting for restoration of native ecosystems is the
high costs involved in establishment and maintenance. In some projects, high mor-
tality may occur due to the attack of ants and competition with grasses. For exam-
ple, the costs of establishment and maintenance during the first 2 years after planting
native forests of the Atlantic Forest can exceed 5000 USD per hectare. These costs
may be even higher if farmers request access to technical assistance, since seedlings
and manpower are limited. Alternatives proposed to reduce costs of planting by
generating more revenue include the mixing of Eucalyptus species for wood pro-
duction with a relatively high-diversity (about 20–30) native species (Amazonas
et al. 2018).

1.3 History of Mixed Plantations

Since the 1940s, several native and exotic forest species have been tested to select
the most suitable ones for monospecific plantations. In Brazil, monocultures of
Eucalyptus and Pinus have stood out in relation to native species, showing faster
growth and good wood quality for multiple uses. Mixed forest plantations have been
planted mainly with the objective of recovering degraded areas and restoring eco-
systems (Kageyama and Castro 1989; Rodrigues et al. 2009). These plantations
were planned according to the logic of ecological succession observed in natural
forests, mixing groups of native and exotic species each one with different require-
ments for growth resources and lifetimes. The species used have little or no genetic
improvement and the productivity of these types of plantations is not an important
factor to consider. The use of mixed plantations for timber production is not very
common in the practice of forest companies and producers.
In the last 30 years, several experiments about mixed plantations have been
established in Brazil. These plantations were tested in experimental fields installed
in different regions of the country in partnership with national and international
research institutes and universities. Mixed forest plantations with fast-growing spe-
cies with economic value, especially Eucalyptus × Acacia mangium, have recently
been tested. The first experiment with A. mangium was set up in 1979 by EMBRAPA
(Brazilian Agricultural Research Company) (Tonini et al. 2010). In 1985 the first
plantation of Acacia mangium for genetic improvement was established and, in
1993, EMBRAPA Agrobiology established the experimental plantations that later
culminated in the pioneering research center in studies of recovery of degraded
areas with fast-growing leguminous species (Franco and Faria 1997; Macedo et al.
2008; Chaer et al. 2011).
From 1989 to 2000, there was a cooperation between Brazil and Germany in the
studies of A. mangium in the North of Brazil with the project “Studies of Human
1 Why Mixed Forest Plantation? 7

Impact on Forests and Floodplains in the Tropics.” In 1995, the project “Soil and
Climate Zoning for the planting of fast-growing tree species in the Amazon” was
created. This project was financed under the “Pilot Program to Conserve the
Brazilian Tropical Forest.” The aim was to contribute to the reduction of ­deforestation
rates in the region supplying the market with timber from areas with less legal
restrictions instead of using native forests (Balieiro et al. 2018). The network of
experiments was established in several units of EMBRAPA, in the states of
Amazonas, Pará, Amapá, Acre, Rondônia, and Roraima. Different clones of
Eucalyptus and Acacia mangium seedlings and several native species were tested.
In the last 10 years, Brazil, in cooperation with 34 countries, as France, the
United States, Germany, Australia, Congo, the Netherlands, South Africa, China,
Colombia, and Cuba, has developed studies specifically with Acacia mangium
(Balieiro et al. 2018). In cooperation with the research institute CIRAD UMR
Eco&Sols (La Recherche Agronomique pour le Développement), the thematic proj-
ect “Ecological intensification of eucalypt plantations by the association with nitro-
gen fixing tree legumes” was approved by the Research Support Foundation of the
State of São Paulo and its French counterpart, the “Intensification écologique des
écosystèmes de plantations forestières. Modélisation biophysique et évaluation
socio-économique de l’association d’espèces fixatrices d’azote,” which was
financed by the French National Research Agency. This project included a network
of experiments installed in the southeast region, covering three states of Brazil,
Minas Gerais, Rio de Janeiro, and São Paulo. The results showed that there were
gains of biomass in the mixed plantations compared to Eucalypt monoculture when
under favorable climatic conditions (hot and humid climate) for the development of
A. mangium, low soil fertility and low water restrictions (Bouillet et al. 2013). This
network of experiments has been recently expanded (since 2015) in two other
Brazilian states, Tocantins and Mato Grosso. Previous studies were conducted in the
Congo with similar edaphoclimatic condition as observed in the northern part of
Brazil, showing a great productivity of these plantations and indicating a high
potential of the eucalypt-acacia association (Bouillet et al. 2013). Chapter 2 details
the studies about mixed forest plantation growth at different sites and under diverse
silvicultural management.

1.4  ajor Combinations of Species Already Tested

M
in Practice and Potential

There are only few studies testing the growth of native species in mixed plantations
compared to monocultures with the same species (Carvalho 1998, 2003; Machado
and Bacha 2002). Carvalho (1998 and 2003) indicated the success of some of these
studies to minimize the risks of pest attacks, such as the mixture of species of the
Meliaceae family, as Cedrela fissilis and Cabralea canjerana, with other native or
exotic fast-growing species to reduce the attacks of the cedar borer (Hypsipyla
8 R. R. Paula et al.

grandella). According to this author, species with reduced requirement of light at

young age and with a large canopy when associated with fast-growing species gen-
erate stands with higher growth and straighter stem. For example, Aspidosperma
polyneuron trees mixed with Grevillea robusta showed a straighter stem and 41%
higher height growth than in monoculture after 16 years. Other timber species with
good performance in mixed forest plantations, highlighted in Carvalho’s bibliogra-
phy, include the non-legumes Cordia trichotoma, Prunus brasiliensis, Talauma
ovata, Laplacea fruticosa, Luehea divaricata, Patagonula americana, and Tabebuia
heptaphylla, and the legumes Anadenanthera peregrina var. falcata, Parapiptadenia
rigida, Peltophorum dubium, Piptadenia gonoacantha, Piptadenia paniculata, and
Sclerolobium paniculatum. Additionally, potential species for timber indicated for
mixed forest plantations are Apuleia leiocarpa, Caesalpinia leiostachya,
Enterolobium contortisiliquum, Hymenaea courbaril, Machaerium scleroxylon,
and Pterogyne nitens (Carvalho 1998). Planting of yerba mate (Ilex paraguariensis)
in southern Brazil has been done in monoculture. In a literature review, Baggio et al.
(2008) verified that there is great potential to associate this species with other natives
of the southern region of Brazil, including leguminous N2 fixers, with relevant eco-
nomic gains in small properties.
The mixture of fast-growing species, including the N2-fixing ones, has been
tested in recent years in Brazil (Balieiro et al. 2002; Coelho et al. 2007; Bouillet
et al. 2013; Santos et al. 2016; Soares et al. 2018). Mixed-species plantations of
Eucalyptus and N2-fixing Pseudosamanea guachapele with a 1:1 proportion were
established in 1993 in the municipality of Seropédica, Rio de Janeiro state, Brazil
(Balieiro et al. 2002). The authors showed that mixed stands had higher biomass
production than pure plantations of each species, and despite the 10% less biomass
of eucalypt in mixed than in pure stands, the efficiency of nutrient use of eucalypt
increased in the consortium.
In São Paulo state, Brazil, a combination of five leguminous native trees,
Peltophorum dubium, Inga sp., Mimosa scabrella, Acacia polyphylla, and Mimosa
caesalpiniaefolia, and one exotic species, Acacia mangium, was tested with
Eucalyptus grandis (Coelho et al. 2007). Each species was planted in monocultures
and in consortium with E. grandis in commercial spacing (3 m × 3 m). The legumi-
nous trees were planted between the plants of E. grandis in alternating rows with a
1:1 proportion. The study showed that interspecific competition between E. grandis
and legumes is greater than intraspecific competition until the age of 24 months.
Among the species studied, A. mangium was the one that best resisted to the com-
petition with E. grandis.
Studies have indicated that higher yields occur mostly in mixed plantations with
species of Eucalyptus sp. and Acacia mangium, and in monospecific Eucalyptus sp.,
under tropical climate (Bouillet et al. 2013). In regions of subtropical climate, mixed
forest plantations of E. grandis and A. mangium are less productive than pure plan-
tations of E. grandis. One of the main concerns of these authors is the high competi-
tion capacity of E. grandis on A. mangium in places where climatic conditions are
optimal for the development of eucalypt and suboptimal for acacia. The same
behavior was not observed in mixed plantations of the same species in an experiment
1 Why Mixed Forest Plantation? 9

in Congo (Bouillet et al. 2013). In this case, mixed plantations produced more bio-
mass than eucalypt monocultures because they were embedded in areas character-
ized by nutrient-poor soils (e.g., sandy soils, deep soils, leachate), and warm and
humid climates, but with low water limitation. These conditions are favorable for
the growth of A. mangium but not optimal for eucalypt trees. Similar soil and cli-
mate conditions are found in the Brazilian Cerrado and transitional areas with the
Amazon rainforest (e.g., Mato Grosso, Tocantins, and Roraima states). Santos et al.
(2016) investigated the consortium between Eucalyptus grandis × E. urophylla and
A. mangium in the municipality of Seropédica, Rio de Janeiro state, in a region with
N-deficient soils and favorable climate for acacia. They also found a higher produc-
tivity of mixed plantings compared to pure eucalypt plantations.
The mixture with a 1:1 proportion of Eucalyptus spp. and Acacia mearnsii has
been tested mainly in the southern part of Brazil. A. mearnsii has been more suc-
cessful than A. mangium in facing eucalypt competition in this region. For example,
the wood production of A. mearnsii in mixed stands with E. globulus was 77% of
the production found in monospecific stand. In contrast, eucalypt wood production
in the mixture was only 36% of the production found in monocultures (Soares et al.
2018). Mixed stands of A. mearnsii with Eucalyptus sp. presented similar produc-
tion to monocultures (Vezzani et al. 2001; Soares et al. 2018), besides improving the
nutritional status of soil and eucalypt trees (Vezzani et al. 2001).
Recent studies have suggested the use of eucalypt in consortia with many native
species (20–30), in order to promote the restoration of ecosystems linked to the
economic return from the sale of timber (Amazonas et al. 2018). Native species,
including N-fixing legumes, established in mixture between eucalypt lines had their
growth affected by eucalypt regarding their growth rates in three experimental sites
with tropical climate without a dry season. The authors highlight the high capacity
of interspecific competition of eucalypt and native species, reaching 75% of the
basal area of pure eucalypt plantations, although with only 50% of tree density.
The planting of N2-fixing trees is necessary for reclamation of degraded lands by
agriculture and livestock or more severe situations such as mining. In a recent
review, Chaer et al. (2011) described several successful studies using N2-fixing
legumes for land reclamation. The main objective of these plantings is the recupera-
tion of the soil or substrate to provide colonization of new species in the future. A
major concern today is the degraded soils of the Cerrado and Amazon region.
Studies have shown that pastures cover about 62% of the deforested area of the
Brazilian Legal Amazon, representing 335,700 km2, and that the states with the
highest incidence of pastures occur in Mato Grosso, Pará, and Rondônia (Almeida
et al. 2016). According to EMBRAPA, half of this area is degraded, 30% is moder-
ately degraded, and only 20% is in good condition. An alternative to recover
degraded areas and improve the region’s economy is through the insertion of inter-
cropped plantations with fast-growing N2-fixing legumes and eucalypt. The intro-
duction of mixed acacia and eucalypt plantations is an alternative for the recovery
of degraded areas and can increase the economy of small- and medium-sized farm-
ers (Griffin et al. 2011).
10 R. R. Paula et al.

1.5 Final Remarks

Brazil has millions of hectares of lands where forest plantations should be used to
promote both economic and environmental gains. Forest covers promote important
ecosystem services with emphasis on soil protection against erosion, silting of
watercourses, and improvement of water infiltration.
Monospecific forest plantations with non-N2-fixing species require higher fertil-
izer inputs and may have limited productivity on degraded soils with low nutrient
and water availability. The environmental benefits of monospecific forest planta-
tions may be more limited in these regions.
Mixed forest plantations involving the mixture between N2-fixing and non-­N2-­
fixing trees have been highlighted as the most promising to sustain and/or increase
the productivity of forests in regions limiting for development of monocultures.
These more biodiverse plantations may be composed of two or more species used
for different purposes, such as timber and non-timber products, soil protection in
steep land, and recharge area of the groundwater, besides the recovery of
degraded soils.
The introduction of the N2-fixing species into eucalypt plantations, for example,
is associated with improved nutrient cycling, especially nitrogen, with the addition
of hundreds of kilograms of nitrogen via litterfall, root turnover, pruning of branches
and leaves, and crop residues. Lower yields sometimes found in mixed forest plan-
tations relative to monocultures are balanced by the increase in long-term
sustainability.
There is need to broaden the debate on the ecosystem benefits of mixed forest
plantations in relation to monocultures. Several species are promising for the com-
position of these more biodiverse forests, but little is known about the combinations
and the edaphoclimatic conditions that permit to maximize the gains of the mixture.

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Chapter 2
Growth Patterns at Different Sites
and Forest Management Systems

Carolina Braga Brandani, Felipe Martini Santos, Ivanka Rosado de Oliveira,

Bruno Bordon, Maurel Bheling, Eduardo Vinicius Silva,
and José Leonardo de Moraes Gonçalves

2.1 Introduction

Associating biological nitrogen-fixing trees (NFT) with non-nitrogen-fixing trees

can increase biomass production of plantations (Bouillet et al. 2013; Santos et al.
2016). Nitrogen provided by biological fixation is likely the main reason for mixed-­
forest plantations with N2-fixing trees being more productive than non N2-fixing
monocultures, since N plays an important role in the plant metabolism, soil-­
microbial activity, and cycling of other macronutrients that foster the forest growth.
Hence, the introduction of N2-fixing species in fast-growing eucalypt plantations
could be a management strategy in sites where eucalypt growth is limited by N
availability (Stape et al. 2010; Koutika et al. 2017; Tchichelle et al. 2017).
Decades of eucalypt breeding in Brazil, associated with adequate fertilizer inputs
and weed control, have made the seedlings and clones in Brazilian plantations much
more productive than N2-fixing tree species. Therefore, the competition between
eucalypt and N2-fixing species in this scenario has differed largely from patterns
observed in less productive eucalypt plantations (Laclau et al. 2008).

C. B. Brandani (*)
College of Agricultural, Consumer and Environmental Sciences - Animal and Range
Sciences, New Mexico State University, Las Cruces, NM, USA
e-mail: brandani@nmsu.edu
F. M. Santos · E. V. Silva
Federal Rural University of Rio de Janeiro, Seropédica, RJ, Brazil
I. R. de Oliveira · B. Bordon · J. L. M. Gonçalves
Department of Forest Sciences, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
M. Bheling
Embrapa Agrosilvopastoral, Brazilian Agricultural Research Corporation, Sinop, MT, Brazil

© Springer Nature Switzerland AG 2020 15

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_2
16 C. B. Brandani et al.

The management practice aiming to supply the nutritional demand for N fertil-
ization in eucalypt plantations has been achieved by the introduction of Acacia
mangium in Brazilian forest plantations (Voigtlaender et al. 2012; Voigtlaender
et al. 2019). Future studies seek to consolidate the increase of the productive poten-
tial of acacia in order to improve its competitiveness in terms of wood production
with eucalypt in mixed stands as well as conciliate both trees’ growths. Therefore,
two issues are of great importance: (1) to find the best arrangements (additives and
replacement designs) between trees and (2) to obtain improved acacia genetic mate-
rials that match the site conditions and woody product of interest.
Thus, it is necessary to consider that the productivity of tree plantations is a func-
tion of supply, capture, and efficiency of resources (Richards et al. 2010). In this
sense, to unravel the competition for light, water, nutrients, and effects of intra- and
interspecific competition on biomass partitioning between tree components (Le
Maire et al. 2013) becomes fundamental, since these are the main processes influ-
encing tree growth in mixed-forest plantations.
Our objective in this chapter is to gather a large number of data obtained in the
last decade regarding above- and belowground mixed-forest growth in Brazil and to
give insights into the main drivers influencing the development of Eucalyptus and
Acacia mangium, including soil and climate conditions, silvicultural management,
and species interactions. Additionally, we intend to provide important information
for a wide range of land managers, from small farmers producing firewood to large
commercial forestry companies focused on timber or pulp production, looking for
sustainable mixed-forest systems.

2.2  oil and Climatic Conditions on Stand Growth

S
of Mixed-­Forest Plantations

Climatic characteristics play a key role on the aboveground biomass production of

mixed-forest plantations relative to monoculture. Acacia is well suited for the hot-
test and most humid sites (Atipanumpai 1989; Krisnawati et al. 2011) and, for this
reason, its productivity can vary greatly according to solar radiation intensity, vapor
pressure deficit, and water availability. Acacia has not been studied thoroughly for
breeding characteristics as has the eucalypt, and does not offer many genotypes
(hybrids, clones, genetic material) that could better adapt to specific sites. However,
eucalypt has a broad option of genetic material (species and hybrids) provided by
several decades of eucalypt breeding, offering different kinds of genetic materials
that can be chosen to match certain climatic and edaphic conditions of each site
(Gonçalves et al. 2013), in order to maximize the growth and yield of these
plantations.
Although acacia has not yet achieved an exponential breeding potential, it has
attracted great attention due to its physiological ability to fix atmospheric nitrogen,
which benefits the soil-plant system. In the last decade, studies on the growth
2 Growth Patterns at Different Sites and Forest Management Systems 17

Table 2.1 Main edaphic and climatic characteristics from experimental sites in Brazil and Congo
Soil
Mean Mean air Annual Soil total organic
temperature humidity rainfall N matter
Sites Soil type (°C) (%) (mm) (g kg−1) (g kg−1)
Santana do Ferralsol 24.4 71 1240 1.7a 3.8a
Paraíso/
Brazil—Cenibra
Bofete/ Ferralsol 21.4 71 1420 0.84a 2.4a
Brazil—Suzano
Luiz Antônio/ Ferralic Arenosol 23.3 65 1420 0.64a 1.7a
Brazil—
International
Paper (IP)
Itatinga/ Ferralsol 19 70 1390 0.91a 3.5a
Brazil—(USP)
Seropédica/ Planosol 24 81 1370 0.38b 0.62b
Brazil
Pointe-Noire/ FerralicArenosol 25.7 81 1130 0.46a 1.14-­
Congo 1.71a
Source: Bouillet et al. (2013) and Santos et al. (2016)
a
[0–5 cm] layer
b
[0–10 cm] layer

dynamic of mixed-species plantations at different tropical and subtropical sites

were carried out by a multidisciplinary thematic project entitled “Ecological
intensification of eucalypt plantations through association with nitrogen-fixing
­
leguminous tree species.” The project was developed by French researchers from
the Centre de Coopération Internationale en Recherche Agronomique pour le
Développement (CIRAD), with the collaboration of Brazilian researchers from for-
estry companies, research institutes, and universities. A network of experiments was
set up in several Brazilian soil and climatic conditions. Some of the obtained results
were published by Bouillet et al. (2013) and Santos et al. (2016) (Table 2.1 and
Fig. 2.1), where they evaluated Eucalyptus and Acacia mangium in pure and mixed
plantations established in distinct regions of southeastern Brazil and in Congo, dur-
ing a complete rotation (~6 years).
The results from Bouillet et al. (2013) showed that there were gains of aboveg-
round biomass in the mixed plantations compared to eucalypt monoculture only in
Congo. This result was attributed to the local conditions of hot and humid climate
(annual averages of 27 °C and relative humidity of 80%), low soil fertility (espe-
cially with regard to N), and water restrictions. However, at the Brazilian sites, the
global biomass production of the mixed plantations was not different and some sites
showed inferior biomass production relative to eucalypt monoculture, which evi-
denced the suppression of acacia growth by the superior genotypes of Eucalyptus
(Laclau et al. 2008; Bouillet et al. 2013). These results were attributed to the unfa-
vorable climatic conditions of the sites located at the southeast of Brazil for the
development of acacia, specially the low temperatures (ranging from 19 to 24 °C,
18 C. B. Brandani et al.

(A)
160 A. mangium
Eucalyptus spp.
140
Stemwood production (%) vs E100
120

100

80

60

40

20

(B)
140

120
Stemwood production (%) vs E100

100

* *
80

60

40

20

0
Cenibra Suzano USP IP Congo Seropédica

Fig. 2.1 The values of stemwood production were compared between the mixed-species
Eucalyptus sp. and A. mangium 100%—E100A100 (a) and 50%—E50A50 (b) stands of the plant-
ing density composed by two species with the stemwood production of Eucalyptus monoculture
without nitrogen fertilization (E100) in different tropical regions, site by site. Data compiled from
the sites evaluated by Bouillet et al. (2013) and compared with the site in Seropédica (Santos et al.
2016). ∗Indicates significant statistical difference in trunk/stem production relative to control
(E100). Source: Extracted from Santos et al. (2016)

throughout the year, including frost in cooler periods), and equally due to the high
competition for resources in these highly productive plantations.
Contrarily, Santos et al. (2016) performed an experiment in the Southeastern
Brazilian coast (in Seropédica, Rio de Janeiro state), where the climatic conditions are
favorable for the development of acacia (average annual temperatures of ~25 °C, uni-
form rainfall distribution throughout the year, and relative humidity close to 80%).
Additionally, the soil is sandy with low natural fertility, which could enhance the
benefits of the biological nitrogen fixation (BNF) of A. mangium in consortium with
2 Growth Patterns at Different Sites and Forest Management Systems 19

E. urophylla x grandis, according to the stress gradient hypothesis (Forrester 2014).

In this study the dynamics of aboveground biomass production in monospecific and
mixed stands of eucalypt and acacia over 5 years were compared with those obtained
by Bouillet et al. (2013) by relativizing the overall production of the arrangements
(A. mangium + E. grandis) in relation to the pure eucalypt (E100) treatment (with
1111 eucalypt ha−1) of each respective site. The mixed stands with the E100A100
arrangement (with 1111 acacia +1111 eucalypt; totaling 2222 plant ha−1), in all sites,
produced similar amounts of stem wood biomass relative to the E100 arrangement.
However, the biomass production at the Seropédica site was approximately 40%
greater than that of the E100 treatment. The low relative production of A. mangium
stem wood biomass at the sites located in the São Paulo state (Suzano, USP, and IP)
may explain why the production in the E100A100 arrangement did not surpass that in
the E100 treatment. These sites have similar annual average temperatures below those
of the Seropédica and Cenibra sites (Santana do Paraíso, Minas Gerais state), where
the contributions of A. mangium to the overall stem wood biomass of the population
in E100A100 were considerably greater relative to the other sites.
For the E50A50 arrangement (with 555 acacia + 556 eucalypt, totaling 1111
plants ha−1) a site located at Pointe-Noire, in Congo, characterized with an ideal
climatic condition, was also included in this comparison. The stem wood production
of E50A50 stands only exceeded that of the E100 at the Congo and Seropédica sites,
although the statistical differences in both studies were not significant at the 5%
level. Proportionally, A. mangium was more productive in Congo, followed by the
Santana do Paraíso and Seropédica sites in Brazil. These sites have similar annual
temperatures, above 24 °C, whereas the Seropédica and Congo sites have the poor-
est soils in terms of nutrients and organic matter.
In the North of Brazil (Roraima state), where the weather is characterized by a
higher annual temperature (27 °C) and precipitation (2000 mm) than in the
Southeast, the average productivity was 25 m3 ha−1 year−1 (Tonini 2010). There are
reports of wood productivity of Acacia mangium from 10 to 61 m3 ha−1 year−1
obtained in the Southeast of Brazil (at the Vale do Rio Doce region), at 5.3 years of
age (Silva et al. 1996), where the average annual temperature and precipitation are
lower than in the Northeast of Brazil, such as in Roraima state. Plantations with
adequate silvicultural management, at 3 years of age, can reach 15 m of height and
40 cm in diameter at breast height (DBH), which represents an average annual
increment of 45 m3 ha−1 year−1 (Souza et al. 2004).
It is worth noting that in mixed-forest plantations, if species or sites are not
complementary and correctly chosen, one species may suppress the growth of the
other, which may result in less productivity than in monocultures. The success of
mixed-species plantations is greatly dependent on the selection of N2-fixing species
depending on site attributes, relative growth rate of both species, and N limitation of
tree growth at the site (Forrester et al. 2005; Laclau et al. 2008). It is difficult to
predict which species combinations will lead to increases in productivity in mixed-­
forest plantations when no empirical information exists. This depends not only on
the attributes of the species but also on the conditions of the site, mainly relative to
water and nutrient availability, average annual temperature and precipitation, as
well as weather through the year.
20 C. B. Brandani et al.

2.3 Silvicultural Management

Eucalyptus and Acacia species are chosen for their capacity to grow rapidly (the
average rotation in Brazil is of ~7 years) and produce wood of excellent quality for
cellulose, charcoal, and construction and fence posts. In some cases, a certain site
can support high wood production with proper management, but in others, there
may be serious problems.
The mixed eucalypt and acacia plantations can be established aiming at enhanc-
ing the productivity of lands that were degraded by deforestation and intensive agri-
cultural disturbances. The development of improved forest planning and operations
can increase the utilization and minimize or avoid adverse environmental effects.
Some principles, aims, strategies, and silvicultural practices must be followed to
develop sustainable single- and mixed-species eucalypt and acacia stands.
The success of single- and mixed-species eucalypt and acacia plantations
depends directly on the soil preparation. The great advances in the last 30 years in
Brazil were the understanding and abolition of burning as a way to clean the land
and the adoption of conservationist techniques for soil management, which culmi-
nate in the implementation of tillage systems with minimum soil disturbance
(Gonçalves et al. 2008).
Concerns regarding the conservation of natural resources and the use of post- and
preemergence herbicides were the factors predisposing and permitting the adoption
of minimum tillage. Weed control with herbicides was a crucial factor, since the
minimum tillage system uses no ploughed land inversion (unlike the conventional
system), so the weed seed bank remains on the topsoil rather than buried, which
favors the infestation of plants and makes manual control operationally and eco-
nomically unfeasible (Gonçalves et al. 2008). For the mixed-species eucalypt and
acacia plantations, the minimum tillage has been considered as an important prac-
tice as well, since it decreases costs related to weed control, mainly because of the
suppress effect of the forest residue on weed seed bank in the soil surface. A major
limiting factor for plant productivity is the presence of weeds. Good practices can
reduce weed infestation considerably by providing cover by crops, residues, and
mulch, and by minimum soil disturbance. In forests, the problem of weeds is a great
concern. The procedures for their elimination usually are carried out by combining
mechanical and chemical methods, using total-action herbicides (nonselective),
such as glyphosate. During the planting of forest stands, most production systems
apply preemergence herbicides at a 1 m strip on the crop row. After planting, the
postemergence control of weeds is performed by spraying postemergence herbi-
cides. During application, special care must be taken to avoid the drift to leaves and
stems of the cultivated plants because this can cause phytotoxic effects of reduced
growth (Salgado et al. 2011).
The water availability is a critical requirement in mixed eucalypt and acacia
plantations (Nouvellon et al. 2012). Soil preparation can help overcome the limita-
tions of water resources for forest plantations in two ways. The first way is due to
increased rainfall infiltration and reduced runoff, which augment the water reserve
2 Growth Patterns at Different Sites and Forest Management Systems 21

in the soil profile. The second way refers to increasing the effective soil depth when
there are soil layers with physical impediment (Gonçalves et al. 2002; Stape 2002).
The large infiltration is favored when compacted or hardened soil layers are dis-
rupted, especially when forest residues are kept on the soil surface. The reduction of
bulk density (resistance to soil penetration) through soil preparation in the planting
row or hole facilitates root growth and, consequently, increases fertilizer use effi-
ciency through great use of water and nutrients by adjacent seedlings. In flat and
slightly undulating terrain/relief, soil preparation may consist of ripping up to a
depth of 30–40 cm. Regarding soil hardening and compaction, ripping-up depth is
usually about 30–35 cm and the planting hole opening, either manually or mechani-
cally, is limited to 25–30 cm. These depths should sometimes be increased depend-
ing on the soil bulk density, for example, for soils that have a fragipan or hardpan
between 50 and 80 cm, or above 80 cm, the ripping depth will be in the range of
60–90 cm, or will reach 110 cm, respectively (Gonçalves et al. 2008).
The effect of soil compaction and other soil disturbances can be severe if opera-
tions are not managed properly. Inappropriate harvesting systems have the potential
to severely and adversely affect soil conditions and water availability. The effects of
planting, tending, and harvesting on the physical properties of the soils will be
highly dependent on the characteristics of soil and equipment used. Delimbing and
debarking the stem at the stump and avoidance of fire significantly reduce nutrient
exports from the aboveground biomass and soil compaction (Gonçalves et al. 2000).
Rotation length is another variable that affects soil quality, because longer rotations
reduce the frequency of major disturbance during harvesting, besides the decrease
in wood production per unit of nutrient exported with an increase in rotation length,
since the average concentration of most nutrients decreases with tree age. Hence,
overall nutrient-use efficiency measured as wood production per unit of nutrient
accumulated can be increased by prolonging forest rotations and using practices
that lead to nutrient and organic matter retention (Gonçalves et al. 2004).
Maintenance of forest residues on soil is undoubtedly important for sustaining
long-term site productivity (Rocha et al. 2016). This requires residues from the pre-
vious rotation as the main resource. Retention of forest residues helps to reduce
erosion, improves water infiltration as well as moisture conservation, maintains or
increases soil organic matter levels and soil microbiology indicators, as well as
contributes to the nutrient cycling in the long term (Gonçalves et al. 2013; Rocha
et al. 2016).
When N2-fixing species are used to facilitate the growth of non-N2-fixing spe-
cies, they should be selected based on the rate at which they cycle nutrients in gen-
eral (Bachega et al. 2016; Pereira et al. 2018) through leaf and fine-root litter and
only secondarily one should consider their ability to fix N. Tree species in mixtures
must also have compatible height growth dynamics to avoid the suppression of
shade-intolerant plants and to reduce competition for light (Forrester et al. 2005).
Mixtures should only be planted on sites where the interactions between species
will increase the availability of (through facilitative interactions) or reduce competi-
tion for (through competitive reduction interactions) one of the major growth-­
limiting resources at that site (see Sect. 2.4 of this chapter).
22 C. B. Brandani et al.

Since investments in fertilizers are relatively high for most forest producers, fer-
tilization should be combined with other silvicultural practices (i.e., soil prepara-
tion, residue management, and weed control) to reduce fertilizer demands in the
short and long terms (Nambiar and Kallio 2008). Adequate nutrient supplies and
balance resulting from fertilization can also improve forest vigor, and reduce the
incidence of disease and the need of fungicides (Almeida et al. 2010). There are
significant yield gains in response to fertilization in most forest plantations
(Gonçalves et al. 2013). Regardless of weather conditions, the magnitude of the
response depends on the nutritional demand of the genotype and on the availability
of soil nutrients. Gains in productivity attributed to mineral fertilizers (macro- and
micronutrients) are quite variable and high, but in general they represent at least
30–50% on average (Gonçalves 2011).
Nutrient cycling reduces tree dependence on net nutrient supply from soil
reserves. Mobile nutrients (N, P, and K) in the plant are redistributed from the older
to younger tissue, increasing efficiency for biomass production. Nutritional stages
of a forest stand can be divided into before, during, and after canopy closure
(Gonçalves et al. 2014). Understanding these stages and nutrient cycling is essential
for the adequate planning of fertilizer application (rate, method, and time). Fertilizer
recommendation should be adjusted preferably at local level to the most representa-
tive species and soil types, based on field experimentation, and should allow optimi-
zation of financial returns. Fertilization should be performed during the initial stage
of tree establishment, from the planting to canopy closure. The most frequent and
most significant responses to fertilizers in Brazilian soils are to N, P, K, and
B. Normally, for sandy and water-deficient soils, responses to fertilizers are more
common (Gonçalves et al. 2008; Gonçalves 2011).
Regarding how much fertilizer to apply, especially for fast-growing species
such as acacia and eucalypt, phosphorus doses can be applied at planting, since
this nutrient has low mobility in the soil and relatively low solubility. The K doses
should be divided into one or two surface applications (Gonçalves et al. 2008).
Doses up to 50 kg ha−1 of K2O may be applied thoroughly in one single surface
application, once risks of leaching are low (Maquère et al. 2005; Laclau et al.
2010). The N contribution will be initially to acacia and later will be shared with
eucalypt. Santos et al. (2017a) showed that A. mangium in mixed-species planta-
tions with eucalypt can provide ~30 kg of N ha−1 year−1, only through the leaf
litter deposition over 5 years of rotation, while eucalypt contribution could reach
15–20 kg N ha−1 year−1 at the same period, totalizing 45–50 kg N ha−1 year−1.
Other studies have shown that mixed plantations of A. mangium and eucalypt have
larger concentration of mineral N in the soil than monospecific eucalypt stands
(Voigtlaender et al. 2012, Bachega et al. 2016; Tchichelle et al. 2017s; Voigtlaender
et al. 2019). After mineralization of acacia litter, significant quantities of biologi-
cally fixed N become available for the eucalypt trees. This process may promote
N nutrition in poor tropical soils when the fine roots of eucalypt and acacia are
intermingled or are connected directly through common mycorrhizal networks
(Paula et al. 2015; Pereira et al. 2018). The scenario which does not include resi-
due burning or removal (litter, slash, and bark) and includes fertilizer application
2 Growth Patterns at Different Sites and Forest Management Systems 23

is a practical and economically proven strategy for sustaining production in the

long term (Rocha et al. 2018).
Planting arrangements are one of the main factors that influence the tree growth
and determine the quality and applications of the wood produced. The appropriate
planting density promotes optimum growth rates and efficient plantation management.
Defining the initial spacing for forest plantations is essential because it determines
the amount of resources (water and nutrients) available for each tree growth species.
The planting spacing represents the number of trees in a given area and should be
associated with the best way to manage and harvest the forest stand (Scolforo 1997).
The recommended tree planting design is 3–4 m between rows and 1–3 m between
trees, giving an initial stocking rate, usually of 1000–1800 trees per hectare.
The mixed-specie plantations can be arranged in varied designs (Figs. 2.2 and
2.3). They can be in alternating rows of each species, or even with both species
interplanted in the same row. The replacement and additive series are the most com-
mon types of arrangements (Forrester et al. 2006). In replacement series, the total
number of trees per stand is constant; only the proportion of each species will be
changed. For example, in an area with 1111 trees per hectare 50% of the stand will
be composed by one tree species (555 trees) and 50% by another species (555 trees).
Recent experiments have indicated that planting trees of each species in double
rows instead of alternating plants may reduce competition between eucalypt and
acacia as well as facilitate the harvesting of trees at different stages of development.
In additive series, the total number of the main species of interesting (e.g.,
Eucalyptus) will be the same, while the density of the other species will vary: for
example, 100% of eucalypt and 25% of another species or 100% of eucalypt and
50% of another species. These types of series allow the evaluation of the effects of
the stand density and the interactions between species. Replacement and additive
series have been used in mixed-species experiments to analyze the growth and the
productivity of eucalypt and leguminous trees.
Based on the published mixed-species trials utilizing the replacement series
design, and where mixtures were more productive than monocultures, 1:1 mixtures
were one of the most productive arrangements (Binkley et al. 2003; Forrester et al.
2004). These density and proportion between two species encourage the canopy to
close rapidly, reducing weed problems and improving the tree form and branching.
If the goal is to produce solid timber for sawmills this density of planting is high
enough to allow trees with exceptional form and vigor to be selected in a thinning
plan of the stand.
During the pre-closure phase, trees tend to be more responsive to cultivation,
fertilizers, and weed control. After canopy closure, intra- and interspecific competi-
tion for resources becomes strong. The density and the design of plantations directly
influence the processes of facilitation, competition, and consequently tree growth
(Medhurst et al. 2001). An important issue for the design of mixed plantations is the
definition of the optimal spatial arrangement depending on localization (e.g., cli-
mate and type of soil) to better understand inter- and intraspecific interactions and
also to facilitate the management. Wide spacing may also be used in water catch-
ments to increase water yield in the site (Lima et al. 2012).
24 C. B. Brandani et al.

Fig. 2.2 Scheme of the 100 / 100E+N 100A

different planting designs
with additive and
replacement series

30 m
(adapted from Laclau et al.
2008)

30 m
100E:25A 100E:50A

100E:100A 50E:50A

Eucalyptus grandis
Acacia mangium

33A:67E 50A:50E

Eucalyptus
Acacia mangium

Fig. 2.3 Scheme of Eucalyptus and Acacia trees in one or double rows instead of alternating
plants with two lines of Eucalyptus trees with one (33A:67E) or two (50A:50E) lines of Acacia
trees
2 Growth Patterns at Different Sites and Forest Management Systems 25

There are many different ways to manage the interactions in mixed-species plan-
tations. These involve different designs, delayed planting of certain species, varying
plant densities, or early removal and thinning of some species. Therefore, mixed-­
species plantations can be used to meet a wide range of economic, silvicultural, and
sustainability objectives.

2.4 I ntra- and Inter-specific Interactions (Competition

and Facilitation Processes) in Stand Growth

In the tropics, eucalypt plantations are predominantly established in monocultures

throughout successive short rotation cycles (6–8 years) (Gonçalves et al. 2013) that
can result in substantial changes in soil quality and biogeochemical cycles of nutri-
ents (Chaer and Tótola 2007; Gonçalves et al. 2004; Stape et al. 2010; Rocha et al.
2018). One of these important changes concerns the soil nitrogen balance, which
generally becomes negative with multiple rotations due to combinations of high N
exports from timber harvests and low doses of N fertilizers that are typically applied
(Corbeels et al. 2005; Laclau et al. 2010; Rocha et al. 2018). Hence, the establish-
ment of mixed-species plantations of eucalypt with N2-fixing trees has been pro-
moted due to the increase in the availability of N for eucalypt trees, making it
possible to dispense the use of N fertilizers (Laclau et al. 2008; Voigtlaender et al.
2012; Voigtlaender et al. 2019). We can show other benefits of these mixtures, as
increase of soil fertility and recycling of micro- and macronutrients (Balieiro et al.
2004; Forrester et al. 2005; Santos et al. 2017b), intensification of above- and
belowground biomass production (Bouillet et al. 2013; Laclau et al. 2008), and
increase of soil carbon (Balieiro et al. 2008; Forrester et al. 2006; Resh et al. 2002)
and nitrogen stocks (Voigtlaender et al. 2012; Voigtlaender et al. 2019). In fact,
these benefits have been seen in studies in which mixed plantations with legumi-
nous trees were more productive than in monospecific forest plantations (Binkley
et al. 2003; Forrester et al. 2006; Laclau et al. 2008; Bouillet et al. 2013; Santos
et al. 2016). However, other studies showed productivity of mixed plantations not
different from eucalypt monoculture in the same stock density (Forrester et al. 2006;
Firn et al. 2007; Bouillet et al. 2013).
The benefits and processes influencing the mixed-forest growth must be better
understood through concepts regarding ecological interactions between tree species
in mixed-forest stands, such as competition, competitive reduction, and facilitation.
The balance between competition and facilitation will cause a strong impact on the
productivity and the biomass accumulation in mixed plantations.
Competition occurs when two or more species are interacting and seeking the
same sources of light, water, and nutrients until a given species exerts a negative
effect, such as a decrease in the growth rate or mortality of the other species, less
adapted to the environmental dynamics created by the mixtures (Forrester et al.
2006; Vandermeer 1989). The competition among plants can be through the aboveg-
round compartments when they seek light to keep photosynthetic activity (Austin
26 C. B. Brandani et al.

et al. 1997; Hunt et al. 2006) or by belowground compartments when they are in a
limiting water and nutrient uptake environment (Boyden et al. 2005; Silva
et al. 2009).
When species in mixed plantings present contrasting traits the competitive reduc-
tion normally is expressed, which allows for a more efficient use of the site resources
through complementary niche exploitations. This condition generally occurs
through canopy and root stratification that are benefits associated to an increase in
light-use efficiency and higher soil resource (i.e., water and nutrients) uptake,
respectively (Vandermeer 1989). When two species with similar traits are mixed,
the interspecific competition may be equal to the intraspecific competition of the
same species in monoculture. However, when the species present complementary
traits, the interspecific competition may be smaller relative to the intraspecific com-
petition (Kelty 2006). The complementarity of resource uses between species is a
trait that can benefit the mixed-forest productivity, which can lead to a more effi-
cient capture of resources when compared to monocultures, as well as the reduction
of competition through the niche partitioning by stratification of the canopy of two
species (Hunt et al. 2006; Laclau et al. 2008). Thus, it may result in better soil
exploitation without stratification of the root systems of species (Laclau et al. 2013).
Facilitation typically occurs when at least one species acts positively on the other
species increasing the availability of a resource for another species, such as N2-­
fixing trees increasing the availability of organic and inorganic forms of N in the
ecosystem, through biological nitrogen fixation (BNF) (Vandermeer 1989; Forrester
et al. 2006). Thus, when a N2-fixing species is planted with non-N-fixing species, it
is possible to improve the nutritional status of the non-fixing species and to increase
the growth rates in response to transferring of biologically fixed N (Bouillet et al.
2008; Paula et al. 2015). Indirect facilitation can also happen, when the plant
changes the environment, such as the faster closure of the canopy that reduces light
availability for weeds (Little et al. 2002; Le Maire et al. 2013). Sometimes partial
shading of a fast-growing species may be beneficial to some species.
The ecological interactions (competitive reduction and facilitation) that are
favorable for the success of mixed plantations occur at the same time. However, in
practice, it becomes very difficult to distinguish one from the other. Hence, they are
collectively described as “complementarity” (Forrester 2014). This is particularly
relevant because a more efficient capture of limiting resources may alleviate
­competition and contribute to enhance above- and belowground production of the
mixed-species plantations (Forrester et al. 2006).
Therefore, the correct choice of species is highly important, which should be
based on contrasting morphological and physiological traits, especially with respect
to shade tolerance, growth rate, crown structure (i.e., leaf area density), and effec-
tive depth of the root system (Forrester et al. 2006). In addition, the spatial arrange-
ment of species has also been defined as a key strategy for the occurrence of
complementarity (Kelty 2006). Thus, the success of mixed plantations is reached
when the biomass production becomes significantly higher or at least equal to that
of monocultures (Forrester et al. 2005). When it happens, the complementarity
effects stand out from those of interspecific competition. These factors could even
2 Growth Patterns at Different Sites and Forest Management Systems 27

contribute to an overyielding effect, in which biomass production in species mix-

tures exceeds the productivity of the contributing species when grown in monocul-
ture (Bauhaus et al. 2000).

2.4.1  cological Interactions Change Throughout a Single

E
Rotation

The stress-gradient hypothesis (SGh), proposed by Bertness and Callaway (1994),

correlates the frequency of ecological interactions along a biotic or abiotic stress
gradient. The theory predicts that under conditions of low environmental stress
competition plays a more relevant role than facilitation. However, under high-stress
conditions the facilitation interactions prevail in the sense of improving the neigh-
boring habitat. This hypothesis becomes an excellent theoretical basis to explain the
behavior of mixed eucalypt plantations with legume trees, especially during a com-
plete rotation, since the balance between these interactions can be modified with the
dynamics of tree growth and environmental conditions of the site (Forrester 2014).
The complementarity index represents a measure of the occurrence of ecological
interactions favorable to the success of mixed plantations (competitive reduction
and facilitation). This index is based on the differences between the growth (or pro-
duction) at the level of the stand (Eq. (2.1)) and/or of each species (Eq. (2.2)) in the
mixed stands relative to the monocultures, according to the following equations
(Loreau and Hector 2001):

growth mix − growth mono

Complementary ( % ) = (2.1)
growth mono

 yield mix 
Complementary ( % ) =  − 1 (2.2)
 yield mono × species proportion 

where growth is expressed through diameter at breast height (DBH), in centimeters

and yield is expressed by total aboveground biomass, in Mg ha−1.
This index also allows inferring if these interactions change spatially or over
time and what are the possible factors that are controlling these changes (see also
Forrester et al. 2014).
In this chapter, we used experimental data from 5-year-old mixed and monocul-
ture stands of Eucalyptus urophylla x grandis and Acacia mangium established in
southeastern Brazil. The results revealed that complementarity interactions changed
as the stands developed (Fig. 2.4). With the advancement of age, changes in the
availability and uptake of water, light, and nutrients for the species occur. In the
E100A100 mixture, instead of the greater competition among the trees caused by
the high densification, an increase in the complementarity index was expected based
on the stress-gradient hypothesis, which presupposes that facilitative interactions
28 C. B. Brandani et al.

(A) E50A50
400 E100A100

350
Complementarity (%)
300

250

200

150

100
25 30 35 40 45 50 55 60 65

(B) Eucalyptus - E100A100

Eucalyptus - E50A50
30 Acacia - E100A100
Acacia - E50A50

20
Complementarity (%)

10

-10

-20
25 30 35 40 45 50 55 60 65
Age (months)

Fig. 2.4 Complementarity index at stand level (a) and at tree/species level (b) within the stand at
30 and 60 months after planting

increase, while the competition decreases with the increase of the abiotic/biotic
stress, and vice versa. However, the opposite occurred because, at the stand level,
complementarity decreased by almost 200% from the younger phase to the end of
rotation in the E100A100 stands.
Forrester et al. (2014) reviewed studies with mixed plantations and monocultures
using the same methodology and found results similar to the present study. These
authors consider that complementarity may decrease as nutrient availability increases,
which may explain the decrease in complementarity in the E100A100 arrangement.
Thus, at the beginning of planting, the litter stock was still incipient but, with the
advancement of age, there was larger deposition and release of nutrients through litter
decomposition, in comparison with E. urophylla × grandis monocultures.
2 Growth Patterns at Different Sites and Forest Management Systems 29

In contrast to E100A100, the E50A50 mixture showed a small increase in the

complementarity index throughout the growth cycle. This behavior demonstrates
that under this arrangement the competition between the two species was less
intense. Eucalypt at E50A50 increased its complementarity index by 20%, probably
due to the better growth conditions for this species, such as greater intraspecific
spacing and better light utilization (i.e., greater leaf area index (LAI) than acacia,
see Santos et al. (2016)). These factors may have led to increased leaf projection in
the canopy and greater growth in stem diameter of eucalypt in comparison to acacia
trees, which resulted in a greater allocation of C in the aboveground biomass
(Forrester et al. 2014). This fact may explain why 50% of eucalypt trees, planted
with 50% acacia, produced equivalent amounts of stem wood in relation to the E100
monoculture.

2.5 Aboveground Biomass

In the last decade, many studies have been carried out with different designs between
eucalypt and leguminous trees, especially with A. mangium plantations in the south-
east of Brazil (Tables 2.2 and 2.3). The following studies contributed to a better
understanding of the dynamics of aboveground biomass production, as well as the
main drivers and interactions for production responses (Balieiro et al. 2002; Coelho
et al. 2007; Laclau et al. 2008; Nouvellon et al. 2012; Bouillet et al. 2013; Laclau
et al. 2013; Le Maire et al. 2013; Epron et al. 2013; Germon et al. 2018; Santos et al.
2016; Paula et al. 2018).
Nitrogen fixed by A. mangium during the initial growth phase (up to 30 months)
has been the key to the superior performance of the mixed stands cycle/rotation in
terms of growth, stemwood biomass production, and net primary production in rela-
tion to E. urophylla x grandis monoculture (E100) (Santos et al. 2016). The mixed
stands contributed nearly 200 kg N ha−1 to the soil, almost twice that of the E100
monoculture at 60 months. This great contribution can be explained mainly by the
larger N richness of the acacia leaf litter (~17 g kg−1 for A. mangium vs. ~10 g kg−1
for E. urophylla x grandis), which corroborated the high BNF rates observed for
acacia at the beginning. This early increase in the N levels resulted in a greater
decomposition rate of eucalypt litter, as well as the biogeochemical cycling, which
persists up to the mature growth phase.
In addition, canopy stratification in mixed-species stands may increase light
interception as well as make them more productive than monocultures. However,
this complementarity niche that occurs aboveground may not lead to an increase in
stem wood biomass, if another important resource is strongly limiting tree growth.
Le Maire et al. (2013), for instance, highlighted that in the Eucalyptus grandis
W. Hill ex Maiden and Acacia mangium Willd. mixed-species plantations before
canopy closure, the N2-fixing trees allocated their assimilated C mainly to vertical
growth in an effort to compete with E. grandis trees for light, because eucalypt grew
faster in height. Thereafter, when A. mangium trees were completely dominated by
Table 2.2 Mean height, CBH, stemwood, and total aboveground biomass of harvest residues at clear cutting depending on sites (Mg ha−1)
30

Spacing 100E 100E + N 100A 25A:100E 50A:50E 50A:100E 100A:100E

(m ×
Site/age m) E E A A E Total A E Total A E Total A E Total References
Santana do 3 × 3 Height (m) 27.4 26.7 18.8 20.3 25.5 – 19.6 26.6 – 18.5 24.6 – 16.4 24.3 – Bouillet et al.
Paraiso CBH (cm) 47.8 47.6 57.0 60.3 44.6 – 57.8 52.1 – 49.7 42.2 – 39.8 41.2 – (2013)
Minas Stemwood 132.0 126.0 59.3 32.4 108.9 141.3 52.1 64.6 116.7 41.2 88.1 129.3 45.7 87.1 132.8
Gerais biomass
76 months (Mg ha−1)
Total 153.6 146.9 82.1 46.0 127.2 173.2 74.2 75.9 150.1 59.8 103.4 163.2 68.2 102.5 170.7
aboveground
biomass
(Mg ha−1)
Bofete 3×2 Height (m) 24.2 24.5 16.2 12.4 24.3 – 14.5 26.5 – 12.9 24.3 – 11.6 23.7 –
São Paulo CBH (cm) 49.4 48.8 48.0 33.0 47.9 – 42.1 56.8 – 33.4 48.4 – 26.8 46.2 –
75 months Stemwood 131.8 125.5 71.8 6.9 126.3 133.2 25.9 92.2 118.1 16.1 120.2 136.3 17.1 112.8 129.9
biomass
(Mg ha−1)
Total 173.0 165.0 123.7 12.7 165.6 178.3 42.9 148.2 191.1 29.5 157.7 187.2 32.3 147.9 180.3
aboveground
biomass
(Mg ha−1)
Luiz 3×3 Height (m) 24.9 24.4 14.1 8.6 24.3 – 11.2 26.1 – 8.5 24.7 – 8.4 24.5 –
Antonio CBH (cm) 53.4 53.3 41.2 19.4 52.8 – 27.1 65.5 – 18.3 53.0 – 18.3 52.9 –
São Paulo Stemwood 132.4 124.5 29.1 1.0 124.5 125.5 6.2 105.4 111.6 2.4 126.2 131.4 4.2 126.3 130.4
73 months biomass
(Mg ha−1)
Total 159.1 149.6 44.3 2.3 149.6 151.8 10.6 127.8 138.4 5.3 152.2 160.3 9.6 151.7 161.2
aboveground
biomass
C. B. Brandani et al.

(Mg ha−1)
 2

Itatinga 3×3 Height (m) 24.2 24.9 15.4 9.0 25.1 – 12.6 24.8 – 9.3 24.5 – 9.1 24.0 – Nouvellon
São Paulo CBH (cm) 50.7 52.3 52.3 24.0 51.9 – 39.9 61.5 – 26.0 50.9 – 23.5 50.4 – et al. (2012),
72 months Stemwood 109.2 115.2 63.0 1.9 114.9 116.9 15.2 72.7 87.9 4.5 107.7 112.2 7.8 102.1 109.9 Bouillet et al.
biomass (2013), Le
(Mg ha−1) Maire et al.
(2013)
Total 136.4 143.8 108.7 3.6 143.4 147.1 24.4 99.7 124.1 8.3 134.4 142.7 14.4 127.4 141.8
aboveground
biomass
(Mg ha−1)
Seropédica 3 × 3 Height (m) 16.4 20.6 13.7 – – – 11.0 19.9 – – – – 10.5 18.2 – Santos et al.
Rio de CBH (cm) 45.2 51.8 43.0 – – – 34.5 56.2 – – – – 32.9 45.2 – (2016)
Janeiro Stemwood 66.3 106.9 43.5 – – – 17.1 58.7 75.8 – – – 25.0 63.6 88.6
60 months biomass
(Mg ha−1)
Total 56.1 75.2 40.5 – – – 13.8 54.9 68.7 – – – 17.9 51.1 69.1
aboveground
biomass
(Mg ha−1)
Growth Patterns at Different Sites and Forest Management Systems
31
 32

Table 2.3 Mean height, CBH, stemwood, and total aboveground biomass of harvest residues at the mid of the rotation depending on sites (Mg ha−1)
Spacing 100E 100E + N 100A 25A:100E 50A:50E 50A:100E 100A:100E
Site/age (m × m) E E A A E A E Total A E A E Total References
Santana do 3×3 Height (m) 18.3 18.0 12.5 11.1 18.0 11.4 18.5 11.2 17.5 10.3 17.5 Bouillet et al. (2013)
Paraiso CBH (cm) 38.4 38.3 44.4 38.7 36.4 42.7 40.4 35.1 34.9 30.3 33.4
Minas Gerais
31 months
Bofete 3×2 Height (m) 19.7 19.4 12.4 9.2 19.3 10.9 20.0 9.1 18.8 8.7 18.6
São Paulo CBH (cm) 40.3 40.3 38.9 20.4 39.3 33.1 44.9 22.8 39.5 19.0 37.5
38 months
Luiz Antonio 3×3 Height (m) 12.1 12.1 5.5 5.4 11.8 5.9 11.4 5.3 12.0 5.5 11.3
São Paulo CBH (cm) 31.3 31.1 21.6 13.2 30.4 18.5 34.5 13.1 30.7 13.8 28.7
22 months
Itatinga 3×3 Height (m) 13.7 14.1 7.3 5.4 14.2 7.2 13.3 5.7 14.0 5.8 14.0 Laclau et al. (2008),
São Paulo CBH (cm) 35.1 36.5 36.3 15.5 35.9 28.6 40.4 16.7 35.6 16.7 35.7 Nouvellon et al. (2012),
29 months Bouillet et al. (2013), Le
Maire et al. (2013)
Seropédica 3×3 Height (m) 9.0 13.0 8.4 – – 8.0 10.0 – – 8.5 10.4 Santos et al. (2016)
Rio de Janeiro CBH (cm) 25.7 36.4 32.6 – – 33.6 28.9 – – 27.6 25.4
30 months Stemwood 12.6 31.6 13.4 – – 6.4 9.2 15.5 – – 13.2 15.6 28.9
biomass
(Mg ha−1)
Total 22.3 47.7 22.1 – – 11.07 15.6 26.6 – – 19.8 25.0 44.8
aboveground
biomass
(Mg ha−1)
C. B. Brandani et al.
2 Growth Patterns at Different Sites and Forest Management Systems 33

the E. grandis canopy, they invested relatively more biomass into their resource-­
capturing organs (i.e., leaves and fine roots) and less into stemwood production.
Finally, the authors stated that A. mangium likely suffered from greater water stress
(than in monocultures) due to competition with E. grandis trees.
Greater stemwood biomass production in mixed stands (E100A100) compared
with the monoculture (E100) can also be explained by the improved utilization of
light by two species as a function of the canopy stratification in the mixed stands
(Santos et al. 2016). In this case, E. urophylla x grandis trees occupied the upper
stratum and acacia capturing the light underutilized by E. urophylla x grandis, as
well as by the higher density of the stand. This argument is supported by the leaf
area index (LAI) of the mixed E100A100 stand in relation to that of the E100 stand,
which explains the greater biomass production of the E100A100 stand. An increase
in the leaf area index and the capture of photosynthetically active radiation (PAR) in
mixed stands were previously reported by Nouvellon et al. (2012) for stands of
E. grandis with A. mangium. The authors found that the total LAI (considering both
species) was almost twice that of the eucalypt monoculture (E100); however, the
increased LAI did not cause an increase in the gross primary production or wood
production of mixed stands compared with the monoculture, and this result was
attributed to water limitations at the site.
A net of experiments regarding replacements and additive series were replicated
in three sites in the southeast of Brazil, Bofete and Luiz Antônio in São Paulo state,
and Santana do Paraíso in Minas Gerais state (Bouillet et al. 2013). In the first years
after planting eucalypt trees had a negative effect on acacia tree growth in all sites,
as also was shown in a previous study conducted in Itatinga, located in São Paulo
state (Laclau et al. 2008). However, the interspecific competition was less in São
Paulo sites than in Minas Gerais probably because of more suitable climatic condi-
tions (temperature and precipitation) in Santana do Paraíso, Minas Gerais state, for
A. mangium development. The 50A:50E mixed stand evidenced greater eucalypt
circumference growth, 52.1 cm in Santana do Paraíso, 56.8 cm in Bofete, 65.5 cm
in Luiz Antônio, and 61.5 cm in Itatinga, respectively, compared to eucalypt in
monocultures, either non-fertilized (47.8, 49.4, 53.4, and 50.7 cm, respectively) or
fertilized with N (47.6, 48.8, 53.3, and 52.3 cm, respectively). Other replacements
and additive series along the rotation at all sites evaluated in this study also showed
greater growth for eucalypt (Tables 2.2 and 2.3). However, the eucalypt mean annual
increment in 50A:50E was lower than in the additive series (25A:100E, 50A:100E,
and 100A:100E) due to 50% less stocking density.
The same growth pattern was observed for tree growth in mixed (50A:50E and
100A:100E) and monospecific stands at Seropédica site, located in Rio de Janeiro
state (Santos et al. 2016). Acacia evidenced limited competitive ability with euca-
lypt, with minor height and circumference growth found in the replacement treat-
ments with greater density of eucalypt trees (Table 2.2). Eucalypt had a greater
circumference growth (56.2 cm) in the replacement 50A:50E stand than in mono-
cultures fertilized with nitrogen (51.8 cm). Even with a lower number of eucalypt
trees, this arrangement resulted in an overall biomass production equal or less than
the eucalypt monocultures with or without nitrogen. At both ages evaluated (30 and
34 C. B. Brandani et al.

60 months), the stemwood biomass production was lower in monocultures without

nitrogen fertilization of both species (100A and 100E). The replacements 50A:50E
and 100A:100E and eucalypt monocultures with nitrogen fertilization (100E+N)
showed the highest increases in annual net primary production in comparison with
monocultures of acacia and eucalypt.
These results showed the potential growth and productivity of the acacia and
eucalypt mixed plantations as a result of the arrangement 50A:50E that had a better
development compared to the other treatments, although with one half of the euca-
lypt population.

2.6 Belowground Biomass

Interactions occurring in the plant community root system can interfere with species
diversity through competitive exclusion, niche partitioning, and facilitation (Schenk
2006). Some experiments have shown that plant roots interact with their biotic and
abiotic environments using mechanisms that influence the availability of resources,
exchange of various types of signals, and allelochemical interactions (Callaway
2002; Hierro and Callaway 2003; Semchenko et al. 2007). Some roots may detect
other roots, or inert objects, and can distinguish between proper and non-proper
roots. This has provided new experimental challenges to evaluate the effects of root
competition on plant development (Semchenko et al. 2007). However, information
on these mechanisms controlling root growth in forest environments is very limited
(Kueffer et al. 2007), even more regarding belowground competition and fine-root
density in mixed-species forests (Silva et al. 2011).
It is very important to understand the effects of inter- and intraspecific competi-
tion on root development to improve, e.g., the control of invasive tree species, and
to model the forest dynamics (Leuschner et al. 2001; Kueffer et al. 2007) which can
contribute to recommend sustainable management practices.
As shown previously, acacia growth is expected to be suppressed by eucalypt
trees, depending on the region in Brazil (Bouillet et al. 2013; Santos et al. 2016).
The mixtures may exploit site resources more completely through the development
of a stratified canopy and soil niche separation by fine roots (Germon et al. 2018;
Laclau et al. 2013; Kelty 2006; Forrester et al. 2006). In mixed plantations, the dom-
inant species containing more fine roots, located closer to the soil surface, will have
a competitive advantage over the dominated species, excluded from the resource-­
rich upper soil layer (Laclau et al. 2013).
Soil resources are localized along a strong vertical gradient of nutrient and water
availability provided by rainfall and fertilizer application over the early growth and
then throughout the biological cycle of nutrients after canopy closure. Most of the
available nutrients are in the topsoil layer, particularly for forest plantations estab-
lished in highly weathered tropical soils and transported by gravitational solutions
(Laclau et al. 2003, 2010).
2 Growth Patterns at Different Sites and Forest Management Systems 35

Belowground competition has been studied through the dynamics of the distribu-
tion of fine roots, but other factors that play an integral part of the interactions
among species have been less studied yet, such as mycorrhizal associations (Pereira
et al. 2018), which interfere in the availability of resources with low mobility (Zobel
et al. 1997). Mixed plantation with eucalypt and acacia (50E50A) presented a sig-
nificant increase in root colonization by arbuscular mycorrhizal fungi (Glomus
genus) at the 0–20 and 20–50 cm soil layers, indicating a possible stimulation at
superficial soil layers of the symbiosis in eucalypt roots when in consortium (Pereira
et al. 2018).
Interspecific competition between E. grandis and leguminous trees (Peltophorum
dubium, Inga sp., Mimosa scabrella, Acacia polyphylla, Mimosa caesalpiniaefolia,
and Acacia mangium) was larger than intraspecific competition up to 24 months of
age (Coelho et al. 2007). The E. grandis root system distribution relative to the dis-
tribution of the M. scabrella and A. mangium roots (the most resistant leguminous
tree species to competition) in the soil profile indicated that there were different root
exploration niches between species. Laclau et al. (2008) also verified that Eucalyptus
grandis (Hill ex Maiden) and Acacia mangium (Willd.) tree roots occupied different
niches of soils when in additive or replacement stands (Fig. 2.5).
Besides the diversified soil exploitation, fine roots showed overyielding of 27%
down to 2 m of soil depth in 50A50E (445.3 g m−2), when compared with 100A
(352.0 g m−2) and 100E (346.9 g m−2) at 5 years after planting. In 50A:50E, eucalypt
fine root biomass per tree was 72% greater than in 100E, whereas the opposite was
found for acacia with fine root biomass per tree 17% lower than in 100A (Laclau
et al. 2013). After 4 years of the replanting of the same experiment conducted by
Laclau et al. (2013), total fine root biomass in 50A50E (1127 g m−2) was 44%
higher than in 100A (780 g m−2) and 58% higher than in 100E (714 g m−2) (Germon

a
4 a
b
Fine roots (t ha–1)

a
a a
3
b
ab 100A:0E
0A:100E
2 50A:100E (Ac)
b 50A:100E (Euc)
50A:50E (Ac)
1 50A:50E (Euc)
c
c b
0
6 12 18 24 30
Age (months)

Fig. 2.5 Dynamics of fine root biomass accumulation in different additive and replacement stands
between Acacia (A, Ac) and Eucalypt (E, Euc). Different letters at each age indicate significant
differences in dry matter amounts (P < 0.05). Modified figure from Laclau et al. (2008)
36 C. B. Brandani et al.

et al. 2018). These results suggest that mixing acacia and eucalypt might lead to a
strong fine root overyielding at very deep soil layers, increasing fine root explora-
tion at deep soil layers compared to their respective monospecific stands, which is
likely to enhance the uptake of soil resources. The authors found impressively
higher concentrations of fine root biomass below 2 m of soil depth, with 50, 45, and
35%, respectively, for 100E, 50A50E, and 100A.
The reduction in acacia fine root density in 50A100E (addictive stand), when
compared to the monospecific 100A0E acacia stands, in the upper soil layer at age
6–12 months after planting (Fig. 2.6), showed that belowground competition started
roughly at the same time in the 50A100E treatment, due to a strong competition
imposed by genetically improved eucalypt trees, relative to acacia (Bouillet et al.
2008), and because of the environmental conditions, cold for acacia trees. The high-
est fine root density of eucalypt in the upper soil layers occurred at 18 months of age
and subsequent decreases indicated a decrease in intraspecific competition (Silva
et al. 2011). Competition between eucalypt and acacia species occurred in the
50A100E stand through the horizontal distribution of the fine roots, with strong
decreases of acacia roots at greater distances from the tree, whereas the eucalypt
roots were not influenced by the presence of acacia. However, root competition
among species in mixed treatments shifted root growth to non-favorable depths. The
monospecific stands explored the soil similarly (Silva et al. 2011).
Whatever the tree stock density of eucalypt (50A100E vs. 50A50E), all authors
reported a competitive exclusion of acacia fine roots from the upper soil layer
(Laclau et al. 2013; Germon et al. 2018; Silva et al. 2009). According to Silva et al.
(2009) and Laclau et al. (2013), the facilitation processes were weak because of the
lack of aboveground transgressive overyielding in 50A50E (when the consortium
production is greater than the most productive monoculture). Other factors involve
the lack of influence of acacia trees on eucalypt distribution of fine roots in 50A:100E
stands, besides N concentrations in eucalypt tree components, which were not sig-
nificantly different from those of the 100E and 50A100E stand (Bouillet et al. 2008).
However, in general, increases in soil N availability in mixed plantations of eucalypt
trees planted with acacia (Tchichelle et al. 2017; Voigtlaender et al. 2012) explained
the greater soil exploration by eucalypt fine roots in 50A:50E relative to 100E stands
(Germon et al. 2018).
In this context, the recommendation is that comparative studies should be carried
out mostly in areas highly depleted in N, where acacia trees should improve the
growth of eucalypt trees through complementarity and facilitation mechanisms
(Laclau et al. 2013).

2.7 Final Remarks

In this chapter we showed that mixed eucalypt plantations with acacia can increase
biomass production in relation to eucalypt monocultures, especially in highly
weathered soils (that are especially very poor in N) and with climatic conditions
 2 Growth Patterns at Different Sites and Forest Management Systems 37

Acacia mangium Eucalyptus grandis

Fine root density (g dm-3)

A B
0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6

100A : 0E (P1) 0A :100E (P1)

C D
0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6
Depth (cm)

50A :100E (P4) 50A :100E (P4)

E F
0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6

6 months
12 months
18 months
30 months
50A :100E (P1) 50A :100E (P1)

Fig. 2.6 Fine root densities according to their sampling position in the planting row: P1 position
in 100A:0E close to A. mangium trees (a); P1 position in 0A:100E close to E. grandis trees (b); A.
mangium fine roots in the P4 position in 50A:100E, close to A. mangium trees (c); E. grandis fine
roots in the P4 position in 50A:100E, close to A. mangium trees (d); A. mangium fine roots in the
P1 position in 50A:100E, close to E. grandis trees (e); and E. grandis fine roots in the P1 position
in 50A:100E, close to E. grandis trees (f). The horizontal bars show the LSD values when the dif-
ferences between treatments were significant (P < 0.05)
38 C. B. Brandani et al.

favorable to acacia (average annual temperatures higher than 24 °C and annual rain-
fall above 1000 mm). In mixed plantations, Acacia mangium can compete with
eucalypt on equal terms or at least similar growth rates. However, for the facilitation
process to occur between both species, it is necessary to develop strategic programs
of A. mangium breeding similar to those developed for eucalypt in the last years.
Further studies should be developed to evaluate different spacing or planting
arrangements that minimize interspecific competition in mixed plantations and,
consequently, promote better growth and biomass production. For example, plant-
ing trees of each species in double lines instead of alternating plants could not only
decrease the competition of eucalypt over acacia, but also facilitate the harvesting
of trees. In addition, other questions should be answered to foster the understanding
of mixed plantations in tropical conditions, such as the following: (1) What are the
silvicultural practices (e.g., thinning, pruning, complementary fertilization) to
ensure greater productivity? (2) Are there other legume tree species, specially native
from Brazil, with productive potential that could be evaluated in the mixed planting
system with eucalypt?
It is important to note that, in addition to the positive responses on growth and
biomass production, mixed plantations can also result in several indirect benefits
that can improve the long-term sustainability of the production system, such as
increase in soil C sequestration, increase in soil N concentrations which will impact
directly the dynamics of nutrient cycling, and increase in biodiversity and protec-
tion against pests and diseases, besides creating the diversification of timber and
non-timber forest products, which are discussed in several chapters in this book.

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63 meses de idade, no Vale do Rio Doce-MG. Revista Árvore 20(3):299–308
Silva EV, Gonçalves JLM, Coelho SR, Moreira RM, Mello SLM, Bouillet J-P, Jourdan C, Laclau
J-P (2009) Dynamics of fine root distribution after establishment of monospecific and mixed-­
species plantations of Eucalyptus grandis and Acacia mangium. Plant Soil 325:305–318.
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79(1):1–8. https://doi.org/10.2989/20702620.2016.1221702
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Chapter 3
Nutrient Cycling in Mixed-Forest
Plantations

José Henrique Tertulino Rocha, José Leonardo de Moraes Gonçalves ,

and Alexandre de Vicente Ferraz

3.1 Introduction

Nutrient cycling in forests was defined by Attiwill and Adams 1993 as the range of
natural processes that govern the availability of nutrients for the forest trees, as well
as the interactions between plants and soil in the uptake and return of nutrients,
microbial interactions in which nutrients are transformed between organic and inor-
ganic forms, and balance between input and output of nutrients. Thus, nutrient
cycling is a term used to cover all the pathways and processes by which nutrients
enter, leave, and move within forest ecosystems.
In planted or managed natural forest for wood production the nutrient cycle is
open once a large amount of nutrients is removed with harvest and in some places
large amounts of nutrients are applied through fertilizers. The magnitude of the
nutrient output and, consequently, the dependence on fertilizer application increase
with the management intensity. In Brazil, most of the wood consumed and exported
comes from planted forest managed in short rotation (5–7 years) with high produc-
tivity (from 20 to 80 m3 ha−1 year−1). The main genus planted is Eucalyptus. This
system of production is highly efficient and highly productive, but highly dependent
on fertilizer application. This dependency is intensified because of highly weathered
soils, poor in nutrients or plantation established at steep sites susceptive to soil
­erosion. As commented in other chapters an alternative to reduce the dependence of
fertilizer is the introduction of nitrogen-fixing trees (NFT) into eucalypt plantations.

J. H. T. Rocha (*)
Agriculture and Forest Engineering College (FAEF), Garça, SP, Brazil
J. L. M. Gonçalves
Department of Forest Sciences, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
A. V. Ferraz
Institute of Forest Science and Research (IPEF), Piracicaba, SP, Brazil

© Springer Nature Switzerland AG 2020 45

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_3
46 J. H. T. Rocha et al.

In natural ecosystems, the wood productivity is lower and there is no dependence on

fertilizer application; on the other hand, in eucalypt plantation, the high wood produc-
tivity increases the dependence in terms of fertilizer application. As ­suggested in this
book, perhaps the sustainable alternative is somewhere in between the natural forest
and the traditional monospecific eucalypt plantation. Thus, the main goal of this chap-
ter is to compare the nutrient cycling in mixed forest (mainly Acacia with Eucalyptus)
with monospecific plantation and natural forest (Atlantic Forest and Cerrado—
Brazilian savannah). Nutrient cycling can be divided into six main stages, as suggested
by Attiwill and Adams (1993). They are (1) inputs of nutrients by rain, dust, biological
fixation, and parental rock weathering; (2) uptake and accumulation of nutrients by
trees; (3) outputs of nutrients by leaching and gaseous forms and in harvested material;
(4) internal redistribution of nutrients within and among plants; (5) return of nutrients
from plant to soil; and (6) decomposition of the forest floor and nutrient mineralization.
Some of these subjects are presented in more details in Chaps. 4 and 6.

3.2 Nutrient Inputs

In tropical planted forest, fertilizer application is frequently the main nutrient input
into the system, but atmospheric deposition, biological N2 fixation, and parental
rock weathering can also play an important role. Biological N2 fixation (BNF) is
discussed in another chapter. In this chapter, we discuss the role of atmospheric
deposition and parental rock weathering.

3.2.1 Atmospheric Deposition

In forest plantations the importance of atmospheric deposition increases with the

annual deposition rate and with the length of the rotation (Ranger and Turpault
1999; du Toit et al. 2014). The main sources of nutrients contributing to atmospheric
deposition are mineral and marine aerosols, wildfires, industrial activity, combus-
tion of fossil fuel, and agricultural activity (Wieder et al. 2016; Lequy et al. 2014;
Nyaga et al. 2013).
The amount of nutrients deposited is highly dependent on the source, and highly
variable in the spatial and temporal scale. In the literature, we found references to
annual depositions of N, P, K, Ca, Mg, and S ranging from 1 to 10, 0.1 to 5, 1 to 25,
1 to 30, 0.3 to 3, and 1 to 10 kg ha−1 year−1, respectively (Table 3.1). The deposition
reduced exponentially with the distance from the emission center. Unlike N and S
deposition, the K, Ca, and Mg depositions occur more concentrated around the
emission center (Wieder et al. 2016; Nyaga et al. 2013). Wieder et al. (2016) found
small Ca and Mg deposition rates 69 km from the emission center, while for N and
S a small deposition rate was present even in the most distantly assessed point
(251 km).
3 Nutrient Cycling in Mixed-Forest Plantations 47

Table 3.1 Nutrient deposition by rainfall (kg ha−1 year−1)

Location N P K Ca Mg S Source
Alberta, Canada 1.2 0.1 9.0 2.0 5.0 Wieder et al. (2016)
Northeastern France 0.5 1.1 0.8 0.3 Lequy et al. (2014)
West coast of South Africa 3.9 0.1 3.0 15 5 Nyaga et al. (2013)
São Paulo, Brazil 4.1 3.6 9.3 1.5 Laclau et al. (2010)
Kondi, Congo 5.4 6.2 7.3 3.1 Laclau et al. (2010)
São Paulo, Brazil 4.2 4.4 7.4 2 Vital et al. (1999)
Rio de Janeiro, Brazil 15.5 de Souza et al. (2017)
Average 3.8 0.2 3.7 8.1 2.3 5.0

3.2.2 Rock Weathering

Rock weathering rates are difficult to be quantified and frequently low in relation to
the rotation scale. Many methods have been proposed, and despite the good rela-
tionship among the results, the accuracy of absolute data is uncertain (Hodson and
Langan 1999; Klaminder et al. 2011; Koseva et al. 2010; Ouimet and Duchesne
2005; Whitfield et al. 2006, 2011). Generally, in highly weathered soils, with low
levels of primary minerals, nutrient inputs by weathering are effectively negligible
(Melo et al. 2005).
In young and shallow soils, rich in primary minerals and where trees are grown
in long rotations, this nutrient input can be important for nutrient supply to the
stand. Starr and Lindroos (2006) assessed the rate of Ca and Mg released by weath-
ering in a soil chronosequence ranging from 340 to 5279 years of age in Finland
with the same parent material under Pinus sylvestris forests. They found releases of
around 2.0 and 0.6 kg ha−1 year−1 of Ca and Mg, respectively, in the youngest soil,
and releases of 0.4 and 0.2 kg ha−1 year−1 of Ca and Mg in older soil. There was a
drastic reduction in the Ca and Mg release up to soil ages of 1000 years followed by
stabilization thereafter. Under an 80-year-old P. sylvestris forest in Finland, Starr
et al. (2014) found weathering rates (1.8, 0.5, and 0.7 kg ha−1 year−1 of Ca, Mg, and
K, respectively) which almost equaled the leaching rate. They reported that the
quantities of exchangeable cations at the 0–40 cm soil layer are equivalent to
approximately 30 years of weathering and the quantities accumulated in the aboveg-
round biomass are equivalent to almost 50 years of weathering. These data sets
indicate that in some sites weathering on its own is sufficient to supply the K, Ca,
and Mg requirements of the trees. However, in Oxisols in tropical climate, the
release of K, Ca, and Mg is very close to zero (Melo et al. 2005).

3.3 Nutrient Uptake and Accumulation

The nutrient uptake and consequent accumulation in the biomass are linearly related
with the growth rate in planted forest, but are also related with the site nutrient avail-
ability (Gonçalves et al. 2014; Rocha et al. 2019). In natural unmanaged forest on
48 J. H. T. Rocha et al.

steady state, the uptake rate is equal to the nutrient return to soil and the amount of
nutrients accumulated in the biomass is proportional to the biomass stock.
The amount of nutrients accumulated in the biomass is equally affected by the
species composition. Santos et al. (2017), comparing mixed-species and monospe-
cific plantations of Acacia mangium and Eucalyptus (hybrid between E. urophylla
and E. grandis), found 354 t ha−1 of aboveground biomass and 268 kg ha−1 of N
accumulated in this biomass in monospecific eucalypt at 5-year-old stands. At the
same site and age, these authors found, in the monospecific acacia plantation,
107 t ha−1 of aboveground biomass and 186 kg ha−1 of N accumulated. The overall
N concentration of the aboveground biomass of eucalypt was 2.19 g kg−1 and of
acacia was 2.44 g kg−1. If the productivity of both stands were the same, the N accu-
mulation in the acacia aboveground biomass would be 11% bigger than in the euca-
lypt plantation. When we look at the overall P concentration in the aboveground
biomass for the same productivity, the eucalypt monospecific plantation accumu-
lates around 33% less P than acacia monospecific plantation. Due to genetic differ-
ences among the species, when we mix acacia and eucalypt in a plantation, there is
an increase in the N, P, K, Ca, and Mg content per ton of biomass produced (Santos
et al. 2017).
The mixture of A. mangium with Eucalyptus plantation increases the fine root
biomass and consequently the soil exploration, especially in deep soil layers (see
also Chap. 2). Germon et al. (2018) studying soil exploration by fine roots down to
a depth of 17 m found an increase of 58% in the root biomass when eucalypt was
mixed with acacia (50%E 50%A), when compared with monospecific Eucalypt
plantation. Beyond the root biomass, they also found an increase of 50% in the root
specific area (cm2 g−1) of acacia in mixed plantations when compared with acacia in
monospecific plantation. In this study, the root of eucalypt dominated the upper soil
layer and “forced” acacia to increase the root density in deeper soil layers. The root
front of the monospecific acacia plantation was down to 12 m while under mixed
plantation acacia roots reached 17 m.

3.4 Nutrient Outputs

The harvest output increased linearly with stand productivity and with harvest
intensity. Rocha et al. (2019), based on 45 stands, estimated the nutrient harvest
output for three levels of productivity and two levels of harvest intensity for mono-
specific eucalypt plantations (Table 3.2). Santos et al. (2017) assessed the harvest
outputs of 5-year-old monospecific and mixed plantations of eucalypt with acacia in
Rio de Janeiro state, Brazil. The productivity of plantations was 110, 50, and
80 t ha−1 of stem wood, when comparing monospecific eucalypt, acacia, and mixed
plantation, respectively. The nutrient harvest outputs of the monospecific eucalypt
plantation were higher than those in the mixed plantation due to the higher produc-
tivity (Table 3.3).
3 Nutrient Cycling in Mixed-Forest Plantations 49

Table 3.2 Nutrient outputs by harvestinga in eucalypt plantations (with and without bark) in
rotations of 7 years and mean annual increment (MAI) ranging from 30 to 50 m3 ha−1 year−1
MAI (m3 ha−1 year−1)
30 40 50
Nutrient kg ha-1
Wood with bark
N 198 264 330
P 41 54 67
K 116 155 194
Ca 202 270 338
Mg 23 31 39
S 37 49 61
Wood
N 168 224 280
P 32 42 53
K 66 88 110
Ca 83 110 138
Mg 12 16 20
S 34 45 56
a
Adapted from Rocha et al. (2019)

Table 3.3 Biomass and nutrient outputsa by harvest of a monospecific eucalypt plantation (hybrid
between E. urophylla and E. grandis—100E), a monospecific Acacia mangium plantation (100A),
and a mixed eucalypt with acacia plantation (50E50A), all 5 years old, harvested in the system of
only stem and full tree
Stem Full tree
Biomass/nutrient 100E 100A 50E50A 100E 100A 50E50A
Biomass (t ha−1) 110 50 80 123 63 95
N (kg ha−1) 120 62 92 269 187 232
P (kg ha−1) 13 10 12 23 23 24
K (kg ha−1) 98 43 74 189 135 165
Ca (kg ha−1) 84 56 76 130 125 137
Mg (kg ha−1) 19 13 17 40 39 41
a
Adapted from Santos et al. (2017)

Beyond harvest outputs, other nutrient losses can be significant in forest planta-
tion. The soil loss by erosion under eucalypt plantation managed by minimum
­tillage is low, ranging from 0 to 2 t ha−1 year−1 and being influenced by the age and
management of the plantation (Martins et al. 2003; Silva et al. 2011). The soil loss
under acacia plantation is also low, around 1 t ha−1 year−1 (Barros et al. 2009). Due
to the depth of the root system and the low deep-water drainage, nutrient leaching
under forest plantation is negligible (Laclau et al. 2013; Christina et al. 2017).
Ammonia volatilization in forest plantations in Brazil is also negligible, because
these plantations are established normally on acidic soils.
50 J. H. T. Rocha et al.

3.5 Nutrient Redistribution Within and Among Plants

Nutrient redistribution or biochemical nutrient cycling is a well-known process in

deciduous trees as well as in evergreen trees. The nutrients differ greatly in their
mobility. Calcium, for example, is considered immobile, because it is a structural
element, while K is highly mobile due to being a nonstructural element.
Some authors found that under conditions of high nutrient availability, the retrans-
location tends to be reduced (Boerner 1984; Pugnaire and Chapin 1993; Andrews
et al. 1999), but others found no nutrient retranslocation (Millard and Proe 1993).
Among species, the N retranslocation rate is higher in eucalypt trees, K and P
retranslocation rate is higher in acacia trees, and the Mg retranslocation rate is equal
in both species (Santos et al. 2017). These authors found no difference in the retrans-
location rate of both species, when comparing mixed with monospecific plantations.
Since the K and P retranslocation rates are higher in acacia trees, the introduction of
this species in monospecific eucalypt plantations can increase the nutrient retranslo-
cation (Table 3.4).
Beyond the nutrient retranslocation within the trees, the nutrient retranslocation
among trees can play an important role in the nutrition of mixed plantations, espe-
cially when there are NFTs. Paula et al. (2015), using 15N, found transference from
acacia to eucalypt trees 5 days after application among trees 6 m away from each
other in a mixed plantation located in Itatinga, Brazil. These authors concluded that
the transference belowground may provide a significant amount of N requirement of
the tree close to NFT. This transference may be direct, when roots of eucalypt and
acacia are connected by mycorrhizal network, or indirect, by root exudation of N
compounds (See also Chap. 6).

3.6 Return of Nutrients from Plants to Soil

Monospecific eucalypt plantation returns to soil on average 5.6 t ha−1 year−1 of litter
(Table 3.5). The litterfall rate normally increases until 3 to 4 years of age and stabi-
lizes or shows a little reduction afterwards (Rocha 2017). This litterfall rate results
in a return to the soil of around 45, 2, 16, 40, 12, and 5 kg ha−1 year−1 of N, P, K, Ca,
Mg, and S, respectively. When compared with the native Atlantic Forest these
amounts are markedly lower, especially for the nutrients, which indicates a lower
nutrient concentration in the eucalypt litterfall (Table 3.5).
In mixed plantations, there is an increase in the total amount of nutrients d­ eposited
on the soil, especially N and P. This higher nutrient deposition is a result of higher
nutrient concentration in the litter and of a higher litterfall rate (Table 3.5). These
findings indicate that the introduction of acacia into monospecific eucalypt planta-
tion accelerates and increases the nutrient cycling as also evidenced by Binkley
(1992) and Forrester et al. (2005).
3 Nutrient Cycling in Mixed-Forest Plantations 51

Table 3.4 Nutrient retranslocation ratea of Eucalyptus (hybrid between E. urophylla and E.
grandis) and Acacia mangium trees at 30 and 60 months after planting
N P K Mg
Age (month) %
Eucalyptus
30 77 68 61 34
60 51 70 70 43
A. mangium
30 62 84 74 46
60 45 83 81 37
Adapted from Santos et al. (2017)
a

Table 3.5 Litterfall rate and amount of nutrients deposited on the soil by litterfall in monospecific
eucalypt plantation, Natural Forests, and in a trial which compares monospecific eucalypt
plantation (100% eucalypt) with mixed-species plantation (50% eucalypt, 50% acacia)
Age Mass N P K Ca Mg S
Species (year) (t ha−1 year−1) kg ha−1 year-1 Source a
Monospecific eucalypt plantation
E. grandis 1–9 5.6c (3.8–7.8) 44.0 1.9 15.8 39.4 11.7 4.9 1, 2, 3,
and [14] (24.0– (0.9– (4.4– (11.2– (7.0– (2.5– 4, 5, 6,
hybridb 83.5) 5.1) 44.2) 84.0) 16.2) 8.1) 7, and 8
[14] [14] [14] [14] [13] [6]
Eucalypt with acacia trials
100% 2–6 8.5 (5.0–11.5) 49.5 5.3 15.6 30.0 8.8 [1] – 9, 10,
Eucalypt [8] (30.0– (1.8– [1] [1] 11, and
62.0) 8.8) 12
[8] [4]
50% 2–6 8.7 (6.1–11.0) 70.7 6.2 18.8 33.2 9.0 [1] – 9, 10,
Eucalypt [8] (63.0– (1.7– [1] [1] 11, and
50% 80.0) 10.7) 12
Acacia [8] [4]
Natural Forest
Atlantic Forest 9.1 (6.3–13.0) 169.6 5.9 44.3 148.2 25.8 13.6 6, 13,
[10] (122– (1.6– (11.7– (88.9– (11.0– (13.5– 14, 15,
218.9) 11.6) 67.7) 231.1) 38.7) 13.6) 16, 17,
[10] [10] [10] [9] [9] [2] 18, and
19
Cerrado 3,8 (2,1–7,8) 34.4 2.1 6.3 14.6 5.2 0.7 19 and
[4] (12.7– (0.4– (2.3– (4.7– (1.9– [1] 20
64.7) 4.7) 12.5) 26.5) 10.9)
[4] [4] [4] [4] [4]
a
1—Gonçalves et al. (2000), 2—Zaia and Gama-Rodrigues (2004), 3—Cunha et al. (2005), 4—
Ferraz (2009), 5—Silva (2006), 6—Gama-Rodrigues and Barros (2002), 7—Silva et al. (2013),
8—Rocha (2017), 9—Voigtlaender et al. (2019), 10—Koutika et al. (2014), 11—Santos et al.
(2016), 12—Santos et al. (2017), 13—Vital et al. (2004), 14—Pinto et al. (2009), 15—Pimenta
et al. (2011), 16—Godinho et al. (2013), 17—Domingos et al. (1997), 18—Pereira et al. (2008),
19—Toledo et al. (2002), 20—Nardoto et al. (2006)
b
Hybrid between E. grandis and E. urophylla
c
Average, followed by the amplitude between parentheses and followed by the number of sites plus
the number of years assessed between brackets
52 J. H. T. Rocha et al.

Table 3.6 Litterfall, litter layer, decomposition rate (k), half lifetime, and decomposition time of
95% of the litter in monospecific eucalypt plantation and in Natural Forests
Litterfall Decomposition time
Age Layer 50% 95%
Species (year) t ha−1 year−1 (t ha−1) k year Sourcea
Monospecific eucalypt plantation
E. grandis 1-9 5.6b 11.6 0.63 1.46 6,31 1, 2, 3, 4,
and hybridb (3.8–7.8) (3.9– (0.23– (0.58– (2,50– and 5
[10] 23.7) [10] 1.2) [10] 2.97) [10] 12,84)
[10]
Natural Forest
Atlantic Forest 8.5 6.0 1.53 0.49 2.10 5, 6, 7, 8,
(6.3–10,6) (3.4– (0.93– (0.28– (1.22– 9, and 10
[8] 10.1) [8] 2.45) [8] 0.74) [8] 3.22) [8]
a
1—Zaia and Gama-Rodrigues (2004), 2—Cunha et al. (2005), 3—Ferraz (2009), 4—Gonçalves
et al. (2000), 5—Gama-Rodrigues and Barros (2002), 6—Vital et al. (2004), 7—Morellato (1992);
8—Pinto et al. (2009), 9—Pimenta et al. (2011), 10—Godinho et al. (2013)
b
Average, followed by the amplitude between parentheses and followed by the number of sites plus
the number of years assessed between brackets

3.7 Decomposition of Forest Litter

We will discuss litter layer decomposition in detail in the next chapter. In this topic,
we will be comparing only the litter decomposition in eucalypt stands with the
­natural vegetation. Under monospecific eucalypt plantation the litterfall and litter
layer rates are around 5.5 t ha−1 year−1 and 11.6 t ha−1, and, under Atlantic Forest,
8.6 t ha−1 year−1 and 6.0 t ha−1, respectively. The decomposition rate (k) of the
Atlantic Forest litter is 2.4 times greater than the k of eucalypt plantation (Table 3.6).
When NFTs are mixed with eucalypt despite an increase in the litter N and P
concentration and a reduction in the concentration of phenol, the k does not neces-
sarily increase (Bachega et al. 2016). A large increase in the N mineralization under
NFT in monospecific or mixed plantations was detected (Voigtlaender et al. 2012,
2019). On the other hand, as discussed in Chap. 4, changes in decomposition rates
could be site specific.

3.8 Conclusion

The introduction of NFT, such as Acacia mangium, at monospecific eucalypt stands

can improve the capacity of the trees in obtaining nutrients, mainly due to the atmo-
spheric N2 fixation and by the wider soil exploration. The NFT also accelerates and
increases nutrient cycling and contributes to a large return of nutrients to soil by
litterfall, increasing the topsoil nutrient availability. The N mineralization increases
greatly. Thus, the dependence of mixed plantations on nitrogen fertilizer application
is lower. More studies need to be incentivized, encompassing other NFT species.
3 Nutrient Cycling in Mixed-Forest Plantations 53

The concentration of some nutrients in the acacia biomass is higher than that in
eucalypt biomass. If mixed plantations reach the same productivity of monospecific
eucalypt plantation, an increase in the nutrient harvest output can occur.

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Chapter 4
Litter Decomposition and Soil Carbon
Stocks in Mixed Plantations of Eucalyptus
spp. and Nitrogen-Fixing Trees

Fabiano de Carvalho Balieiro , Fernando Vieira Cesário,

and Felipe Martini Santos

4.1 Introduction

Increased demand for forest products around the world has contributed to the growth
of planted forest areas over the last few decades (FAO 2015). The annual growth
rate of planted forests in the tropics has been 2.5% per year, corresponding to an
increase of around 20 million hectares from 1990 to 2015 (Payn et al. 2015). In
Brazil, the planted forest generates and offers a huge diversity of products, ­especially
pulp, paper, charcoal, sawn wood, and plywood, among others. Brazil c­ urrently has
7.84 million hectares of planted trees and its planted tree industry is responsible for
91% of the wood produced for industrial purposes in the country and 6.2% of the
Brazilian gross domestic product; it is one of the industries with the greatest poten-
tial to help build a green economy (IBA 2017). Most of these planted forests are
monocultures of Eucalyptus spp. (72%) and Pinus spp. (20%), but other species can
also attend the internal and external market, such as Acacia mangium and Acacia
mearnsii that together occupy 2.0% of the planted forest area. Other species include
Hevea brasiliensis (2.9%), Schizolobium amazonicun (1.1%), and Tectona grandis
(1.1%) (IBA 2017).
Despite the success of the Brazilian forestry agribusiness, most of these forest
plantations occupy extensive areas of marginal soils, previously managed soils
with low fertility or at some stage of degradation (Gonçalves et al. 2013). The sus-

F. de Carvalho Balieiro (*)

EMBRAPA Soils, Brazilian Agricultural Research Corporation, Rio de Janeiro, RJ, Brazil
e-mail: fabiano.balieiro@embrapa.br
F. V. Cesário
Fluminense Federal University, Niterói, RJ, Brazil
F. M. Santos
Federal Rural University of Rio de Janeiro, Seropédica, RJ, Brazil

© Springer Nature Switzerland AG 2020 57

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_4
58 F. de Carvalho Balieiro et al.

tainability of these plantations could be compromised in the medium and long

terms, because they have been managed under short rotations and a fertilization
regime, often far from high nutrient exports due to timber harvests, especially for
P, K, and N (Santana et al. 2008; Laclau et al. 2010; Bouillet et al. 2013; Gonçalves
et al. 2013).
Soil organic matter (SOM) in tropical planted or native forests has many func-
tions that affect soil properties and processes. It plays a role of the nutrient reserve,
and energy source for animals, plants, and microorganisms since its soil minerals
are not great suppliers of mineral nutrients due to the high degree of weathering
(Sanchez 1979; Maquere et al. 2008; Quesada et al. 2010). In addition, SOM fea-
tures the greatest cation exchange capacity (CEC) of these soils (Senesi and
Loffredo 1999; Oorts et al. 2000; Motta et al. 2002), which prevents essential nutri-
ents from being easily lost by leaching and, consequently, not utilized by forests.
Instead, the SOM allows such nutrients to be exchanged easily with the soil solution
and to be taken up by plants. SOM participates in soil aggregation and consequently
in soil pore space formation (Tisdall and Oades 1982; Denef et al. 2001; Denef and
Six 2005). With an expressive and balanced pore space (i.e., macro- and micro-
pores) the roots exploit the soil profile much better, water infiltration is facilitated,
and plants get benefit from increased soil water storage (Doran and Parkin 1994;
Franzluebbers 2002).
Poorly managed planted forests stimulate decomposition of SOM and C loss.
This poor management includes excessive use of machines, with high traffic inten-
sity in soil preparation or harvesting, in addition to removing or burning crop
­residues from the harvested area and excessive soil disturbance during preparation,
which comprises the provision of numerous soil ecosystem services and the sustain-
ability of these forests (Chaer and Tótola 2007; Dominati et al. 2010; Gonçalves
et al. 2013; Jesus et al. 2015; and Chap. 10).
The rates of SOM and litter decomposition are clearly influenced by many
­factors, including temperature, air humidity, soil moisture content, soil microbial
community, and litter quality. The last one may be described by lignin, polyphe-
nols, carbon, and nutrient concentrations (especially N and P) or ratios of these
(Attiwill and Adams 1993; Hättenschwiler et al. 2011). The N2-fixing species often
have higher N concentrations and decompose more rapidly. Thus, mixtures of
Eucalyptus litter with more readily decomposable and more nutrient-rich litter
may enhance the litter decomposition rates (Briones and Ineson 1996). Gartner and
Cardon (2004) in a meta-analysis found synergistic effects in the majority of
mixed-litter decomposition studies (47.5%), while antagonistic effects (19.1%)
were less frequent. However, some expected improvements due to the introduction
of N2-fixing trees in litter decomposition, such as microbial activity and nutrient
release (especially N), seem to be conditioned by the structural quality of the resi-
dues, the N:P ratio of litter, and the integration with microorganisms, driven by the
increase in diversity of the plant community (Forrester et al. 2006; Rachid et al.
2015; Santos et al. 2018).
This chapter presents and discusses some data about changes in key soil pro-
cesses, litter decomposition, and C stabilization (i.e., humification) arising from the
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 59

introduction of N2-fixing legumes in mixed Eucalyptus spp. plantations. We must

emphasize the dynamics of C in tropical soils, especially Brazilian soils, and of the
understanding of the main drivers of C stock in mixed-forest soil. Many researchers
believe that one of the legacies of mixed plantations is the increase of soil C stocks,
and at the end of this chapter, some of the practices and challenges to overcome
obstacles of C storage will be introduced.

4.2  arbon Assimilation and Partitioning in Forest

C
Plantation

Understandings of carbon dynamics in forests involve knowledge of the biotic and

abiotic factors that interfere in the growth of species that colonize a particular site,
as well as where assimilated C is allocated (Cannell 1989; Davidson and Hirsch
2001). According to Cannell (1989), the CO2 conversion efficiency in forest
­biomass is variable and associated with factors such as earth geometry, geographic
location of the plantations, CO2 diffusion rate for chloroplasts, canopy interception
capacity (Io), respiration rate, and proportion of the different aboveground tree
compartments.
Carbon accumulation in a forest occurs in several aboveground and belowground
compartments. In the case of woody tissues such as stem, thick roots, and branches,
this accumulation may last for years or decades. On the other hand, in labile tissues
such as leaves, flowers, and fine roots, after the senescence C will return to the
atmosphere in days or weeks via decomposition (Landsberg and Gower 1997;
Fearnside 2000; Schlesinger and Lichter 2001; Nouvellon et al. 2012; Bachega
et al. 2016).
In general, about half of all CO2 annually fixed in terrestrial biomass via photo-
synthesis (~120 Pg C y−1) is respired by plants (~60 Pg C y−1) and the other half is
respired heterotrophically (Janzen 2004). In other words, if not disturbed, the C
reservoirs shall remain constant in these environments, including the soil compart-
ment. Because soil is the largest active C compartment of the terrestrial ecosystem
(~1500–2000 Pg) and is in direct connection with other environmental components
(i.e., atmosphere, hydrosphere, pedosphere, and biosphere), land use and climate
changes have led to the loss of soil capacity to provide varied ecosystem services
associated to SOM loss.
The net primary production (NPP) of forests increases with the reduction of lati-
tude because there is a higher incidence of global radiation, higher evapotranspira-
tion, and, consequently, higher cloud formation and rainfall in tropical regions
(Ometto 1981). Reducing the vapor saturation deficit in these regions increases sto-
matal conductance and rate of carbon fixation of plant species (Sands and Mulligan
1990; Novais and Barros 1997; Whitehead 1998). Recent papers with Eucalyptus in
Brazil have shown that NPP of the genus is determined preferentially by local water
60 F. de Carvalho Balieiro et al.

availability and, to a lesser extent, by soil fertility (Reis et al. 1985; Stape et al.
2004, 2010; Rigatto et al. 2005; Balieiro et al. 2008). The importance of water
supply for Eucalyptus grandis and E. urophylla was highlighted by Stape et al.
(2004), when evaluating 14 sites with a significant productivity gradient
(9.7–39.1 Mg ha−1 year−1). According to the authors, the NPP of the sites with
­intermediate productivity (i.e., average of 16 Mg ha−1 year−1) was 46% higher than
NPP of the sites with low productivity (i.e., average of 11.9 Mg ha−1 year−1), where
32% of this variation was related to the site of water supply. Although the productiv-
ity difference between the high and medium productivity sites was 72%, one-third
of this difference was related to the availability of soil water.
Similarly, when measured by the average monthly increment of the stem, the
productivity of eucalypt was directly related to precipitation in the Rio Doce
Basin, in Minas Gerais (Souza et al. 2006). According to the authors, for each
increase of 100 mm in the total precipitation within a year, there was an average
increase of 0.45 m3 ha−1 month−1, while 100 mm reduction affects this increase in
0.64 m3 ha−1 month−1. Rigatto et al. (2005) also found very high correlations
between the height of Pinus taeda plants and the available water in eight different
forest sites. Stape et al. (2010) across a large edaphoclimatic gradient (~1000 km)
and eight regions found that fertilization beyond the current operational rates did
not increase the growth of clonal Eucalyptus plantations, whereas irrigation raised
growth about 30% (to 30.6 Mg ha−1 year−1).
At mixed-forest plantations in Brazilian and Congolese conditions, where the set
of trials with Eucalyptus and Acacia mangium (Acacia) were developed, the com-
plementary interactions in the mixed stands of acacia and eucalypt led to significant
biomass production. However, the NPP was higher than in monocultures without N
fertilization only where appropriate climate conditions (i.e., temperature, high
humidity, and rainfall) for Acacia and poor soil occur (Bouillet et al. 2013; Santos
et al. 2016; Voigtlaender et al. 2019). Under milder and drier climate, Acacia cannot
compete with Eucalyptus. For E50:A50 arrangement, and comparing six different
sites (five in Brazil and one in Congo), Santos et al. (2016) after Bouillet et al.
(2013) found that stemwood production only exceeded E100 ones at the Congo and
Seropédica sites, although the differences in both studies were not significant at the
5% level (Santos et al. 2016).
Using the C budget approach to quantify growth, C uptake, and C partitioning in
pure and mixed plantations with the same stocking density of E. grandis and A. man-
gium plantations, Nouvellon et al. (2012) developed an interesting work with C
allocation of mixed plantation in São Paulo state. According to the results, the pro-
duction in mixed plantation is lower than in Eucalyptus due to the lower gross pri-
mary production and net primary production values, as well as shifts in C allocation
from above- to belowground and from growth to litter production. However, the
pattern seems to be site specific due to the two contrasting tropical site environ-
ments (i.e., Brazilian and Congolese). Epron et al. (2013) compared Brazilian and
Congolese site, and found that mixed-species plantations at the Brazilian site had a
lower stand of wood biomass and aboveground net primary production (ANPP)
without change in total belowground C fluxes (TBCF). In contrast, the mixed-species
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 61

plantations overyielded the monocultures at the Congolese site, which led to higher
standing wood biomass at the harvest. The NPP p­ artitioning of the mixed planta-
tions shifted towards aboveground growth at Kissoko (Congo site) and towards
belowground growth at Itatinga (Brazil).

4.3  itterfall and Nutrient Deposition in Pure

L
and Mixed-­Forest Plantations

As Chap. 3 explores this subject, we briefly discuss the main nutrient cycling
­alterations during the presence of N2-fixing trees in Eucalyptus plantations.
In general, the amount of litter deposited by a given species or forest follows the
same pattern of NPP (Fraser et al. 2015). Studies of litterfall are essential for the sus-
tainability of planted forests since litter management significantly changes the bio-
geochemistry of these ecosystems and has already known consequences on plant
growth, soil quality, and climate (Bowen and Nambiar 1984; Bonan 2008; Ponge
2013; Berg 2018). The C accumulation pattern and partitioning in the different tissues
of plants, including the litterfall per unit area, depend on the density, arrangement,
and interaction between the species (Reis et al. 1985; Leite et al. 1998; Nouvellon
et al. 2012; Epron et al. 2013; Laclau et al. 2013).
The amount and quality of the material deposited on forest soils are related to not
only genetics (i.e., planted species), structural, and aging factors of the plantation,
but also climatic variables and soil type (Bernhard Reversat 1996; Landsberg and
Gower 1997; Laclau et al. 2010; Voigtlaender et al. 2019). Soil fertility and climate
significantly shape these two variables (i.e., quantity and quality of leaf litter) (Reis
and Barros 1990; Negi and Sharma 1996; Stape et al. 2010). In soils with low fertility,
it is natural for species to use nutrients more efficiently than nutrient-richer areas
(Novais and Barros 1997; Malhi et al. 2006; Laclau et al. 2010). Therefore, it is com-
mon to find more nutrients being recycled in litter in soils of better fertility or without
nutritional limitation. However, if there is water deficit during forest development, the
water deficit induces stomata closure and, consequently, reduction in carbon fixation;
that is, the plant will not succeed to express its potential and efficiency of nutrient
use (Novais and Barros 1997; Epron et al. 2009; Stape et al. 2010).
Based on some studies about N deposition via litterfall in pure and mixed planta-
tions, it was found that the litterfall in N2-fixing leguminous plantation is 65%
higher (in average) than that in the monocultures of Eucalyptus (without N). In
addition, combining such legumes with Eucalyptus can promote significant increase,
even 42% higher, which evidences the N input increase with the introduction of a
leguminous in a mixed plantation (Fig. 4.1).
The presence of A. mangium in adult mixed plantations (i.e., >5 years) of five
sites in Brazil also intensified the contribution of N via litterfall (Table 4.1), although
the deposition pattern was different in the sites analyzed. In four sites, Acacia
showed higher deposition in comparison to Eucalyptus without N fertilization,
62 F. de Carvalho Balieiro et al.

Fig. 4.1 Scatterplot between litterfall dry mass and N aboveground litterfall (Kg ha−1) among N2-­
fixing, non-N2-fixing, and mixed plantations. Data from n = 53 selected studies (see Tables 4.1 and
4.2). The black line represents the mean regression line independent of plantations, that is, the
overall regression line (R2 = 0.60, p < 0.001). The regression line for red (circle) for non-N2-fixing
species, blue (square) for mixed plantations (E50:A50), and green (triangle) for N2-fixing species
are given. The shadows represent the standard error around lines for non-N2-fixing, N2-fixing, and
mixed plantations only

while the other one showed similar deposition. This trend correlated with the cli-
matic adaptation of the A. mangium.
In Brazilian sandy soils, the addition of 120 kg ha−1 of N via fertilizer in the
Eucalyptus monoculture increased the N via litterfall around 10 kg ha−1 above the
monoculture without N fertilization (final phase of the first rotation). On the other
hand, in mixed plantations with half of the plant density replaced by Acacia man-
gium (E50:A50) and double density (E100:A100), the contributions were 110 and
79 kg ha−1 higher than in the monocultures without N fertilization, respectively. In
younger plantations, the contribution of N inputs via litterfall was lower. But in the
first and second rotations and up to 33 months, the contributions for pure Acacia or
mixed plantations are significantly higher than in the Eucalyptus monocultures
(without N fertilization) (Santos et al. 2016; Tchichelle et al. 2017).
Most studies referred in Table 4.1 do not provide information about deposition of
other nutrients, so it is not possible to imply whether mixed plantations improve the
contributions of these elements. On the other hand, since litterfall in mixed planta-
tions is superior to monocultures, it is believed that the overall contribution is higher,
as observed for N (Fig. 4.2a). The variability of P and N deposition data (Fig. 4.2)
 4

Table 4.1 Litterfall mass and nutrient deposition associated (kg ha−1 ano−1) under pure and mixed-forest plantations of N2-fixing and non-N2-fixing trees in
different countries around the world*
Country Rainfall Temp. Soil (texture) or Age Mass N P K Ca Mg
o
Species (proportion) State mm C substrate years kg ha−1 year−1 Reference
Pseudosamanea guachapele Brazil 1500 25 Planosol (sandy) 5 7,968 132 7 34 119 51 Froufe (1999)
(RJ)
P. guachapele + E. grandis Brazil 1500 25 Planosol (sandy) 5 7,653 80 5 20 71 20 Froufe (1999)
(RJ)
A. mangium Brazil 1500 25 Planosol (sandy) 5 12,854 165 6 57 96 23 Froufe (1999)
(RJ)
Eucalyptus grandis Brazil 1500 25 Planosol (sandy) 5 9,903 40 6 29 84 21 Froufe (1999)
(RJ)
E. urograndis- Brazil 1370 24 Planosol (sandy) 2.5 500 4 0.3 2 5 1 Santos et al. (2016)
(RJ)
E. urograndis + N Brazil 1370 24 Planosol (sandy) 2.5 1,000 8 0.6 4 9 2 Santos et al. (2016)
(RJ)
A. mangium + E. urograndis (100:100) Brazil 1370 24 Planosol (sandy) 2.5 1,800 19 0.6 6 13 3 Santos et al. (2016)
(RJ)
A. mangium + E. urograndis (50:50) Brazil 1370 24 Planosol (sandy) 2.5 1,620 19 0.6 5 12 3 Santos et al. (2016)
(RJ)
A. mangium Brazil 1370 24 Planosol (sandy) 2.5 2,100 27 0.4 7 13 3 Santos et al. (2016)
(RJ)
E. urograndis Brazil 1370 24 Planosol (sandy) 5 11,600 108 4 37 69 0 Santos et al. (2016)
(RJ)
E. urograndis + N Brazil 1370 24 Planosol (sandy) 5 12,500 118 4 38 74 21 Santos et al. (2016)
(RJ)
A. mangium + E. urograndis (100:100) Brazil 1370 24 Planosol (sandy) 5 16,100 218 5 51 89 24 Santos et al. (2016)
Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus…

(RJ)
(continued)
63
 64

Table 4.1 (continued)

Country Rainfall Temp. Soil (texture) or Age Mass N P K Ca Mg
o
Species (proportion) State mm C substrate years kg ha−1 year−1 Reference
A. mangium + E. urograndis (50:50) Brazil 1370 24 Planosol (sandy) 5 15,300 197 4 47 83 22 Santos et al. (2016)
(RJ)
A. mangium Brazil 1390 24 Planosol (sandy) 5 13,400 230 3 52 61 15 Santos et al. (2016)
(SP)
A. mangium Brazil 1390 19 Ferralsol (loam) 6 6,890 98 – – – Voigtlaender et al.
(SP) (2019)
A. mangium + E. grandis (50:50) Brazil 1390 19 Ferralsol (loam) 6 8,693 63 – – – Voigtlaender et al.
(SP) (2019)
E. grandis Brazil 1390 19 Ferralsol (loam) 6 9,201 49 – – – Voigtlaender et al.
(SP) (2019)
A. mangium Brazil 1420 21 Ferralsol (loam) 6.3 8,394 103 – – – Voigtlaender et al.
(SP) (2019)
A. mangium + E. grandis (50:50) Brazil 1420 21 Ferralsol (loam) 6.3 10,107 77 – – – Voigtlaender et al.
(SP) (2019)
E. grandis Brazil 1420 21 Ferralsol (loam) 6.3 11,302 62 – – – Voigtlaender et al.
(SP) (2019)
A. mangium Brazil 1420 23 Arenosol (sandy) 6.1 5,297 75 – – – Voigtlaender et al.
(SP) (2019)
A. mangium + E. urograndis (50:50) Brazil 1420 23 Arenosol (sandy) 6.1 10,296 64 – – – Voigtlaender et al.
(SP) (2019)
E. urograndis Brazil 1420 23 Arenosol (sandy) 6.1 10,804 54 – – – Voigtlaender et al.
(SP) (2019)
A. mangium Brazil 1240 24 Ferralsol (clayed) 6.3 8,185 82 – – – Voigtlaender et al.
(SP) (2019)
A. mangium + E. urograndis (50:50) Brazil 1240 24 Ferralsol (clayed) 6.3 8,504 76 – – – Voigtlaender et al.
(SP) (2019)
F. de Carvalho Balieiro et al.
 4

E. urograndis Brazil 1240 24 Ferralsol (clayed) 6.3 8,195 49 – – – Voigtlaender et al.

(SP) (2019)
P. guachapele Brazil 1250 24 Planosol (sandy) 7 12,750 248 – – – – Balieiro et al.
(SP) (2004)
E. grandis Brazil 1250 24 Planosol (sandy) 7 11,840 58 – – – – Balieiro et al.
(RJ) (2004)
E. globulus Australia 1009 16 Acrisol (sandy 8.8 2,430 14 0.5 – – – Forrester et al.
loam) (2013)
A. mearnsii Australia 1009 16 Acrisol (sandy 8.8 3,290 49 1 – – – Forrester et al.
loam) (2013)
E. globulus + A. mearnsii Australia 1009 16 Acrisol (sandy 8.8 3,560 32 1 – – – Forrester et al.
loam) (2013)
E. globulus + A. mearnsii Australia 1009 16 Acrisol (sandy 8.8 3,740 39 1 – – – Forrester et al.
loam) (2013)
E. globulus + A. mearnsii Australia 1009 16 Acrisol (sandy 8.8 3,690 47 1 – – – Forrester et al.
loam) (2013)
E. globulus + N Australia 1009 16 Acrisol (sandy 8.8 3,050 18 1 – – – Forrester et al.
loam) (2013)
E. saligna Hawaii 4600 21 Andosol 4 8,070 70 5 4 61 10 Binkley et al.
(1992)
Albizia falcataria Hawaii 4600 21 Andosol 4 12,340 108 6 6 86 14 Binkley et al.
(1992)
E. saligna + A. falcataria (50:50) Hawaii 4600 21 Andosol 4 18,200 234 9 7 72 19 Binkley et al.
(1992)
A. mangium Congo 1200 25 Arenosol (sandy) 7 7,000 112 10 – – – Koutika et al.
(2014)
A. mangium + E. urograndis (50:50) Congo 1200 25 Arenosol (sandy) 7 7,000 63 11 – – – Koutika et al.
Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus…

(2014)
E. urograndis Congo 1200 25 Arenosol (sandy) 7 6,200 30 9 – – – Koutika et al.
(2014)
65

(continued)
 66

Table 4.1 (continued)

Country Rainfall Temp. Soil (texture) or Age Mass N P K Ca Mg
o
Species (proportion) State mm C substrate years kg ha−1 year−1 Reference
A. mangium (2nd rotation) Congo 1200 25 Arenosol (sandy) 2 5,000 388 Tchichelle et al.
(2017)
A. mangium + E. urograndis (50:50) (2sd Congo 1200 25 Arenosol (sandy) 2 3,300 306 Tchichelle et al.
rotation) (2017)
E. urograndis (2nd rotation) Congo 1200 25 Arenosol (sandy) 2 2,700 89 Tchichelle et al.
(2017)
P. guachapele + E. grandis – M (50:50) Brazil 1250 24 Planosol (sandy) 7 66 – – – – – Balieiro et al.
(RJ) (2004)
Leguminous tree plantations
A. mangium Brazil 1005 25 Planosol (sandy) 4 10,155 211 12 28 80 24 Andrade et al.
(RJ) (2000)
A. holosericea Brazil 1005 25 Planosol (sandy) 4 9,062 149 6 20 83 17 Andrade et al.
(RJ) (2000)
Mimosa caesalpiniaefolia Brazil 1005 25 Planosol (sandy) 4 9,132 147 4 21 60 11 Andrade et al.
(RJ) (2000)
Sclerolobium paniculatum–P Brazil 2100 27 Ferralsol (sandy 9 9,646 117 3 6 26 10 Mochiutti et al.
(AP) loam) (2006)
M. caesalpiniaefolia Brazil 1300 26 Acrisol (sandy 10 7,830 157 10 55 115 26 Ferreira et al.
(PE) loam) (2007)
Degraded lands
Mimosa caesalpiniaefolia Brazil 1005 25 Gravel extraction 10 11,200 170 7 31 190 40 Costa et al. (1998)
(RJ) pit
M. caesalpiniaefolia + Gliricidia sepium Brazil 1005 25 Gravel extraction 10 100 4 18 110 25 Costa et al. (1998)
(RJ) pit
Gliricidia sepium Brazil 1005 25 Gravel extraction 10 5,700 100 4 18 100 32 Costa et al. (1998)
(RJ) pit
F. de Carvalho Balieiro et al.
 4

Acacia auriculiformis Brazil 1005 25 Gravel extraction 10 6,900 110 5 19 120 29 Costa et al. (1998)
(RJ) pit
M. caesalpiniaefolia/A. auriculiformis Brazil 1005 25 Gravel extraction 10 130 5 24 150 29 Costa et al. (1998)
(RJ) pit
M. caesalpiniaefolia Brazil 1900 27 Red mud deposits 3 9,727 198 – – – – Fortes (2000)
(MA)
M. acutistipula Brazil 1900 27 Red mud deposits 3 9,221 197 – – – – Fortes (2000)
(MA)
A. mangium Brazil 1900 27 Red mud deposits 3 10,376 195 – – – – Fortes (2000)
(MA)
E. camaldulensis Brazil 1020 24 Clay extraction 4 6,300 35 3 19 45 10 Silva et al. (2015)
(RJ) pit
A. mangium Brazil 1020 24 Clay extraction 4 8,400 69 4 18 31 9 Silva et al. (2015)
(RJ) pit
*
Most of the information in the table is short rotation (1 year). When data were not available in tables or supplementary materials within the papers, the “web
plot digitizer program” was used to extract the graphical data (https://automeris.io/WebPlotDigitizer/)
Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus…
67
68 F. de Carvalho Balieiro et al.

Fig. 4.2 Box plots of N (a) and P (b) in aboveground litterfall (Kg ha−1) under N2-fixing and
­non-­N2-­fixing monocultures and mixed plantations of both. Data from n = 58 selected studies
(see Tables 4.1 and 4.2). Black points represent outliers

is mostly due to the evaluated species, age of plantations, and variations in the soil
types studied that present different mineralogy and fertility, as well as different pat-
terns of growth and accumulation in plants.

4.4  itter Decomposition Under Pure and Mixed-Forest

L
Plantation

The logic of non-N2-fixing and N2-fixing species’ mixed plantations is to promote

forest sustainability through complementarity and competitive reduction interac-
tions among species. The “extra” supply of N provided by legume trees via biologi-
cal nitrogen fixation and its redistribution offer throughout the system an
intensification of leaf litter decomposition, N mineralization, and transferring
between fixing and non-fixing species. Collectively, they are key processes to
improve the growth and yield of the mixed forests, eliminating or using less N fertil-
izers (Forrester et al. 2006; Kaye et al. 2000; Koutika and Richardson 2019).
In general, decomposition of forest residues is driven by the litter chemical attri-
butes, environmental conditions, and surface area/volume ratio of the residue
(Landsberg and Gower 1997; Gholz et al. 2000; Laclau et al. 2010). Although the N
deposition is high in pure and mixed plantations with N2-fixing trees (Fig. 4.1), this
chemical characteristic is not a guarantee of higher litter decomposition, especially
under tropical conditions. For instance, A. mangium in sandy and loamy t­extured
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 69

Table 4.2 Changes in soil C stocks (Mg ha−1) under plantations of Eucalyptus spp. in comparison
to native vegetation as a function of rotation, soil texture, and biome evaluated
n observations;
Depth comments Max Min Median SD Mean*
Carbon stock budget in pure stands of Eucalyptus related
to natural vegetation
Mg ha−1
0–20 cm 50 20.0 −20.9 −1.8 10.0 −1.5
20–40 cm 39 42.0 −25.0 −1.9 15.9 0.3
Carbon stock change induced by time rotations
Mg ha−1
0–20 cm 13; 1st rotation 19.0 −20.7 1.2 11.6 −2.3
15; 2nd rotation 20.0 −20.9 3.0 11.5 2.3
21; not reported 14.0 −18.2 −4.0 7.3 −3.8
20–40 cm 9; 1st rotation 24.0 −21.2 5.0 16.3 −1.0
14; 2nd rotation 42.0 −25.0 −0.6 20.6 3.1
14; not reported 20.0 −21.0 −1.8 10.0 −1.5
Carbon stock change induced by soil texture
Mg ha−1
0–20 cm 10; sandy 7.8 −10.0 −1.6 6.9 −1.0
17; clayed 19.0 −18.2 0.0 11.5 1.2
22; not reported 20.0 −20.9 −2.2 9.9 −3.9
20–40 cm 12; sandy 24.0 −12.0 −1.5 10.7 2.5
13; clayed 32.8 −21.0 1.0 15.5 2.6
12; not reported 42.0 −25.0 −9.1 20.3 −4.4
Carbon stock change induced by biome
Mg ha−1
0–20 cm 13; Cerrado 19.0 −10.0 1.0 8.7 3.5
22; Atlantic rainforest 15.0 −21.0 −6.5 10.3 −5.2
12; Pampa 20.0 −13.0 −3.5 9.4 −0.3
20–40 cm 10; Cerrado 33.0 −12.0 2.5 13.6 6.4
18; Atlantic rainforest 14.0 −23.0 −4.5 12.1 −5.3
9; Pampa 42.0 −25.0 10.0 21.6 5.6
Adapted from Fialho and Zinn (2012); * In average, Eucalyptus spp. plantations do not affect the
soil organic carbon stocks in Brazil (t-test at p < 0.05 were used in all comparasions)

soils shows lower leaf and fine root decomposition in comparison to Eucalyptus,
although it has high N leaf concentration (Balieiro et al. 2004; Bachega et al. 2016;
Doughty et al. 2018). Besides, A. mangium has high internal cycling of P (Balieiro
et al. 2004; Bachega et al. 2016; Doughty et al. 2018), providing a litter with low P
concentration. Furthermore, A. mangium has a more recalcitrant leaf litter, lignin
rich with low contents of nonstructural carbohydrates or low-­molecular-­weight phe-
nols and P concentration (Santos et al. 2017). Thus, the microbiota faces a harsh
condition to decompose its residues. The concept of “decomposer starvation,” pro-
posed by Hättenschwiler et al. (2011), reveals a syndrome of poor C litter in tropical
rainforests which could be applied to pure A. mangium plantations in oligotrophic
70 F. de Carvalho Balieiro et al.

soils (e.g., Arenosol). According to these authors “in the neotropical rainforest,
natural selection favored a leaf litter trait that leads to starvation-­inhibition of
decomposers, thereby increasing the tree ability to compete for the uptake of highly
limiting nutrients, P in particular, via mycorrhizal associations.” Other authors who
have also observed a decrease of P in the soil in areas in mixed plantations claim
that this decrease comes from the P uptake by Eucalyptus to maintain the N:P stoi-
chiometry of their leaves (Koutika et al. 2014).
It is worth noting that legume trees have a different demand for P as a function
of symbiosis with diazotrophic bacteria (Giller and Cadisch 1995; Vadez et al.
1995). Therefore, different strategies are required for capturing this element, such
as acidification of the rhizosphere that improves the solubilization of less soluble
forms of P (Raven et al. 1990) and root exudation of acid phosphatases and organic
acids that leads to PO4 desorption from the soil matrix and improves P availability
(Vance 2001; Venterink 2011). These strategies are paramount in tropical soils since
they are mainly able to fix P by ligand exchange and occupation of P sorption sites
(Bhatti et al. 1998; de Campos et al. 2016). This is possibly due to the high content
of aluminum and iron oxides in the Oxisols and Ultisols typically found in moist
tropical sites (Leal and Velloso 1973; Lloyd et al. 2001).
Land-use history may also affect the litter decomposition. Under Ferralsols, pre-
viously managed with Eucalyptus (for 60 years), Bachega et al. (2016) detected that
early decomposition of leaves and fine roots of Acacia mangium was markedly
slower than that of Eucalyptus residues, despite higher N and P concentrations in
both tissues of Acacia (respectively, 1.9 and 1.5 times higher for leaves and 2.9 and
3.3 times for roots). The lower values of C:N and C:P ratios were associated to litter
decomposition rates of Acacia, but the authors did not confirm the home field
advantage (HFA) that states which plants create a specialization of local decom-
poser communities of their litter. For Acacia, authors claim that the time since the
start of the first rotation was not long enough to allow the decomposers to become
specialized for its residues. In contrast, several researches have demonstrated that in
the short term the litter and soil bacterial and fungi communities are very specific
for both (Rachid 2013; Rachid et al. 2015; Bini et al. 2013).
As was pointed out in the perspective of the HFA theory, our research group
studied the litter leaf decomposition of both species (i.e., Acacia and Eucalyptus) in
a sandy soil. Our team observed a distinct HFA for decomposition litter from Acacia
and Eucalyptus, with Acacia decomposing in the home stands faster than under
Eucalyptus stands. In contrast, litter from Eucalyptus decomposed faster under
Acacia stands. Additionally, the litter of each material showed very distinct fungal
communities and did not change in function of time, and the local of incubation did
not influence the microbial community (Rachid 2013). Higher diversity and lower
dominance of fungi were reported in litter from Acacia and mixed plantations dur-
ing the decomposition period (180d), regardless of the place at which they were
established (Rachid 2013). By using infrared spectroscopy, it was found that
Eucalyptus litter during the decomposition under Acacia stands remain more pro-
teinaceous material than the initial residue, and the migration of N to Eucalyptus
litter may be considered. On the other hand, the Acacia litter did not change its
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 71

chemical composition during the incubation (Novotny et al. 2013). These results
demonstrate the importance of biological N2 fixed for the Eucalyptus litter decom-
position, and suggests that the most diverse fungi community is essential for mixed
litter decomposition allowing N mobility. Nonetheless, it is interesting to note that
the higher P concentration in Eucalyptus litter acts simultaneously and synergisti-
cally with the decomposition process in the mixed plantation (Santos et al. 2017). In
addition, the C:N ratio alone seems not to be the main predictor of soil organic and
litter decomposition (Cotrufo et al. 2013; Lehmann and Kleber 2015; Berg 2018).
Some predictors such as N:P, lignin:N, and lignin:P, when possible, should be ana-
lyzed collectively.
The N:P ratio of the litter trait is often cited as an essential drive of litter decomposi-
tion (Güsewell 2004; Bakker et al. 2011). However, differences in the N:P ratio observed
in aboveground biomass and leaf litter usually reflect even more significant changes in
the available N:P ratio of soil (Güsewell 2004). Figure 4.3 demonstrates the broad range
of the N:P ratio (mass) of the litter in the papers analyzed and, consequently, about
edaphic conditions of the studies. Also, there is a trend towards increasing this relation
in mixed plantations: non-N2-fixing (N:P–14) < N2 fixing (N:P–25) < mixed (N:P–32).
Although the contribution of N via litterfall is higher for leguminous plantations, fol-
lowed by mixed plantings compared to Eucalyptus plantations, for P there is a lower

Fig. 4.3 Box plots of N:P relationship in aboveground litterfall (Kg ha−1) among N2-fixing, non-­
N2-­fixing, and mixed plantations. Data from n = 58 selected studies (see Tables 4.1 and 4.2). Black
points represent outliers
72 F. de Carvalho Balieiro et al.

recycling trend in mixed planting conditions (Fig. 4.2b). This finding corroborates the
productivity of these plantations and the accumulation of P in the aboveground biomass
of the species, besides the edaphic limitations in the P supply. In other words, although
P is being absorbed more efficiently in these plantations, the plants begin to drain this P
for internal use. This process decreases the availability of P for the soil in the medium
and long terms (Sanchez 1979; Binkley et al. 2000) and requires attentive management
with phosphate fertilization in future rotations.
Climate change and especially temperature rise may also affect the chemical char-
acteristics of leaf litter with effects on decomposition. Trees growing in high-­
temperature environments have a reduction in the N content of the leaves and an
increase in the rate of carboxylation, which results in increased structural and
­nonstructural carbon levels in the leaves (e.g., glucose, sucrose, fructose) (Güsewell
2004; Pandey et al. 2015) and a recalcitrant leaf litter. These effects can be intensified
in the tropics, where the soils are acidic and poor (i.e., with minerals with high
adsorption capacity of P). In addition, the presence of leguminous species with high
internal P recycling, such as A. mangium (Balieiro et al. 2005; Inagaki et al. 2011;
Santos et al. 2017), may impair the decomposition process with unfavorable stoichio-
metric ratios in the leaf litter (e.g., C:N, C:P, or N:P) (Güsewell 2004). Therefore,
changes in leaf litter quality may be reflected by changes in soil ­enzymatic activity
(Fanin and Bertrand 2016; Santos et al. 2017), stabilization of C stocks (Fisk et al.
2015; Castellano et al. 2015), emission of CO2 through microbial r­ espiration (Zhou
et al. 2013, 2015), and nutrient mineralization rates (e.g., P, N, and S) (Marklein et al.
2016; van Huysen et al. 2016). All these aspects are ­feedbacks of climate change and
productivity of forest systems (i.e., plantations or natural forests) (Bonan 2008).

4.5  re Soil Carbon Stocks Really Higher in Mixed

A
Plantations than in Monocultures?

In general, soils present several mechanisms related to the protection of organic

matter that is associated with chemical complexation (e.g., polymerization, humifi-
cation, organic synthesis, and organo-mineral interaction) and physical protection
(e.g., complexation with mineral fractions and degree of aggregation) (Feller and
Beare 1997; Sollins et al. 1996; Roscoe and Machado 2002). In planted forests, crop
residue management, machine traffic, planting structure, climate, and planted and
understory species all were identified as determinants for nutrient dynamics and
degree of C storage in soils (Bernhard Reversat 1996; Binkley et al. 2000; Kaye
et al. 2000; Resh et al. 2002; Qiao et al. 2014; Jesus et al. 2015). With the possibility
of managing the communities of soil bacteria and fungi in mixed Eucalyptus and
A. mangium plantations (Rachid et al. 2013, 2015; Bini et al. 2013), it is also reason-
able to think about changes in belowground interactions (i.e., belowground compe-
tition for nutrients and water). These consequences are still poorly studied in soil C
dynamics, although Sokol and Bradford (2019) have claimed that belowground
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 73

Fig. 4.4 Schematization of the priming effect—nonadditive interactions between decomposition

of the added substrate and of soil organic matter (SOM): (+) acceleration of SOM decomposi-
tion—positive effect; (−) retardation of SOM decomposition—negative priming effect (adapted
from Kuzyakov et al. (2000))

inputs provided by the microbial formation pathway form mineral-stabilized soil C

are more effective than aboveground inputs, partly due to the higher efficiency of
formation by the rhizosphere microbial community relative to the bulk soil com-
munity. In mixed plantations of A. mangium and Eucalyptus, there might be a more
favorable environment for soil C stabilization, because we observed a complemen-
tarity in terms of nutrient deposition (e.g., N and P deposition) (Santos et al. 2017,
2018), soil bacterial and fungi communities (Rachid et al. 2013, 2015), and fine root
growth (segregated) in soil profile (Silva et al. 2009; Laclau et al. 2013).
The dynamics of soil organic matter from natural and planted forests, including
mixed plantations, have been studied from the viewpoint of the “priming effect” by
several authors (Resh et al. 2002; Balieiro et al. 2008; Hoosbeek and Scarascia-­
Mugnozza 2009; Forrester et al. 2013; Koutika et al. 2014). The priming effects
were defined by Kuzyakov et al. (2000) as the “strong short-term changes in the
turnover of soil organic matter caused by comparatively moderate treatments of the
soil.” Such changes might be the input of organic or mineral fertilizer to the soil,
exudation of the organic substances by roots, and simple mechanical treatment of
soil or its dry and wet cycles. Figure 4.4 presents the schematic representation of the
priming effect. Under an ecological point of view, the negative priming effects have
a much greater significance than positive ones, but the direction of these changes
depends mostly on the nutrient status of the soil and the C:N ratio of the active SOM
pool (i.e., labile organic matter) (Kuzyakov et al. 2000).
74 F. de Carvalho Balieiro et al.

4.5.1 Soil Carbon Stocks in Pure Plantations of Eucalyptus

The impacts of Eucalyptus on soil carbon stocks vary according to many factors,
including the land-use history, previous crop, post-logging residue management,
climate, and spatial variability of soil attributes (Forrester et al. 2006; Chaer and
Tótola 2007; Balieiro et al. 2008; Gonçalves et al. 2013). Under a broader point of
view, in a recent meta-analysis, Fialho and Zinn (2014) compiled data on the organic
soil C stocks using 50 observations for depths between 0 and 20 cm and 39 between
0 and 40 cm of studies in Brazil in paired plots (i.e., plantations and natural forests)
aiming to evaluate the impact of native vegetation conversion on plantations of
Eucalyptus. The authors verified that, on average, the net effect of the conversion is
null; that is, it does not damage the original C stocks of the soil, although losses and
gains are related to local site conditions (Table 4.2). The authors conclude that this
null effect, even after considering the rotation time, texture, and biome, suggests
that other factors may control the direction and intensity of changes in soil C stocks
in Eucalyptus plantations and point to the productivity, techniques of soil prepara-
tion, soil type, and management as essential factors in this evaluation.
Cook et al. (2016) studied the effects of Eucalyptus plantations on soil carbon
stocks, 0–30 cm deep, over two decades, in 306 operational eucalypt plantations
across a 1200 km gradient in Brazil. The study included two tropical states (Bahia
and Espírito Santo) and one subtropical state (São Paulo), and resulted in the find-
ings that the size and rates of change in soil C stocks were due to different factors.
These factors include the history of the site, soil order, clay content, seasonal
­precipitation (especially dry season), and mean annual temperature. In general,
across all sites, the soil C showed a slight decrease (−0.22 ± 0.05 Mg ha−1 year−1)
from the original sampling that ranged in approximately 3–4 rotations, but in sub-
tropical regions the stocks remained the same (0.06 Mg ha−1 year−1).
Maquere et al. (2008) studied the impact of different land uses (i.e., savanna, pas-
ture, and Eucalyptus saligna plantations) and a management (i.e., 60 years under
short rotation vs. 60 years under continuous growth) on soil carbon and nitrogen
stocks. The authors found significant soil carbon increases (approximately 25%)
with Eucalyptus under short rotation management when compared to Cerrado native
vegetation, whereas soil carbon stocks in the continuous forest plantation increased
by 15% in relation to Cerrado vegetation. In the same biome and in degraded p­ astures
Lima et al. (2006) reported that afforestation of former degraded pasture land leads
to increased C storage in the soil in the short term (30 years). They observed carbon
sequestration rates up to 0.57 Mg C ha−1 year−1 by Eucalyptus afforestation.
Finally, it is evident in the studies that pure Eucalyptus plantations present a
potential for soil C increase, especially if preceded by degraded pastures. However,
local abiotic conditions and forest management seem to be the significant con-
straints to the effective increase of C in soil. On the other hand, the introduction of
legume trees associated with diazotrophic bacteria to Eucalyptus monocultures has
gained expression in recent years. The increase of soil C stocks so far had always
been related to these plantations but, as will be seen below, this phenomenon cannot
be generalized, mainly for the Brazilian tropics.
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 75

4.5.2  oil C Stocks Under Mixed Plantations of N2-Fixing

S
and Non-N2-Fixing Plantations

Several authors reported higher soil C accumulation of N2-fixing species over

­non-­N2-­fixing ones (Binkley et al. 1992; Kaye et al. 2000; Resh et al. 2002).
However, when a small or no variation is detected in soil C stocks, changes in soil
morphological and molecular levels of soil organic matter have also been observed
(Kindel et al. 2003; Voigtlaender 2012; Koutika et al. 2014; Santana et al. 2015;
Voigtlaender et al. 2019), and this may have consequences for the nutrient cycling
in these plantations.
Resh et al. (2002), using isotopic techniques, detected that 55% of the soil C
enriching the N2-fixing plantations came from the retention of native C, in a compari-
son between the C soil stocks of N2-fixing species, as Albizia falcataria, Leucaena
leucocephala, and Casuarina equisetifolia, and the soil C stocks of Eucalyptus
saligna in four tropical soils, two Andisols and one Vertisol and Entisol. They
reported that the native C stock was derived from old sugarcane plantations and pas-
tures with metabolic assimilation of C4, while the other 45% came from C stabilized
and derived from recently allocated C3 from the trees, showing a clear negative prim-
ing effect. In addition, 62% of the explanation of the stabilization of native C (C4)
occurred due to the accumulation of N in the soil of the legume trees and Casuarina
plantations. Very similar results were reported by Kaye et al. (2000) in Andisols from
Hawaii, where Albizia monocultures had 2.3 Mg ha−1 more N and 20 Mg ha−1 more
C than Eucalyptus monocultures in the 50 cm topsoil. In Acrisols (Brown Dermasols)
from Australia, Forrester et al. (2013) reported a difference greater than 15 Mg ha−1
between N2-fixing and non-N2-fixing trees in the first 30 cm topsoil. However, in
Arenosols from Congo and Brazil, a lower gain in soil carbon storage was detected
in the N2-fixing Acacia mangium plantations at 7 and 5 years after planting in com-
parison to monocultive of Eucalyptus, respectively (Koutika et al. 2014; Rocha et al.
2019). In the Pseudosamanea guachapele plantations, the C storage was even much
lower than that found under Eucalyptus grandis plantations in southeastern Brazil, in
the same soils (Balieiro et al. 2008), a fact that was justified by the authors by high
contribution of N (~250 kg ha−1 y−1) and other nutrients cycled through litterfall,
resulting in a rapid decomposition of the litter and SOM. In is worth mentioning here
that the pure legume tree stands studied in Brazil (Acacia mangium and
Pseudosamanea guachapele) had no similar growth in comparison to Eucalyptus,
contrary to the plantations of Falcataria moluccana (Albizia falcataria) in Hawaii
that present higher aboveground biomass than Eucalyptus saligna (Kaye et al. 2000).
Climate and soil characteristics can control soil C stocks, but the aboveground
biomass and NPP are also drivers of C stocks in various environments (Lal 2005;
Cornwell et al. 2008; Qiao et al. 2014; Nottingham et al. 2015; Lange et al. 2015).
With the literature data consulted, it is not possible to state that C stocks are a func-
tion of aboveground biomass production since the soil C augmentation pattern is not
very different between monocultures and mixed ones.
Under mixed plantations and Brazilian conditions, mixed plantations presented
aboveground biomass higher than monocultures only in sites with poor soils (for
76 F. de Carvalho Balieiro et al.

Acacia mangium and Pseudosamanea guachapele) (Santos et al. 2017; Balieiro

et al. 2010). However, despite the soil C stocks in N2-fixing plantations did not differ
statistically from Eucalyptus monocultures (without N) (Balieiro et al. 2008; Rocha
et al. 2019), under mixed plantations were detected higher rates of C sequestration
(up to 1.44 Mg ha−1 y−1), in comparison to Eucalyptus monocultives (without N
­fertilization), demonstrating that for oligotrophic soils the mixed plantation is an
great alternative to improve soil quality.
In Australia, Forrester et al. (2013) studied mixed plantations of Eucalyptus
globulus and Acacia mearnsii. They detected a linear relationship between aboveg-
round production and soil C, but not at an N2-fixing proportion, as found by Kaye
et al. (2000), who observed higher aboveground biomass production in mixed plan-
tations and lower in monocultures. In both papers, the increase in C soil stocks in
mixed plantations is justified by the negative priming effect of the mixed litter, that
is, the maintenance of the C originated from previous crops (sugarcane) and by the
addition and stabilization of C derivatives from the trees.
A significant contrast found among these plantations seems to be the pattern of
C allocation in the belowground biomass, because Hawaiian monocultures accumu-
lated more C in the belowground than mixed plantations, contrary to what was
observed in Australia (Forrester et al. 2013; Binkley and Ryan 1998). In Hawaii,
intraspecific competition intensified the use of soil resources, while interspecific
competition in Australia further pressured soil resources, culminating in below-
ground investments to compensate for distinct constraints. In monocultures, the
accumulation patterns of the species can lead to the storage for the aboveground
biomass of critical elements for soil C storage; in contrast, and because of the com-
plementarity of niches and facilitation (in both directions), mixed plantations can
more efficiently cycle nutrients and better use available water. As previously men-
tioned (Sokol and Bradford 2019) and pointed out by other authors (Schmidt et al.
2011; Nouvellon et al. 2012), the change in the pattern of C allocation in plantations
may be due to the large C stock drive to the soil.
The differential input of N by N2-fixing species appears not to be the major rea-
son for increasing soil C storage (Forrester et al. 2013). The complementarity of
niches (above- and belowground) (Tilman 1999; Tilman et al. 2001; Forrester et al.
2006), soil microbial sharing and increased fungal richness (Rachid et al. 2013,
2015), and stimulus to grow and microbial activity (Bini et al. 2013; Pereira et al.
2017; Santos et al. 2017) seem to prove that belowground dynamics commands soil
C storage (Sokol and Bradford 2019), but studies in this sense need to be performed
for mixed plantations.
The difference in the magnitude of C stocks of soils has a great association with
mineralogy and texture (Feller and Beare 1997; Hassink 1997), hence the variations
presented in Table 4.3. In general, Andisols from Hawaii have high specific surface
phyllosilicate clays and naturally higher SOM contents due to the complexes formed
with Al (i.e., noncrystalline Al hydroxide and Al-insoluble organic complexes) and
allophanes (Feller and Beare 1997). Even in soils with a recognized SOM stability,
the biologically fixed N input was responsible for a significant increase of the C and
N stocks, showing the benefit of the N2-fixing species in that environment, which
presents a nonexistent water deficit (i.e., 4500 mm of annual precipitation).
 4

Table 4.3 Soil C stocks (Mg ha−1) in pure and mixed plantations of eucalyptus and N-fixing trees
Non-N- Soil Carbon
Age fixing N-fixing layer stock
Species Country years Proportion cm Mg ha−1 N:P Soil classification Reference
Eucalyptus saligna Hawaii 16 100 0 0–50 123.4a Andosol Kaye et al. (2000)
E. saligna + Albizia falcataria Hawaii 16 75 25 0–50 129.7a Andosol Kaye et al. (2000)
E. saligna + Albizia falcataria Hawaii 16 66 34 0–50 132a Andosol Kaye et al. (2000)
E. saligna + Albizia falcataria Hawaii 16 50 50 0–50 136.1a Andosol Kaye et al. (2000)
E. saligna + Albizia falcataria Hawaii 15 34 66 0–50 140.1a Andosol Kaye et al. (2000)
Albizia falcataria Hawaii 15 0 100 0–50 148.8a Andosol Kaye et al. (2000)
E. globulus Australia 8.8 100 0 0–30 66.3 30b Acrisol Forrester et al. (2013)
E. globulus + Acacia mearnsii Australia 8.8 75 25 0–30 77.9 46b Acrisol Forrester et al. (2013)
E. globulus + Acacia mearnsii Australia 8.8 50 50 0–30 84.5 49b Acrisol Forrester et al. (2013)
E. globulus + Acacia mearnsii Australia 25 75 0–30 86.1 57b Acrisol Forrester et al. (2013)
Acacia mearnsii Australia 0 100 0–30 82.8 66b Acrisol Forrester et al. (2013)
E. urograndis Brazil 5 100 0 0–40 20.0 27b Planosol Rocha et al. (2019));
Santos et al. (2017)
A. mangium + E. urograndis Brazil 5 50 50 0–40 22.4 49b Planosol Rocha et al. (2019);
Santos et al. (2017)
A. mangium Brazil 5 0 100 0–40 22.1 77b Planosol Rocha et al. (2019);
Santos et al. (2017)
E. grandis Brazil 7 100 0 0–40 17.2 7c Planosol Balieiro et al. (2008);
Froufe (1999)
A. mangium + E. grandis Brazil 7 50 50 0–40 23.8 16c Planosol Balieiro et al. (2008);
Froufe (1999)
A. mangium Brazil 7 0 100 0–40 14.2 19c Planosol Balieiro et al. (2008);
Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus…

Froufe (1999)
E. urograndis Congo 7 100 0 0–25 15.9 62d Arenosol Koutika et al. (2014)
A. mangium + E. urograndis Congo 7 50 50 0–25 17.8 75d Arenosol Koutika et al. (2014)
77

(continued)
Table 4.3 (continued)
78

Non-N- Soil Carbon

Age fixing N-fixing layer stock
Species Country years Proportion cm Mg ha−1 N:P Soil classification Reference
A. mangium Congo 7 0 100 0–25 16.7 59d Arenosol Koutika et al. (2014)
E. grandis (Bofete) Brazil 5 100 0 0–15 27.6 — Ferralsol Voigtlaender et al. (2019)
A. mangium + E. grandis (Bofete) Brazil 5 50 50 0–15 29.6 — Ferralsol Voigtlaender et al. (2019)
A. mangium (Bofete) Brazil 5 0 100 0–15 26.7 — Ferralsol Voigtlaender et al. (2019)
E. urograndis (Luiz Antônio) Brazil 6 100 0 0–15 22.2 — FerralicArenosol Voigtlaender et al. (2019)
A. mangium + E. urograndis (Luiz Antônio) Brazil 6 50 50 0–15 24.1 — FerralicArenosol Voigtlaender et al. (2019)
A. mangium (Luiz Antônio) Brazil 6 0 100 0–15 21.6 — FerralicArenosol Voigtlaender et al. (2019)
E. urograndis (Santana do Paraíso) Brazil 6 100 0 0–15 35.1 — Ferralsol Voigtlaender et al. (2019)
A. mangium + E. urograndis (Santana do Paraíso) Brazil 6 50 50 0–15 34.5 — Ferralsol Voigtlaender et al. (2019)
A. mangium (Santana do Paraíso) Brazil 6 0 100 0–15 38.7 — Ferralsol Voigtlaender et al. (2019)
Casuarina equisetifolia Porto 4 0 100 0–40 65.1 191 Andosol Parrota (1999)
Rico
Eucalyptus robusta Porto 4 100 0 0–40 75.7 124 Andosol Parrota (1999)
Rico
Leucaena leucocephala Porto 4 0 100 0–40 75.6 150 Andosol Parrota (1999)
Rico
C. equisetifolia + E. robusta Porto 4 50 50 0–40 65.9 133 Andosol Parrota (1999)
Rico
C. equisetifolia + L. leucocephala Porto 4 50 50 0–40 56.6 179 Andosol Parrota (1999)
Rico
E. robusta L. leucocephala Porto 4 50 50 0–40 61.7 146 Andosol Parrota (1999)
Rico
a
Values estimated from models adjusted by authors for monocultures and mixed stands
b
N:P ratio estimated using the total of N and P (kg ha−1 y−1) deposited by litterfall under each plantation
c
F. de Carvalho Balieiro et al.

N:P ratio estimated using N and P stocked (kg ha−1) in soil (0–40 cm)
d
N:P ratio calculated from N and P stocks cited by authors
e
We classified isohyperthmeric typic troposamments as Andosol, with reservations
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 79

Thus, the feedback effect of the N input and NPP (Kaye et al. 2000), associated with
the fact that N favors, in consonance with high fertility and humification of soil
organic matter (Kirkby et al. 2011) justifies such results for Hawaii. On the other
hand, the Ferralsols, in which the Brazilian plantations were established, are highly
weathered and acidic and have low fertility, which contrast with the high physical
aggregate stability that confers protection of soil C (Feller and Beare 1997; Silva
et al. 2013). Thus, even under tropical conditions, plantings associated with N2-fixing
species can store significant amounts of C in the soil. It is interesting to note that even
under a single soil class (Ferralsols), large variations in soil C stocks occur in planta-
tions, due to variations in soil clay content and climate (Voigtlaender 2012; Bouillet
et al. 2013; Voigtlaender et al. 2019). The Arenosols of Brazil and Congo, from
which the main results of this class originated, are in turn naturally lower in amounts
of C due to accelerated biochemical dynamics and reduced SOM protection, as well
as poor structure and aggregation (Feller and Beare 1997; Zinn et al. 2002). However,
it is a fact that even among the Arenosols, small variations in the clay contents of
these soils can confer significant changes in the C stocks, as well as capping of the
quartz grains by kaolinite and hematite or goethite type clays that increase the forma-
tion possibilities of organo-mineral complexes and C storage of these soils
(Scheidegger et al. 1993; Donagemma et al. 2008).
The storage of C in the soil of mixed plantations is also due to the rate of decom-
position of the deposited residues, which determines how fast the C is incorporated
into the mineral phase. By comparing monocultures, Kaye et al. (2000), Resh et al.
(2002), Forrester et al. (2013), Koutika et al. (2014), and Pereira et al. (2017)
detected greater incorporation of C in soil under N2-fixing species. However, con-
sidering the literature on mixed plantations the C stock in soil was higher but do not
show differences in relation to monocultures of Eucalyptus and legume trees
(Fig. 4.5) due to higher variability of data. In addition, C stocks occur preferentially
in the more labile compartments of SOM fractions (Bini et al. 2013; Koutika and
Mareschal 2017; Pereira et al. 2017).
These authors compared the C content of the microbial biomass as well as C and
N of the soil organic fraction (physically fractionated between 2000 and 75 μm)
and found that, in the four treatments, Eucalyptus without N fertilization,
Eucalyptus + N fertilization, Eucalyptus + Acacia mangium (E50:A50), or pure
A. mangium plantations, they differed and were significantly higher in plantings of
Acacia or in mixed plantations, confirming positive changes in microbial indica-
tors and increases in concentration and nutrient cycling in Ferralsols. When ana-
lyzing Table 4.3, it is possible to detect that, with the exception of allophanic soils,
the storage of C in poor soils follows the N:P ratio up to a certain limit. This
implies that the management of these plantations in oxidic soils with high P adsorp-
tion capacity (Lloyd et al. 2001) or sandy soil with low SOM and P reserves should
require, in the short and medium terms, a special attention to the management of P
fertilizer.
80 F. de Carvalho Balieiro et al.

Fig. 4.5 Mean (●) and SD (whiskers) of carbon stock differences (%) of N2-fixing and mixed
plantations relative to non-N2-fixing species plantations (Eucalyptus) (n = 29)

4.6  ow to Improve the Soil C Stocks in Mixed-Species

H
Plantations Under Tropical Conditions?

Based on the reviewed literature and data collected, it can be suggested that soil C
stocks in planted forests can be increased with improved management practices to
overcome environmental restraints and with a broader logic of available biological
resources.
Planted forests in the tropics and mainly in Brazil occupy marginal soils, with a
history of intense use. Thus, these soils present low fertility, high acidity, Al satura-
tion, and adsorption capacity of P and S (Leal and Velloso 1973; Motta et al. 2002).
However, huge differences in these attributes occur within the tropical climatic
zone (Sanche 1997), and may partially justify changes in species responses under
monoculture and mixed conditions described in this chapter. Although the responses
of the forest plantations to liming and fertilization of the soil are small, the non-
replacement of the exported nutrients leads to a decrease in the nutritional capital
of the soil and the future commitment of these forests. The focus of foresters shall
be on the construction of soil fertility under planted forests, with the adoption of
practices and technologies that potentiate the above- and belowground growth of
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 81

species. For the P case specifically, although most are in the non-­labile form in soil,
considered reserves exist in labile and moderately labile fractions (up to 7.7 and
15.5 Tg, respectively) (Withers et al. 2018) in areas under higher fertilizer regimes.
Especially when combined with no till, correction of acidity, and adoption of the
4R principles of nutrient management (right rate, right time, right place, and right
form) (INPI 2012) the stocks of soil natural capital related migth be at least
maintained.
In Brazilian Eucalyptus plantations, accumulation in the aboveground biomass
of N, P, K, Ca, and Mg in 100 Mg is in the range of 238–298 kg for N, 16–29 kg for
P, 123–236 kg for K, 176–590 kg for Ca, and 40–92 kg for Mg. From these totals,
35% of N, 29% of P, 36% of K, and 21% of Ca and Mg are potentially exportable
by wood (Santana et al. 2008). In the average 7-year rotations for Eucalyptus,
Gonçalves et al. (2013) recommend up to 2 Mg ha−1 of lime, 60–80 kg ha−1 of N,
60–80 kg ha−1 of P2O5, and 140–160 kg ha−1 of K2O. For trace elements around
1–5 kg ha−1 of B are applied, depending on the local water deficit, and 1 kg ha−1 of
Cu and Zn. Roughly, the natural nutritional capital of the soil (Sanche 1997;
Dominati et al. 2010) seems to be compromised, with detrimental consequences to
the organic and inorganic nutrient reserves of these forests.
Managing mixed plantings or rotations with legumes that associate with bacteria
that fix N2 from the atmosphere will lead to substantial changes in fertilizer manage-
ment given the changes in biogeochemical cycles of nutrients and differentiated
nutrient exports (Chap. 3). Legumes have a differentiated demand for P in relation
to non-N2-fixing species (Vadez et al. 1995; Inagaki et al. 2009, Venterink 2011).
Acacia mangium, the species most studied under Brazilian conditions, presents high
absorption of P in the seedling and adult phase (Inagaki et al. 2011; Santos et al.
2017), and it is very efficient in recycling internally this absorbed P, so that it depos-
its litter with a high N:P ratio (Inagaki et al. 2010; Santos et al. 2018). Since plants
and microorganisms compete strongly for soil P, affecting key soil biological
­processes and growth of tropical forests (Wieder et al. 2009; Hättenschwiler et al.
2011), strategies to reduce species competition for soil P or to increase complemen-
tarity in recycling due to P deposition should be pursued jointly with the adoption
of management practices that favor the permanence of crop residues on the soil
and SOM.
The recommendations of crop fertilization in Brazil are based on response curves
of crop production (shoot biomass or stem in the case of Eucalyptus or its productiv-
ity) in relation to the applied fertilizer dose or its availability (i.e., concentration) in
the soil (Cantarutti et al. 2007). Little or no attention has been given to changes in
the C allocated to roots by planted forests and their relationship to fertility manage-
ment and soil C stocks. Based on current hypotheses that the belowground inputs
provided by the microbial formation pathway form mineral-stabilized soil C more
efficiently than aboveground inputs partly due to the greater efficiency of formation
by the rhizosphere microbial community relative to the bulk soil community (Sokol
and Bradford 2019), it can be considered that, by managing the soil chemical limita-
tions (i.e., acidity, P, N, S, Zn concentration, among others), there will be higher
plant growth and consequently root growth, which together will increase soil C
82 F. de Carvalho Balieiro et al.

stocks. Recent works (Kirkby et al. 2011, 2014) also demonstrate the possibility of
altering the potential for soil C accumulation and sequestration of soils from the
introduction of nutrients to the soil, correcting the stoichiometry among C, N, P, and
S of the heavy fraction of organic matter (i.e., humidified). The formation of a “new-­
fine fraction of soil organic matter,” the most stable C component in soil, increased
threefold by increasing the residues with supplementary nutrients, which in other
words implies to say that we can manipulate the nutrients in favor of C sequestration
and restoration of the fertility. In other words, although Eucalyptus or Acacia (or
other leguminous species) is tolerant to acidity and high saturation of Al, it does not
mean that the practice of soil fertilizing and correction shall not be stimulated. On
the other hand, gains in productivity in oxidic soils under the correct management
of soil fertility are always accompanied by increased biomass and microbial activity
(i.e., basal respiration and enzymatic activity) and, consequently, increases in
SOM levels.

4.7 Final Considerations

As shown in this chapter, it seems clear that the establishment of mixed plantations
of Eucalyptus and Acacia mangium represents an alternative to increase soil C
stocks in marginal lands. However, the success of these plantations is not the guar-
antee to increase C stocks. It is necessary to take into account the climatic and soil
conditions of the site for the intercropped species, to perform conservationist prac-
tices of soil preparation, residue management, and conservative harvesting prac-
tices. Better results were obtained where exist appropriated climate condition for
Acacia and oligotrophic soils (e.g. sandy soils).
Finding a new set of other species (including N2-fixing and non-N2-fixing) that
have ecological and economic interest seems to be the main future challenge,
although this is not such a simple task. It could begin through a list of priority
legume tree species with litter traits that, together with eucalypt, can promote the
increase of the global stand biomass production (and also belowground) and
improvements in soil properties and functions. It is interesting to note that C seques-
tration is only an ecosystem service that the soil can provide and that the mix of
non-N2-fixing with N2-fixing trees may provide many other ecosystem services,
such as flood mitigation; greenhouse gas regulation; filtration and recycling of
­nutrients; and biodiversity preservation among others. In Chap. 10, these services
are presented and discussed.
New researches should also elucidate under which arrangements and trees den-
sity could provide positive ecological interactions (complementarity and competi-
tive reduction) that can increase the biomass production (above- and belowground)
and accelerate litter decomposition and soil C sequestration.
Finally, due to the close relationship between the N and C cycle, it has been
reported that as a result of the presence of N2-fixing trees in Eucalyptus plantations
positive changes in soil N stocks are more pronounced than for C (Bernhard Reversat
1996; Voigtlaender 2012; Rachid et al. 2013; Voigtlaender et al. 2019; Rocha et al.
4 Litter Decomposition and Soil Carbon Stocks in Mixed Plantations of Eucalyptus… 83

2019). These general results confirm that the presence of legumes in Eucalyptus
plantation might contribute to reducing the need for mineral N fertilization in the
long term and increasing the soil nutritional capital. New mixtures of species and
arrangements of mixed plantations in combination with nutrient management could
enhance C sequestration and produce a more stable organic matter (humus).

Acknowledgments To the National Council for Scientific and Technological Development

(CNPq) for the Productivity Grant given to the first author. We also thank the Fundação de Amparo
à Pesquisa do Estado de São Paulo (FAPESP) and the Fundação de Amparo à Pesquisa do Estado
do Rio de Janeiro (FAPERJ) for the financial support of our research, the field work and laboratory
analyses and to Coordination of Superior Level Staff Improvement (CAPES) for the grants to the
students involved.

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Chapter 5
Soil Bacterial Structure and Composition
in Pure and Mixed Plantations
of Eucalyptus spp. and Leguminous Trees

Caio Tavora Coelho da Costa Rachid

5.1 Introduction

It is in the first centimeters belowground that the most diverse and rich biodiversity
of our planet can be found. In fact, a single soil sample can harbor billions of organ-
isms assembling thousands to millions of species of bacteria, archaea, and fungi
(Whitman et al. 1998; Lozupone and Knight 2007). In this environment, they form
very complex communities with a highly branched network of ecological interac-
tions (Bonfante and Anca 2009; Fuhrman 2009).
Bacteria populations far exceed fungi and archaea in numbers (Rachid et al.
2013; Siles and Margesin 2016), and they play important roles, such as in nutrient
turnover, phytohormone production, and biocontrol that affect soil functioning and
plant productivity (Chaparro et al. 2012).
Obviously, such rich and diverse community poses a challenge to be studied and
understood. In a scale of an average bacterium, 1 cm can represent a huge distance,
with very different environmental conditions in terms of atmosphere, pH, and quan-
tity and quality of organic and inorganic matter, among others. All these factors,
along with temperature, water, and biological interactions, will affect the structure
of the bacterial community (Fierer 2017).
However, what exactly bacterial community structure means? It means all the
abundance and composition of bacteria in a given environment. Still more spe-
cifically, how many species it encompasses (bacterial richness, alpha diversity),
who they are (bacterial composition), how many they are (bacterial abundance),
and how they vary among sites from the same environment (beta-diversity). All
these factors together compose the bacterial structure and show all aspects of the
bacterial diversity (Konopka 2009).

C. T. C. d. C. Rachid (*)
Institute of Microbiology, Federal University of Rio de Janeiro, Ilha do Fundão, RJ, Brazil
e-mail: caiorachid@micro.ufrj.br

© Springer Nature Switzerland AG 2020 91

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_5
92 C. T. C. d. C. Rachid

How bacterial community structure is modulated is still in debate in literature.

Many studies have shown that there are some factors with very strong effects over
the bacterial community. Among them, the pH, salinity, and organic matter content
(Fierer and Jackson 2006; Lozupone et al. 2006; Lozupone and Knight 2007; Ding
et al. 2015) are the strongest modulators. Some authors argue that the bacterial com-
munity suffers very little influence of the plant coverage (Fierer 2017). However, the
impact of the plant on the soil bacterial community, especially in the rhizosphere
zone (soil region very close and under influence of the plant roots), has also been
very well documented (Berg and Smalla 2009; Mitchell et al. 2010; Rachid et al.
2013). In this context, mixed plantations are one of the best models to demonstrate
how plants can influence the soil microbial community, and how it can cause impact
on the system’s ecology and functioning.
Regarding soil and plant characteristics, previous studies have shown that
Eucalyptus stands intercropped with leguminous trees affect positively a series of
soil attributes increasing soil organic matter and other attributes. Soil nitrate con-
centration, biomass productivity, and water use efficiency, among others, are also
increased, when compared to pure Eucalyptus plantations (Forrester et al. 2005,
2006; Laclau et al. 2008; Balieiro et al. 2008; Voigtlaender et al. 2012; Rachid et al.
2013; Koutika et al. 2014). Soil’s available P in mixed plantations has increased at
the beginning of the rotation but decreased at the end, especially in sandy soils
(Rachid et al. 2013; Koutika et al. 2014), leaving to an apparent P (and N, of course)
control over the litter decomposition (Santos et al. 2017).
Behind most of these soil changes, there is the essential role of the microorgan-
ism associated with the forestry system. The co-cultivation efficacy relies, among
other factors, on the ability of the legume trees to establish symbiotic relationships
with nitrogen-fixing bacteria, which, in turn, can increase soil N levels and improve
nutrient cycling (Rachid et al. 2013; Bernhard-Reversat 1988; Santos et al. 2017;
Tchichelle et al. 2017; Voigtlaender et al. 2019). Additionally, the introduction of
another plant species can change bacteria, archaea, and fungi communities associ-
ated with soil, altering the complex biological network responsible for nutrient turn-
over and soil health. Changes in the microbial community, therefore, could lead to
changes in litter decomposition and soil nutrient balance, which in turn will reflect
in plant productivity (van der Heijden et al. 2008; Chaparro et al. 2012).
In this chapter, we present briefly the role of the bacterial community in forestry
ecosystems and its response from the resulting interaction of mixing different tree
species in a co-cultivation system. Finally, we explore the biotechnological poten-
tial of the microorganisms to improve the sustainability of wood production.

5.2 Soil Bacterial Functioning

The soil microbiome (all microbes of a given site) can cause impacts on the plant
productivity by many ways. For example, symbiotic nitrogen-fixing bacteria, such
as Rhizobiales, Azospirillum, and Frankia, among others, can improve soil N levels,
5 Soil Bacterial Structure and Composition in Pure and Mixed Plantations… 93

and bacteria and archaeal nitrifiers, such as Nitrosomonas, Nitrosococcus, and

Nitrososphaera, can change the predominant form of inorganic nitrogen. Many
microbial groups including the bacteria Bacillus and the fungi Aspergillus can
increase P availability and acquisition by plants by exudation of organic acids.
Additionally, microorganisms can interfere in competitive interactions, helping or
suppressing the growth of a given plant group by phytohormone production or
inhibiting a pathogen by the production of antimicrobial substances (van der Heijden
et al. 2008). These are some examples of specific functions played by well-described
organisms. In nature, many other microorganisms, most of which are still unknown,
play these and many other roles, in highly diverse communities forming a very
complex network of interaction.

5.3  oil Bacterial Communities in Pure and Mixed

S
Eucalyptus Plantations

The soil bacterial community of Eucalyptus plantations has been described for a
number of sites in different locations around the globe. In a broader view of soil
bacterial composition, Eucalyptus plantations do not differ from other cultivations,
with most of the studies showing predominance of the Proteobacteria phylum, fol-
lowed by Acidobacteria, Actinobacteria, Planctomycetes, and Firmicutes among
others, as evaluated in Brazil (Silveira et al. 2006; Pereira et al. 2017; Cuer et al.
2018; Rachid unpublished) and China (Li et al. 2018). However, each study showed
special aspects of the community when compared to native forests or other plant
species cultivated in the same area.
In a Brazilian traditional forest-producing region, located in Minas Gerais state,
Cuer et al. (2018) studied two adjacent Eucalyptus urograndis plantations—a
recently logged site that harbored new seedlings and an adult plantation—and com-
pared them to a site hosting native vegetation. They showed that plant harvesting
and implementation of a new rotation can significantly change the soil bacterial
community in a short term, mainly by reducing the relative abundance of
Acidobacteria and increasing Actinobacteria. When comparing with an adjacent
field with native forest, it was shown that Eucalyptus plantations had a distinct bac-
terial community structure. The authors suggested that the main driver of the
observed differences in microbial community structure was land use type, as
opposed to management practices (i.e., plantation, logging, and initiation of new
rotations) or soil characteristics. Surprisingly, the Eucalypt plantation showed
higher bacterial diversity compared to the fragment of native rainforest. This result
was confirmed in an independent sampling, 9 months after the first (Monteiro et al.
unpublished data). Higher bacterial diversity in Eucalypt compared to a secondary
forest has also been demonstrated in China (Lan et al. 2017). Harboring a higher
diversity is frequently associated with an indication of higher stability in the ecosys-
tem. However, the authors argue that in this case it is probably correlated with
higher primary productivity in young forests.
94 C. T. C. d. C. Rachid

The development of Eucalypt plantations was also associated to increases in bac-

terial community biomass. The proposed mechanisms are diverse. In Eucalyptus
grandis, it has been associated with increased inputs of C from residues or roots
(Zhang et al. 2012), and in Eucalyptus urophylla it was suggested that it could be
caused by the decrease of the dissolved organic carbon (DOC) of the soil. The
reduced DOC would give a competitive advantage to bacteria compared to fungi
and would increase the ratios of bacteria:fungi along the chronosequence (Wu et al.
2013). Contrastingly, the opposite was also suggested in which E. camaldulensis
could negatively impact the microbial community, reducing the microbial biomass
and catabolic diversity, mainly due to soil acidification and accumulation of pheno-
lic compounds (Soumare et al. 2016). Evaluating soil microbiological attributes in
pure and mixed forest plantations of Acacia mangium and Eucalyptus grandis at the
end of a second rotation, Zagatto et al. (2019) did not observe any change among
treatments for Cmic, CO2-C, dehydrogenase, and Cmic/Ct, but only for qCO2-
­C. The qCO2-C was lower for Acacia plantations than in pure and mixed Eucalyptus.
On the other hand, at the beginning of this rotation (27 and 39 months after plant-
ing) Pereira et al. (2018) detected a significant higher microbial C content in Acacia
and mixed plantations than in monoculture of Eucalyptus.
The general pattern shows the prevalence of increased bacterial biomass or activ-
ity in this forestry system. This is often considered a good indicator of soil health.
An active microbial community is important to keep nutrient cycling and soil fertil-
ity, which will direct influence crop productivity and sustainability.
However, these studies were based on indirect measurements, mostly in micro-
bial biomass and phospholipid fatty acid (PFLA) contents. Few studies used more
precise techniques to quantify bacterial communities, such as real-time PCR
(qPCR). The qPCR can provide a measurement of copies of a given gene per gram
of soil. Usually, bacterial communities are quantified through the quantification of
the gene coding for the subunit of the 16S rRNA, a molecular marker for bacteria.
Studies in three different locations in Brazil showed no change in bacterial abun-
dance comparing Eucalyptus to native forests or to Acacia mangium plantations in
upper layers of soil (Rachid et al. 2013; Pereira et al. 2017; Cuer et al. 2018).
Therefore, it is very likely that most of the impacts caused by Eucalyptus on the soil
bacterial community are qualitative and not quantitative.
In recent years, studies of soil microbiology under Eucalypt plantations shed
light on different management regimes, on which we will focus from now on to
describe the intercropping systems. The first report on soil bacterial community
in mixed Eucalypt plantations arose in 2013 and was based on the association of
Eucalypt with Acacia mangium. Using indirect measurements of the community,
such as microbial respiration, dehydrogenase activity, Cmic, and Nmic, Bini et al.
(2013) showed that these attributes present high variation in the initial stage of
development of the mixed stands (from 2 to 20 months). The high variability
poses a challenge on data interpretation, without a clear pattern, but considering
all attributes with other variables in multivariate analysis, they showed that
mixed stands are different from monocultures starting at month two. According
to the authors, despite the high variability of the data within treatments, the co-
5 Soil Bacterial Structure and Composition in Pure and Mixed Plantations… 95

cultivation e­ stablished a new microbial status, with synergistic effects on the two
plant species in maintaining and stimulating biogeochemical cycling with bene-
ficial effects over the system.
Later, this analysis was repeated with older stands (27 and 39 months) (Pereira
et al. 2018). The study confirmed that nutrient cycling in pure Eucalypt systems is
different from when Acacia is present, with changes in enzymatic and metabolic
activity. While some enzymes, such as urease, amidase, and dehydrogenase, tend to
present higher activity in pure Eucalypt plantations, the intercropped system tends
to present higher microbial biomass C and increased C and N concentrations in soil
organic matter, which was interpreted as a gain in soil health by the authors.
Direct measurements were also performed to assess how mixed plantations inter-
fere in the bacterial structure. Using DGGE and qPCR for bacteria (16S rRNA), and
genes involved in nitrogen cycling (nirK, amoA, nifH), Rachid et al. (2013) showed
that mixed plantation resulted in the integration of the bacterial community present
in the monocultures. Additionally, they showed that acacia stands presented higher
amounts of nitrifiers and lower amounts of denitrifiers in the soil, and this could be
directly linked to the higher levels of nitrate found in acacia monocultures and
mixed plantations, which is an indication of better nutrient status of the soil.
Using high-throughput DNA sequencing, the bacterial community of Eucalyptus
and Acacia monoculture and mixed plantations was studied with taxonomic detail
in the superficial soil layer. The results showed that the soil bacterial community
integration occurred, but with higher influence of Acacia on the structuring of the
soil bacteria, compared to Eucalyptus, especially in the first 3 m belowground
(Pereira et al. 2017).
Very few studies addressed the soil bacterial community in mixed plantations of
Eucalypt with legume trees, other than Acacia. Among the exceptions, there is one
study of Eucalypt with Sesbania, in which the plant consortium was evaluated for
its capacity for reforestation of degraded lands. The study measured the microbial
respiration and the hydrolysis of fluorescein diacetate (FDA) in monospecific and
mixed systems, and showed that mixed systems present less seasonal variation and
higher microbial activity (de Oliveira Paulucio et al. 2017).
We are still far from really understanding completely how plants modulate the
soil microbial community. However, altogether, these studies leave no doubt about
the influence of the plant on the soil microbiome. While there are some authors who
argue that Eucalypt plantations can cause negative impact on the soil microbial
community, recent studies have shown no basis for this affirmation. Still, they have
also shown that the metabolic potential of the soil microbial community can be
improved when Eucalypt is associated with a leguminous tree. In fact, the relation-
ship between these plants is so intimate that the presence of one plant can interfere
in the endophyte colonization of the other plant, as previously demonstrated with
Eucalypt and Acacia (Fonseca et al. 2018).
Obviously, the decision whether Eucalypt should be or not be mixed with other
plants cannot be taken only under the soil microbial perspective. Productivity, logis-
tics, and economy are factors to be analyzed, and other factors could be incorpo-
rated in this decision, depending on the ecosystem services expected by the mixed
96 C. T. C. d. C. Rachid

planted forest (see Chap. 11). However, the soil microbial community should always
be considered, since the microbial community is the foundation of soil fertility,
health, and sustainability and, in an ultimate analysis, these will turn back into pro-
ductivity and economy.
Despite the numerous questions, there is a strong indication that the consortium
of Eucalypt with a legume tree can integrate the soil bacterial community, increas-
ing microbial activity and system stability with direct benefits to soil biogeochem-
istry, as discussed in other chapters of this book.

5.4  lant Growth-Promoting Endophytic Bacteria

P
and the Potential for Eucalyptus

It has been proposed that each one of 300,000 species of superior plants harbor
endophytic bacteria inside their tissues (Strobel et al. 2004). In fact, studies have
shown that inside plant leaves, stem, and roots it is possible to find a rich bacterial
community (Gottel et al. 2011; Bodenhausen et al. 2013; Akinsanya et al. 2015).
During the evolution, plants and endophytic bacteria developed a symbiotic rela-
tionship, with mutual benefits (van der Heijden et al. 2008; Rout 2014). Plants pro-
vide shelter and organic compounds for bacterial nutrition, while bacteria can play
many positive roles for plants.
The benefits of endophytic bacteria for plants include nutritional improvement
through biological nitrogen fixation, phosphorus bioavailability, and iron uptake
(Hallmann et al. 1997); growth promotion through phytohormone production,
which can promote plant rooting and stem development (Bent et al. 2001); and also
fitness improvement through defense against pathogens and hydric stress among
others (Sala et al. 2007; Ferreira et al. 2008).
Eucalypt endophytic bacteria have been studied by culture-dependent and -inde-
pendent techniques. Ferreira et al. (2008) showed that seeds from many Eucalypt
species harbor endophytic bacteria. Among the bacterial genera found in seeds and
seedlings were Bacillus, Paenibacillus, Enterococcus, and Methylobacterium. The
vertical transmission (from one generation to another) of a given bacterium is sug-
gested as an indicator that symbiotic relationships of the plant with the transmitted
microorganisms are of great importance for the species fitness (Zilber-Rosenberg
and Rosenberg 2008).
Miguel et al. (2016) showed using DGGE—a molecular typing technique—
that Eucalyptus leaves harbor a complex endophytic microbial community, how-
ever, with a very similar profile among different plants and over different stages
of development. They also showed the occurrence of diazotrophic bacteria
inside the leaves. Among the cultured microbial community, they reported the
isolation of Pantoea, Stenotrophomonas, Massilia, Paenibacillus, Terrabacter,
Rhizobium, Agrobacterium, Novosphingobium, Micrococcus, Streptomyces,
Pseudoxanthomonas, Caulobacter, and Ochrobactrum. More recently, the first
study using high-throughput DNA sequencing technology to understand the
5 Soil Bacterial Structure and Composition in Pure and Mixed Plantations… 97

endophytic microbial community associated with Eucalyptus roots was pub-

lished (Fonseca et al. 2018). The authors reported an unprecedented biodiversity
living inside Eucalyptus roots, with the occurrence of approximately 360 differ-
ent bacterial genera with the most abundant ones being Mycobacterium,
Bradyrhizobium, Streptomyces, Bacillus, Actinospica, and Burkholderia. They
showed that many of these genera were associated with nitrogen-­fixing bacteria
and also that environmental factors can change the community structure inside
the roots.
The occurrence of large amounts of diazotrophic bacteria associated with
Eucalyptus leaves and roots is surprising. This is not because these bacteria do not
colonize trees. For instance, Acacia has promiscuous nodulation, being capable to
symbiotically associate with Rhizobium and Bradyrhizobium among other nitrogen-­
fixing bacteria (Galiana et al. 1990, 1994; Le Roux et al. 2009; see Chapter 6), and
these associations are of great importance in plant nutrition and nutrient cycling.
However, Acacia is a legume tree, and it is a common knowledge that this family of
trees developed symbiotic association with nitrogen-fixing bacteria. However,
Eucalyptus has never been considered a plant which benefits from this association.
Only recently we learned that nitrogen-fixing bacteria are highly abundant also in
Eucalyptus (Miguel et al. 2016; Fonseca et al. 2018), and despite the fact that they do
not form nodules, we cannot disregard their potential to improve Eucalyptus nutrition.
Due to the ability to improve plant development, there is a great interest in the
selection of microorganisms as plant inoculum. In general, these studies include the
cultivation of endophytic bacteria in culture medium, followed by in vitro tests to
evaluate the capacity of the bacteria to perform specific functions, such as phospho-
rus solubilization and indole acetic acid (IAA) production, to grow in the absence of
nitrogen (indication of biological nitrogen fixation), to produce siderophores, or to
inhibit a given phytopathogen. The best bacterial lineages usually are identified and
tested in vivo, with inoculation of seed or micro-propagated plants.
Paz et al. (2012) tested seven selected endophytic Bacillus sp. lineages regarding
their ability to improve plant rooting and growth. When tested in vivo they found
that only one of them significantly increased the growth of the root and aerial parts
of Eucalyptus plantlets. Mafia et al. (2009) evaluated effectiveness of ten plant
growth-promoting rhizobacteria (including the genera Pseudomonas, Bacillus,
Stenotrophomonas, and Frateuria) for the control of mini-cutting rot of Eucalyptus
caused by Cylindrocladium candelabrum and Rhizoctonia solani. They showed that
one lineage of Pseudomonas fulva reduced the incidence of mini-cutting rot, under
nursery conditions, by 33% compared to the control, and by 27% compared to a
fungicide treatment. Teixeira et al. (2007) evaluated the rooting effect of 107 lin-
eages of bacteria isolated from Eucalyptus rhizosphere on seedlings propagated by
mini-cuttings. They found ten isolates with promising results, based on rooting effi-
ciency and root biomass improvements. The best lineage was affiliated to Bacillus
subtilis and induced a 219% increase in rooting frequency and a 223% increase in
root biomass compared to the control.
It is very common, during the development of a bacterial inoculum, to get frus-
trating results when testing the effects in vivo. The main reason is that the in vitro
98 C. T. C. d. C. Rachid

conditions are quite different from the in vivo ones. It is impossible, with the actual
methods, to cultivate most of the microorganisms living associated with the plants.
In general, the ones selected are those fast-growing microorganisms with high affin-
ity to the culture conditions. However, very frequently they are not part of the domi-
nant microbial community, and because they cannot thrive in a highly competitive
natural environment, they fail to colonize the plant and, therefore, fail to develop
growth-promoting activity. For this reason, it was proposed that a bacterial consor-
tium for plant inoculation should be developed on some naturally abundant bacterial
genera (Fonseca et al. 2018).
In recent research (unpublished data), Fonseca and colleagues got a deeper eval-
uation of plant growth-promoting capacity of some bacterial lineages isolated from
Eucalyptus roots. They contrasted the list of the most abundant genera found in
Eucalyptus with the list of bacterial lineages with the best capacity in inorganic
phosphorus solubilization, phytate mineralization, IAA production, and nitrogen
fixation capacity. From these, they selected four lineages, belonging to genera
Paraburkholderia, Methylobacterium, Paenibacillus, and Mesorhizobium, to for-
mulate a bacterial consortium. The results showed that the inoculation of mini-­
cutting propagated seedlings can significantly improve seedling survival, below- and
aboveground biomass, and average plant height.

5.5 Final Comments

The use of plant growth-promoting endophytic bacteria represents a great tool for
improving Eucalyptus and other forestry species cultivation. Still, it is a highly
unexplored world for forestry companies with many gain opportunities. Despite the
costs and time associated with the selection and tests of bacterial lineages for this
application, the use of biotechnology has very low costs, with the capacity to be
applied to any size production and with minimal changes in the seedling production
workflow. The development of this strategy should be encouraged and understood
as a low-cost green technology, which beneficial effects include nutrient optimiza-
tion, higher survival rates, and better plant fitness.

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Chapter 6
Biological Nitrogen Fixation (BNF)
in Mixed-Forest Plantations

Sergio Miana de Faria, Fabiano de Carvalho Balieiro, Ranieri Ribeiro Paula,

Felipe Martini Santos, and Jerri Edson Zilli

6.1 Introduction

The emergence of symbiosis between leguminous plants and bacteria of the

Rhizobia group (bacteria able to induce nodules and fix nitrogen) remains clouded
in mystery and speculation (Sprent 1994; Brockwell et al. 2005; Doyle 2016;
Parniske 2008). However, because the legume plants also possess the ability to take
up N from soil, it is assumed that they were associated with diazotrophic bacteria
(nitrogen-fixing bacteria) primitively in a parasitic mode, later evolving to infection,
nodulation, and fixation patterns (Faria et al. 1987; Sprent 1994, 2007). It is impor-
tant to realize that symbiosis is not obligatory for the plant or bacteria, but when
associated both symbionts have ecological advantages of survival and competition
(Sprent 2007).
The reason why some legume species do not nodulate, even though different
leguminous species are capable of similarly accumulating N in the tissue, is not
fully understood. For example, the genus Cassia comprises about 30 tree species, in
which nodulation and nitrogen fixation remain unconfirmed. On the other hand, the
genus Chamaecrista (closely related to Cassia genus) with more than 250 species
that are herbs, shrubs, and arboreal types is an exclusive nodulant (de Faria et al.

S. M. de Faria · J. E. Zilli (*)

EMBRAPA Agrobiology, Brazilian Agricultural Research Corporation, Seropédica, RJ, Brazil
e-mail: jerri.zilli@embrapa.br
F. de Carvalho Balieiro
EMBRAPA Soils, Brazilian Agricultural Research Corporation, Rio de Janeiro, RJ, Brazil
R. R. Paula
Center for Agricultural Sciences and Engineering, Federal University of Espirito Santo,
Alegre, ES, Brazil
F. M. Santos
Federal Rural University of Rio de Janeiro, Seropédica, RJ, Brazil

© Springer Nature Switzerland AG 2020 103

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_6
104 S. M. de Faria et al.

2010; Sprent 2007, 2009; de Faria et al. 1999; Moreira et al. 1992). It is intriguing,
however, that these two leguminous genera with similar capability to accumulate N
in their tissues vary in their nodulation features.
Is it possible that the ability of some legumes to accumulate N may have exerted
a selection pressure driving towards symbioses, being a way of legumes adapting to
the increasing demand for N in a limiting environment? If so, and given that the
biological nitrogen fixation (BNF) event in prokaryotes is so old, it is questionable
why plants would not have acquired the ability to form a structure (“rhizoplast”),
resembling an organelle. Moreover, why most plants do not nodulate, including
some legumes, is unclear. It is probable that the selection pressure was not strong
enough for the plants to acquire nif genes (genes found in all diazotrophs required
for structure, biosynthesis, and regulation of nitrogenase, the enzyme responsible
for fixing N) and the plant-bacteria relationship is still evolving (Postgate 1992;
Coba de la Peña et al. 2018). Probably, some groups of plants (especially the
Papilionoideae subfamily and Mimosoideae clade) shared a close relationship with
bacteria that had this enzymatic apparatus and took advantage of this association
(Polhill et al. 1981; Sprent 2007).
BNF is the primary N intake form in agroecosystems, promoting equilibrium
between atmospheric N2, being the reactive forms incorporated in soil and organ-
isms. For a number of reasons (such as the cost of production and environmental
impact of synthetic fertilizers), BNF has become indispensable for sustainable agri-
culture on the planet (Crews and Peoples 2004), with Brazil being an excellent
example of leveraging this process in annual crops, such as soybeans, beans, and
others (Hungria and Mendes 2015).
Besides, BNF has also been useful in the restoration of degraded areas, part of
the recovery technologies, which are based on the introduction of pioneering, fast-­
growing N2 -fixing legumes (Franco et al. 1995; Chaer et al. 2011; Balieiro et al.
2018). In this case, the inoculation of legume seeds with rhizobia supplies plants
with nitrogen often scarce on severely degraded lands, improves soil quality, and
supports plant growth and ecological succession (Parrota et al. 1997; Franco and
Faria 1997; Batterman et al. 2013).
Tropical soils, like most in Brazil, are highly weathered and poor in nutrients and
organic matter, which require the supply of nutrients for adequate plant growth.
Forest plantations, whether pure or mixed, depend on external inputs for adequate
growth, although water availability exerts substantial control over growth and bio-
mass accumulation (Stape et al. 2010; Moraes Gonçalves et al. 2013). This is espe-
cially important when it comes to fast-growing species, such as eucalyptus, which
can accumulate about 155 kg ha−1 of N in biomass during the first year after planting
(Laclau et al. 2010). It has been shown, however, that the introduction of N2-fixing
legumes in a consortium with fast-growing non-N2-fixing species may be a strategy
to promote gains in biomass production (wood), decrease the dependence on chemi-
cal nitrogen fertilizer by companion species (Chap. 1), and contribute to several soil
processes, especially those dependent on the soil organic matter (see Chaps. 4
and 10).
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 105

This chapter addresses the biological fixation of N2 as a critical ecological facili-

tation strategy in mixed-forest plantations, allowing N fixation to act positively on
the development of non-N2 -fixing species. The mixture of fast-growing N2-fixing
species is capable of improving the quality of soil organic matter, improving N sta-
tus in the system and crop productivity (Forrester et al. 2005; Voigtlaender et al.
2012; Rachid et al. 2013; Santos et al. 2018). A compilation of information, without
the commitment to exhaust the literature, was made by trying to give numbers to the
benefits of nodulating bacteria. The potential use of the plant microbiome and
growth-promoting microorganisms in forestry is still incipient, but very promising.
This subject is discussed in Chap. 5.

6.2 Nodulating Bacteria and Symbiosis Establishment

Into the plant kingdom, members of the family Leguminosae have the ability to
interact with diazotrophic bacteria and form nodules (Fig. 6.1). The nodules can be
located in the roots of major legume species and in the stem of a few, as seen in the
genera Aeschynomene, Sesbania, and Neptunia that grow in the flooded regions
(Fig. 6.1).
The term “rhizobium” has always represented a group of gram-negative, obligate
aerobic, non-endospore-forming alpha-proteobacteria that induce plants to form
nodules through highly complex molecular signaling (Parniske 2008; Doyle 2011,
2016; Clúa et al. 2018). The taxonomy of nitrogen-fixing bacteria that associate
with legumes has been frequently reviewed, especially as they have been identified
as nodulating (Chen et al. 2006; Peix et al. 2015; Andrews and Andrews 2017).
Nowadays, rhizobia represent several lineages within the alpha-proteobacteria,
and hence the term “rhizobia” does not represent a single taxon but refers to a poly-
phyletic cluster of bacterial lineages having similar functions. Most known rhizobia

Fig. 6.1 Spherical stem nodules of Aeschynomene sp. (approx. 3 mm in diameter); spherical
radicular nodule of Dalbergia nigra (approx. 2 mm in diameter) and branched root nodules of
Andira nitida (approx. 5–10 mm in length)
106 S. M. de Faria et al.

still belong to the family Rhizobiaceae [Rhizobium, Ensifer (Sinorhizobium),

Allorhizobium, Parahizobium, Neorhizobium, Shinella], Phyllobacteriaceae,
Mesorhizobium, Aminobacter, Phyllobacterium, Brucellaceae (Ochrobactrum,
Methylobacterium, Microvirga), Bradyrhizobiaceae (Bradyrhizobium),
Xanthobacteraceae (Azorhizobium), and Hyphomicrobiaceae (Devosia), but some
others belong to beta-proteobacterial genera in the family Burkholderiaceae
(Paraburkholderia, Cupravidus, and Trinickia) (Andrews and Andrews 2017; Peix
et al. 2015; Sprent et al. 2017).
For the establishment of a mutual symbiosis, as is usual in the symbiosis between
rhizobia and nodulating legumes, it is necessary that a series of physical, biochemi-
cal, physiological, and environmental factors complement each other. Several
authors (Moreira and Siqueira 2006; Parniske 2008; Doyle 2011, 2016) describe
that the fundamental stages for the establishment of symbioses are (1) preinfection,
in which symbionts are recognized and interactions occur between surface bacteria
and plant; (2) plant infection by the bacteria and formation of nodules; and (3) func-
tioning of nodules, i.e., nitrogen fixation. According to the authors, several dozen
genes are involved in the process of N2 fixation in nodule-fixing bacteria, which
influence everything from the recognition of the host plant by the bacteria to the
transport of carbon from the plant to the bacteroid (the active form of nitrogen-­
fixing bacteria).
The pink color inside the nodule indicates the effectiveness of nodulation and the
efficiency of nitrogen fixation. It shows the presence of active leghemoglobin,
which is needed to supply oxygen at low tension for the nodules to function. The
oxygen tension inside the nodules, which is usually low, is necessary because nitro-
genase (the enzyme responsible for nitrogen fixation) is irreversibly inhibited in the
presence of high O2 concentration (Raymond et al. 2004). The efficiency of nodula-
tion can be measured by the benefits of symbiosis to the host and the system as a
whole, such as higher production of plant biomass, significant accumulation of
nutrients (including N), and even transfer, directly or indirectly, of N to non-N2- fix-
ing plants.
Among the principal genera of nodulating bacteria of native forest legumes stud-
ied from the Amazon, Cerrado, Caatinga, and Brazilian Atlantic Forest
Bradyrhizobium, Rhizobium, Ensifer, Mesorhizobium, and Paraburkholderia are
the most common (Moreira and Siqueira 2006; Bournaud et al. 2013; da Silva et al.
2014; Zilli et al. 2014; Reis Jr et al. 2010).
The induction of nodules of forest legumes occurs through several bacterial gen-
era; however, there is a certain specificity of response in terms of efficiency in nitro-
gen fixation (de Faria et al. 1999). This specificity appears to increase as symbionts
coevolve in the same geographic region. For example, the species Mimosa pudica
and even other members of Mimosa tribes are efficiently and almost exclusively
nodulated by bacteria of the genus Rhizobium in Central America, whereas, in the
Brazilian Cerrado, nodulation is almost exclusively by Paraburkholderia (Bontemps
et al. 2016). Local climate conditions and specifically edaphic (pH) factors contrib-
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 107

ute to the emergence of this specificity (Bontemps et al. 2016; Pires et al. 2018; Reis
Jr et al. 2010). Patterns relating to strains of Rhizobium nodulating species o­ riginated
in Central America and Paraburkholderia in South America have also been observed
in the Calliandra genus (tribe Ingae) (Silva et al. 2018).
Species of the Acacia genus, commonly used in mixed plantations, are nodulated
by both Rhizobium and Bradyrhizobium and less frequently by Ensifer,
Mesorhizobium, and Paraburkholderia (Lawrie 1981; Barberi et al. 1998, Sakrouhi
et al., 2016). However, there are important differences in the nodulation efficiency
and N2 fixation even within a genus and species to which the strains belong (Galiana
et al. 2002).

6.3  he Ability of the Forest Legumes to Nodulate and Fix

T
Nitrogen

The family Leguminosae was recently reviewed and classified into six subfamilies:
Duparquetioideae, Cercidoideae, Dialioideae, Detarioideae, Papilionoideae, and
Caesalpinioideae, with the latter also encompassing the traditional subfamily
Mimosoideae, which became a clade of Caesalpinioideae (LPWG 2017). The nodu-
lation is mostly concentrated in the subfamily Papilionoideae, in which about 97%
of the investigated species can nodulate. In this subfamily, only some tribes and
genera do not nodulate, such as Dipteryxeae, part of the Dalbergieae (Vaitarea and
Vataereopsis), Swartzieae (only some species of the genus Swartzia nodulate), and
some genera of Sophoreae. Similarly, in the subfamily Papilionoideae, the Mimosoid
clade within the subfamily Caesalpinioideae, 95% of the species fix nitrogen associ-
ated with rhizobia. For the other members of the old subfamily Caesalpinioideae,
until recently, only 25% were associated with rhizobia-producing nodules and these
are concentrated in some genera of the Cassieae (Chamaecrista), Caesalpinieae
(Melanoxylon, Moldenhawrea, Tachigali, Dimorphandra, and other genera in this
tribe) (Allen and Allen 1981, de Faria et al. 1989).
Nodulation and consequently the BNF benefits usually occur when nitrogen is
scarce in the environment, and therefore in mature forests it is rare to find nodules
in the species capable of associating with rhizobia (de Faria et al. 1984; Winbourne
et al. 2018; Piotto et al. 2009), with reduced BNF contributions (Nardoto et al.
2014). Likewise, nitrogen fixation will occur at a higher intensity when the species
requires more nitrogen, that is, during its exponential growth phase. Although the
majority of soils have native bacteria capable of nodulating tree species typically
used in mixed plantations, significant gains in establishment, growth, and produc-
tivity can be obtained when seedlings are inoculated with selected strains (Franco
and de Faria 1999; Galiana et al. 2002).
108 S. M. de Faria et al.

6.4  razilian Rhizobia Selection Program for Leguminous

B
Trees

Embrapa Agrobiologia is a pioneer and internationally recognized for its work in

the selection and maintenance of diazotrophic bacterial germplasm associated with
native and introduced leguminous trees. Since 1960, this research center isolated
over 5000 strains of rhizobia from different regions of Brazil. More than 2600
botanical specimens were investigated for nodulation capacity, which includes more
than 80 genera and 400 forest species reported for the first time as nodulants or non-­
nodulants. It is worth remembering that the pioneering work developed with tree
species was performed by Dr. Döbereiner and her group in the 1960s, including the
preliminary studies on host specificity of the sabiá (Mimosa caesalpiniifolia)
(Campelo and Döbereiner 1969). Native of the Caatinga biome, this legume origi-
nated from Caatinga (Brazilian Northeast), and is widely distributed throughout the
country as it has several uses such as live fences, charcoal, firewood, erosion con-
trol, forage, honey flowers, and others.
A program to obtain and select strains of rhizobia for legumes initially requires
the confirmation of the ability of the isolate to induce nodulation in a host, but in
Brazil, given the large diversity of legume species and the limited knowledge of the
flora it is often necessary first to evaluate nodulation capacity.
Roots of individual plants can be examined directly in the field for the presence
of nodules. If present, the nodules can be collected for bacteria in the laboratory.
Subsequent purification and selection of the most efficient isolates for nitrogen fixa-
tion in the target plant species can be performed. The presence of nodulation can
also be confirmed in the greenhouse by inoculating seed collected in the field where
a target legume grows with a set of several bacteria from different groups. The
inoculation with a mixture of rhizobia strains of different origin along with the soil
from the native location where the legume grows is another strategy.
After confirmation of nodulation in specific species, the selection of most effi-
cient strains for biological N2 fixation is the next step. It is important to note that
some specific responses exist in terms of nitrogen fixation efficiency by a particular
group and/or several bacterial strains, and that due to such preferences it may be
necessary to select the most efficient strain for each forest species.
Embrapa develops trials that are divided into three phases and follow the official
rules of the Ministry of Agriculture, Livestock and Food Supply—MAPA (Brazil
2011). In the first phase, each legume species is tested aseptically in “Leonard jars”
containing a mixture of sand and vermiculite (Vincent 1970), with strains of several
different origins. In this phase, the nature of the isolates (if they are rhizobia) is
confirmed, besides the N2 fixation potential. The best strains are tested in soil, and
unsterilized conditions (second-phase test). This phase evaluates the competitive-
ness and efficiency of bacteria in comparison to those in the native soil. Nursery and
field conditions are part of the third phase.
Studies developed over the last decades by Embrapa Agrobiologia have led to the
selection of several rhizobia strains for different legume species. These strains were
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 109

Fig. 6.2 Legume tree genera and respective rhizobia genera with strain efficient in the BNF sym-
biosis. The numbers in parentheses indicate the number of legume species within each genus for
which strains of rhizobium have already been selected

selected for approximately 90 forest species belonging to 38 genera (Fig. 6.2). For
most legume genera studied (60%), among 57 species, strains of the genus
Bradyrhizobium were selected (Fig. 6.2), followed by the genera Rhizobium and
Paraburkholderia. It is clear, therefore, that the Bradyrhizobium genus not only is
the most common symbiont of native and introduced legumes growing in Brazil, but
also tends to be the most efficient for N2 fixation among most genera (Fig. 6.2).
However, this cannot be generalized as plant-microbe specificity involving another
bacteria genus that can be important. For example, within Mimosa, 16 species that
were identified and selected strains all are members of the genus Paraburkholderia
(Fig. 6.2). The same has also been observed for the plant genera Piptadenia,
Parapiptadenia, and Anadenathera that probably only are nodulated by
Paraburkholderia strains (Fig. 6.2).
For 24 of these legumes, there is at least one strain authorized by MAPA for the
production of inoculants (Brazil 2011). Other forest legumes, for which although
currently there is at least one strain already selected, are not yet included in the
official MAPA list, which still requires significant efforts, including support from
the industry to validate the efficiency for registration (Fig. 6.2). This is the case of
the introduced forest legume such as some Acacia species, and most of the native
species already tested or with potential for use in mixed planting, such as the species
within the genera Enterolobium, Inga, Erythrina, Mimosa, Dalbergia, Tachigali,
and others.
110 S. M. de Faria et al.

6.5 Dependence of Biological N2 Fixation on Mycorrhization

Several microorganisms colonize the rhizosphere, which include bacteria, actino-

mycetes, and fungi. These microbes perform activities that are related to the physi-
ology and nutrition of plants. In this sense, the decomposition of soil organic
compounds, their mineralization, BNF, release of substances that stimulate growth
or antagonism to pathogens, as well as availability of nutrients are important for
plant growth (Grayston et al. 1997; Andrade et al. 2000; Kuiper et al. 2004; Moreira
and Siqueira 2006).
As N and P are usually the most limiting nutrients for plant growth in the tropics,
more attention has been paid to research on these elements and to alternatives for
the use of biological inputs, such as inoculation with rhizobia and mycorrhizal
fungi. Inoculation of tree legumes with rhizobial strains and mycorrhizal fungi can
meet all the N and P requirements for plant growth, taking into account the other
factors that are not limiting (Oliveira Júnior et al. 2016; Patreze et al. 2004; Moreira
and Siqueira 2006).
Several tree species, including A. mangium, have the ability to associate with
arbuscular mycorrhizal fungi as well as ectomycorrhizal fungi, in addition to estab-
lishing efficient nodulation with rhizobia. Mycorrhizal fungi can help increase the
biological nitrogen fixation, by enhancing P availability that is in demand for the
BNF process, as well as the nitrogen-fixing bacteria tend to influence mycorrhizal
colonization. This pattern of synergistic response is commonly observed in the
Mimosoid clade that responds to both types of symbioses (Oliveira Júnior et al.
2016; Bournaud et al. 2017).
In fact, there are complex interactions between legumes with their symbiotic
partners, which is the result of an old coevolution leading plants and microsymbi-
onts to respond more or less effectively to this interaction (Parniske 2008). Variations
in responses by both mycorrhizal fungi and rhizobial inoculation are typical,
because they are also associated with plant genetics and microsymbiotic perfor-
mance (Monteiro 1990a; Patreze and Cordeiro 2004). Monteiro (1990a) studied the
interaction between Mimosa caesalpiniifolia and M. scabrella with rhizobia and
arbuscular mycorrhizal fungi and concluded that the microsymbionts acted syner-
gistically for the production of biomass and nutrient accumulation in plants, with
biomass production exceeding 400% compared to the treatment without the micro-
organisms even with nutrient addition. In the same way Founoune et al. (2002)
evaluated the influence of two isolates of the ectomycorrhizal fungi, Pisolithus sp.
(COI 007, COI 024), and one isolate of Scleroderma dictyosporum (Sd 109) on the
growth of A. mangium and the synergy with rhizobium inoculation. Compared to
the control treatment that lacked inoculation with both the symbionts, A. mangium
plants treated with COI 007 and Sd 109, respectively, had significantly higher bio-
mass of roots and leaves. In addition, treatment with COI 007 resulted in a higher
number of nodules per plant. In the case of Acacia holosericea, however, the highest
number of nodules was present when inoculated with the COI 024 isolate.
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 111

These results show that, although symbiosis with mycorrhizal fungi is a rule
among higher plants, there may be additional benefits from certain isolates (Moreira
and Siqueira 2006; Shiavo and Martins 2002; Diagne et al. 2013).
The vast majority of the tree legumes can benefit from the association with
mycorrhizal fungi and through this association the BNF is improved as well.
However, certain groups of legumes not only benefit from this tripartite association,
but are also highly dependent on the mycorrhization to establish efficient nodula-
tion, even when supplied with phosphorus (Jesus et al. 2005). For example, recent
studies have shown that Piptadenia gonoacantha is only capable of inducing the
formation of inefficient nodules in the absence of mycorrhiza, and in this case, the
color and shape of the nodules formed are different (Bournaud et al. 2017; Oliveira
Júnior et al. 2016).
The importance of field-level and nursery studies with mycorrhizal fungi (mycor-
rhizal fungi and diazotrophic bacteria) is essential to evaluate their efficiency.
Laboratory and greenhouse conditions often do not represent the tougher field con-
ditions, even though nursery conditions for seedling production can be similar to
those in the greenhouse. For practical purposes inoculation with rhizosphere soil of
plants growing in the field will provide well-adapted AMF.

6.6 The Contribution of BNF in Mixed-Forest Plantations

N2-fixing trees, mainly species from the Leguminosae family, have been widely
used to improve N status of non-N2-fixing species in agroforestry systems
(Mafongoya et al. 1998) and mixed-forest planting for timber production (Binkley
and Giardina 1997; Richards et al. 2010) and for recovery of degraded lands (Franco
and Faria 1997; Chaer et al. 2011). However, the contribution of BNF (percentage
of N derived from the atmospheric fixation—% Ndfa) to tree and shrub species
under field conditions is not easy to evaluate, mainly due to the difficulties in esti-
mating the amount of N accumulated in the above- and belowground plant compo-
nents (Khanna 1998; Boddey et al. 2000). Interactions with the abiotic (climate and
soil in particular) and biotic factors (inter- and intraspecific interaction of mixed
plantations) also complicate these estimations, since they affect competition and
facilitation between plants and species, especially in mixed plantations (see Chap. 2).

6.6.1  easuring the Biological Nitrogen Fixation (BNF)

M
in Woody Perennial Species

Determining the BNF contribution in trees and shrubs, both in planted forests and
agroecosystems or in the native forests, has been the subject of several studies and
reviews (Boddey et al. 2000; Galiana et al. 2004; Gehring and Vlek 2004; Gehring
112 S. M. de Faria et al.

et al. 2005; Bouillet et al. 2008; Chalk 2016; Paula et al. 2018). Among the method-
ologies developed for the quantification of BNF and its applicability to woody
perennial species either under greenhouse (pots) or field conditions, Peoples et al.
(1989) cited acetylene reduction analysis (ARA), determination of relative abun-
dance of ureides in plant sap, and use of 15N (isotopic enrichment and natural abun-
dance) isotope dilution (ID) techniques. The N balance and nitrogen accretion
method can also be used to estimate the total N input (kg ha−1) via BNF (Peoples
et al. 1989; Forrester et al. 2007; Voigtlaender et al. 2018) in different ecosystems.
It should be noted, however, that each of these methodologies mentioned has speci-
fications and limitations (see Boddey et al. 2000; Unkovich et al. 2008; Chalk 2016).
The ARA method uses the activity of the nitrogenase enzyme because under high
acetylene concentration, it can be used as a substrate to be reduced to ethylene. This
analysis represents a qualitative evaluation of BNF as a point analysis of the nitro-
genase activity in the nodules from the plant. The evaluation of the abundance of
ureides (allantoins and allantoic acid) in the xylem relies on the ability of the spe-
cies to transport these compounds preferentially, to the detriment of nitrate and
other amino compounds, such as asparagine and glutamine (Peoples et al. 1996).
For example, plants from the genus Acacia, the most transported BNF products, are
asparagine and glutamine (Brockwell et al. 2005).
Isotopic dilution (ID) using the natural abundance of 15N is currently a good
option to determine the proportion of N derived from the BNF from the air (% Ndfa)
under field conditions (Boddey et al. 2000). This method relies on the fact that under
the same natural condition plants that fix some or all of their nitrogen will have
lower 15N signal than plants that obtain their entire N from the soils, which are 15N
enriched.
For the method based on 15N enrichment (E), the soil is enriched with a labeled
fertilizer and paired plots—one containing the legume and the other an N2-fixing
reference plot—are used for the application. However, the ID (NA or E) technique
presents some limitations as plant selection, tissue sampling, unpredictability in the
levels of 15N, N available to plants from organic matter decomposition, quality and
quantity of organic matter, and selective absorption of N sources by ecto- and endo-­
mycorrhizal fungi (Högberg 1997; Natelhoffer and Fry 1988; Boddey et al. 2000;
Gehring and Vlek 2004).
For the N balance and N accretion method, the BNF rate is estimated as the dif-
ference in accumulated N in the plant biomass (aerial and root), in the litter depos-
ited in the soil, or in the soil between plots of the non-N2-fixing species and plots
containing the N2-fixing species (monocultures or mixed species). Thus, it is
assumed that the differences (in kg ha−1) in N in the treatment are mainly due to the
biological process. The amounts of N2 fixation could be underestimated if the N in
the belowground area is not considered, especially in planted forests (Forrester
et al. 2007).
In addition, Chalk (2016) suggested that the uncertainty in BNF rate could be
attributed to the B-value (the relative isotopic abundance of legumes growing in
N-free medium). The reasons are as follows: (1) it is not usually determined simi-
larly in the field or pot experiments; (2) it is dependent on the rhizobial strain used
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 113

as the inoculant; and (3) it depends on the part of the plant tissue sampled. Differences
in the root density among the plants in each treatment (monocultures and mixed
plantation) of the topsoil, and variations in nitrate and ammonium availability, were
reported by Bouillet et al. (2008) as factors contributing to uncertainty in N2 fixation
estimates. These can lead to differences in ™15N of mineral N uptake (NH4+ is less
depleted in 15N than NO3−) by both plant species from soil or from fertilizer applica-
tion. The costs of the enriched fertilizer and the isotope analyses also restrict the use
of these two techniques (NA or E).

6.6.2 Higher Nitrogen Fixation in Mixed Plantations

The rate of the BNF estimates (% Ndfa) in tree species under mixed planting condi-
tions is scarce in Brazil, especially when dealing with native flora. Increased atten-
tion was paid to Acacia mangium because of the increased growth seen in degraded
lands and low-fertility soils in the 1980–1990s of the last century (Franco and Faria
1999; Coelho et al. 2007), additionally to the interest of forestry companies in stud-
ies of silvicultural performance and interaction of the species with eucalyptus at the
end of the twentieth century (Harwood and Nambiar 2014; Parrota and Knowles
1999), and the growing demands in Southeast Asia (Harwood and Nambiar 2014;
Balieiro et al. 2018).
A few reports estimating the %Ndfa in pure and mixed plantations with legumes,
using the NA or E techniques, across the Brazilian states of São Paulo and Rio de
Janeiro, showed a significant contribution of BNF to mixed plantations (Balieiro
et al. 2004, Paula et al. 2018), thus corroborating the work performed in other loca-
tions, such as Puerto Rico (Parrotta et al. 1996) and Ivory Coast (Tchichele et al.
2016). However, Forrester et al. (2007) studied mixed plantations of Acacia mearn-
sii and E. globulus, but observed opposite results. The higher BNF in mixed planta-
tions was attributed to the elevated N requirement of eucalyptus under mixed
plantation regimes. This requirement led to a strong competition for soil N by the
plants and a consequent elevation of the N demand in the system (Balieiro et al.
2004; Paula et al. 2018), by the high litter decomposition rate (Santos et al. 2016)
and soil N mineralization (Voigtlaender et al. 2019). Table 6.1 contains the %Ndfa
estimates for tree legumes in mixed and pure plantations in Brazil and other coun-
tries, using natural abundance (NA) and enrichment of 15N (E) techniques.
The results in Table 6.1 corroborate the work of Brockwell et al. (2005), who
reported that the biological nitrogen fixation rates observed under the field condi-
tions for Acacia, shrubs, and tree species occur in the 2–90% range. The authors
further describe that this range denotes the genetic variability within the genus
Acacia, the efficiency of strains and different species of rhizobia, and the different
estimation techniques of BNF.
In general, BNF contributions are higher when the planting is younger (Parrotta
et al. 1996; Paula et al. 2018; Balieiro et al. unpublished date; Balieiro et al. 2002
—Tables 6.1 and 6.2) and with local infertile soil (Bernhard- Reversat et al. 1996;
Table 6.1 Percentage of percentage of nitrogen derived from atmosphere (Ndfa, %) for native and exotic woody perianniasl species estimated by natural
114

abundance (NA) and enrichment 15N (E) techniques, under pure and mixed plantation
Reference Aboveground component or litter Age Ndfa
N2-fixing species species(a) Country sampled months % Method Reference
Peltophorum dubium (mixed, Eucalyptus Brazil Le 24 NA Coelho et al. (2007)
50:50) grandis
Inga sp. (mixed, 50:50) E. grandis Brazil Le 24 74 NA Coelho et al. (2007)
Mimosa scabrella (mixed, E. grandis Brazil Le 24 92 NA Coelho et al. (2007)
50:50)
Mimosa caesalpiniaefolia E. grandis Brazil Le 24 74 NA Coelho et al. (2007)
(mixed, 50:50)
Pseudosamanea guachapele E. grandis (E100) Brazil Le+Ba+Br+st# 84 17–36 NA Balieiro et al. (2004)
(G100)
P. guachapele (E50:G50) E. grandis (E100) Brazil Le+Ba+Br+st# 84 34–84 NA Balieiro et al. (2004)
Acacia mangium (A100) E. grandis (E100) Brazil Le 39 0–14 E Paula et al. (2018)
A. mangium (E50:A50) E. grandis (E100) Brazil Le 60 30–52 E Paula et al. (2018)
A. mangium (A100) E. urograndis Le+Ba+Br+St+Cr+Mr+Fr+Li# 24 59 E Tchichelle et al. (2017)
(E100)
A. mangium (E50:A50) E. urograndis Le+Ba+Br+St+Cr+Mr+Fr+Li# 24 64 E Tchichelle et al. (2017)
(E100)
A. mangium (A100) E. grandis (E100) Brazil Le+Ba+Br+St+Cr+Mr+Fr+Li# 30 20 NA Bouillet et al. (2008)
A. mangium (E50:A50) E. grandis (E100) Brazil Le+Ba+Br+St+Cr+Mr+Fr+Li# 30 10 NA Bouillet et al. (2008)
A. mangium (E50:A50) E. grandis (E100) Brazil Le+Ba+Br+St+Cr+Mr+Fr+Li# 30 59 E Bouillet et al. (2008)
A. mangium (A100) (plots low E. urograndis Ivory Le 19 27 NA Galiana et al. (2002)
fertility) (E100) Coast
A. mangium (A100) (plots E. urograndis Ivory Le 19 64 NA Galiana et al. (2002)
medium fertility) (E100) Coast
A. mangium (A100) (plots E. urograndis Ivory Le 19 67 NA Galiana et al. (2002)
medium fertility) (E100) Coast
S. M. de Faria et al.
 6

Leucaena leucocephala E. robusta Puerto Le 12 98 E Parrota et al. (1996)

(E50:L50) Rico
Leucaena leucocephala E. robusta Puerto Le 42 98 E Parrota et al. (1996)
(E50:L50) Rico
A. mearnsii (A100) E. globulus Australia Le 120 52– NA Forrester et al. (2007)
(E100) 107
A. mearnsii (E50:A:50) E. globulus Australia Le 120 8–17 NA Forrester et al. (2007)
(E100)
A. mangium (A100) E. urograndis Brazil Le 12 65 NA Balieiro et al. (data not
(E100) published)
A. mangium (A100) E. urograndis Brazil Le 24 26 NA Balieiro et al. (data not
(E100) published)
A. mangium (A100) E. urograndis Brazil Le 60 0 NA Balieiro et al. (data not
(E100) published)
A. mangium (E50:A50) E. grandis (E100) Brazil Le 12 70 NA Balieiro et al. (data not
published)
A. mangium (E50:A50) E. grandis (E100) Brazil Le 24 50 NA Balieiro et al. (data not
published)
A. mangium (E50:A50) E. grandis (E100) Brazil Le 60 0 NA Balieiro et al. (data not
published)
Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations

(a) non-N2-fixing species used to calculate the %Ndfa, (b) componet used by authors to estimate the %Nfda, Le leaves, Ba barck, Br branches, St stem;
Cr coarse roots, Mr medium roots, Fr fine roots, Li litter
115
116 S. M. de Faria et al.

Table 6.2 N2 fixed (kg ha−1) by woody perennial legumes in pure and mixed plantations based on
difference in aboveground N accumulation using the accretion method
N
N accretion
N2-fixing species Reference Age acumulated (A−B or
(A) species (B) Country (months) (kg ha−1) (A+B)-B Reference
Acacia mangium Eucalyptus Brazil 39 204.6 −19.6 Paula et al.
(A100) grandis (2018)
(E100)
A. mangium E. grandis Brazil 39 444.7 +220.5 Paula et al.
(E50:A50) (E100) (2018)
E. grandis Brazil 224.2 Paula et al.
(E100) (2018)
Acacia mangium E. urograndis Brazil 60 186.3 +17.6 Santos et al.
(A100) (E100) (2018)
A. mangium E. urograndis Brazil 60 231.8 +63.1 Santos et al.
(E50:A50) (E100) (2018)
A. mangium E. urograndis Brazil 60 285.5 +116.8 Santos et al.
(E100:A100) (E100) (2018)
E. urograndis Brazil 60 168.7 Santos et al.
(E100) (2018)
Mimosa scabrella E. grandis Brazil 24 317.7 +170.9 Coelho
(mixed, 50:50) et al. (2007)
Mimosa E. grandis Brazil 24 149.6 +2.8 Coelho
caesalpiniaefolia et al. (2007)
(mixed, 50:50)
A. mangium E. grandis Brazil 24 188.4 +41.6 Coelho
et al. (2007)
E. grandis Brazil 24 146.8 Coelho
et al. (2007)
A. mangium Brazil Balieiro
(A100) et al. (2004)
E. grandis Brazil 60 410.5 Balieiro
(E100) et al. (2002)
Pseudosamanea E. grandis Brazil 60 756.8 −57.0 Balieiro
guachapele (E100) et al. (2002)
(G100)
P. guachapele E. grandis Brazil 60 467.5 +289.3 Balieiro
(E50:G50) (E50:G50) et al. (2002)
E. grandis Brazil 60 410.5 Balieiro
(E100) et al. (2002)
Acacia mangium Eucalyptus Ivory 24 30.1 +23.8 Tchichele
(A100) grandis Coast et al. (2017)
(E100)
A. mangium E. grandis Ivory 24 23.5 +17.2 Tchichele
(E50:A50) (E100) Coast et al. (2017)
E. grandis Ivory 24 6.3 Tchichele
(E100) Coast et al. (2017)
(continued)
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 117

Table 6.2 (continued)

N
N accretion
N2-fixing species Reference Age acumulated (A−B or
(A) species (B) Country (months) (kg ha−1) (A+B)-B Reference
A. mearnsii E. globulus Brazil 120 496 +358 Forrester
(A100) (E100) et al. (2007)
A. mearnsii E. globulus Brazil 120 480 +342 Forrester
(A50:E50) (E100) et al. (2007)
E. globulus Brazil 120 138 Forrester
(E100) et al. (2007)
A. mangium E. grandis Brazil 72 2050 +413 Voigtlander
(A100)—Itatinga (E100) et al. (2018)
A. mangium E. grandis Brazil 72 1836 +199 Voigtlander
(E50:A50)— (E100) et al. (2018)
Itatinga
E. grandis Brazil 72 1637 Voigtlander
(E100) et al. (2018)
A. mangium E. grandis Brazil 72 2242 +348 Voigtlander
(A100)—Bofete (E100) et al. (2018)
A. mangium E. grandis Brazil 72 2111 +217 Voigtlander
(E50:A50)— (E100) et al. (2018)
Bofete
E. grandis Brazil 72 1895 Voigtlander
(E100) et al. (2018)
A. mangium E. urograndis Brazil 72 1622 – Voigtlander
(A100)—Luiz (E100) et al. (2018)
Antônio
A. mangium E. urograndis Brazil 72 1848 +84 Voigtlander
(E50:A50)—Luiz (E100) et al. (2018)
Antônio
E. urograndis Brazil 72 1764 Voigtlander
(E100) et al. (2018)
A. mangium E. urograndis Brazil 72 3258 +367 Voigtlander
(A100)—Santana (E100) et al. (2018)
do Paraíso
A. mangium E. urograndis Brazil 72 3168 +277 Voigtlander
(E50:A50)— (E100) et al. (2018)
Santana do Paraíso
E. urograndis Brazil 72 2891 Voigtlander
(E100) et al. (2018)

Galiana et al. 2002, Balieiro et al. 2004). Both factors are related to the upregulation
of N2 fixation depending on the soil N status (Vitousek et al. 2002; Galiana et al.
2002). Galiana et al. (2002) observed the spatial variability in %Ndfa for A. man-
gium as a result of soil fertility variation between plots. The %Ndfa reached 64 and
67% in blocks II and III, respectively, versus 27% in block I, following a parallel
increase in N and P soil content.
118 S. M. de Faria et al.

The total N accumulated in the biomass, litterfall, and soil-derived BNF is calcu-
lated as the difference in total N found in N2-fixing species and reference species
(non-fixing) (Parrotta et al. 1996; Forrester et al. 2007). From some previous work,
the additional amount of N introduced by tree legumes in mixed and pure planting
conditions is estimated, in order to measure the benefits of introducing legumes in
these systems. As shown in Table 6.2, the total N accumulated in the aerial parts of
the plants at a given stage is underestimated, as much of the N2 fixed may be related
to the roots (coarse and fine) and the litter (deposited and on the ground). Although
the N2-fixed N by the legume in the plantation is proportional to its capacity to com-
pete in a specific local, the BNF contribution is always higher in the mixed planta-
tion than in the eucalyptus monocultures. It is expected to contribute up to
60 kg ha−1 year−1 under mixed-forest plantations. These values corroborate with
previous reports on plantations under field conditions, with Acacia spp. in Africa
and Australia, with up to 50 kg ha−1 year−1 of fixed N (Sprent 1993; Sutherland and
Sprent 1993). As much as BNF contribution of leguminous species depends on its
adaptability and growth in local edaphoclimatic conditions, it is imperative that
breeding and selection of these species be carried out for different Brazilian condi-
tions, as it has been done in Southeast Asia (Griffin et al. 2015).
Likewise, the new mixed planting arrangement using Brazilian native species
may offer some benefits, especially for the biological conservation and the associ-
ated ecosystem services (see Chaps. 10 and 12). Silvicultural management of these
plantations needs to be better understood as the pruning, thinning, or proper clean-
ing and maintenance of the plants are activities that could disturb the system and
affect BNF in the legumes.

6.6.3 Nitrogen Transfer between Plants in Mixed Plantations

Although N transfer between plants occurs in both directions, i.e., from N2-fixing
tree to non-N2-fixing and vice versa, the magnitude of the transfer is greater from
N2-fixing tree to non-N2-fixing species (see review by Chalk et al. 2014). Several
studies show that 0–50% of N contained in plants associated with N2-fixing trees
could be derived from such transfers. Due to the transfer, non-N2-fixing trees grow-
ing in a consortium of N2-fixing trees sometimes accumulate more N in their bio-
mass than the individually growing trees. This additional N is assumed to derive
from the transfer (Chalk et al. 2014).
The N present in the N2-fixing trees can be transferred directly or indirectly to
non-N2-fixing species growing within a consortium (Munroe and Isaac 2014)
(Fig. 6.3). Low-molecular-weight nitrogen compounds, such as nitrate, ammonium,
and amino acids, are transferred directly between the plants without transforming,
from the root exudates or by the action of mycorrhiza. The decomposition of the
vegetative tissue, above- and belowground, and its mineralization by soil microor-
ganisms lead to the indirect transfer of N between plants. These N transfer rates vary
in speed and significance, and are poorly understood, as well as the limiting or
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 119

Fig. 6.3 Schematic showing pathways of N transfer between trees in mixed-species plantation
with non-N2-fixing and N2-fixing trees. Direct transfer of N begins with an N compound with low
molecular weight without undergoing transformation by (a) ammonium volatilization, (b) stem-
flow, (c) throughfall, (d) soluble N in litterfall and pruning residues, and (e) root exudates, soluble
N in nodule and roots, and mycorrhiza network. Indirect transfer of N occurs after transformation
of N substance by (d) decomposition and mineralization of litterfall and pruning residues, (e) root
and nodule decomposition and mineralization, and by mycorrhizal network (both ectomycorrhizal
and arbuscular fungi)

facilitating factors of this transfer (Mafongoya et al. 1998; Munroe and Isaac 2014;
Chalk et al. 2014; Peoples et al. 2015).
Among the main source of N potentially transferable in the mixed plantation, the
branches and green leaves of litterfall and the fine roots and nodules represent the
major sources of N in quantitative terms. It is important to notice however that the
amount of N accumulated in the fine roots is still poorly understood (Mafongoya
et al. 1998; Munroe and Isaac 2014; Peoples et al. 2015). The biomass of these roots
(diameter <2 mm) at a depth of 17 m was estimated for pure and mixed plantations
of acacia and eucalyptus at 4 years of age in Itatinga, Brazil (Germon et al. 2018).
Acacia trees produced approximately 4.2 tons ha−1 of fine roots in the mixed planta-
tion up to a depth of 12 m. Using an average of 2.3% N content in fine acacia roots
(Paula 2015), the N content in the fine roots was 98.3 kg ha−1.
120 S. M. de Faria et al.

Living tissue derived from pruning or harvesting is an important source of N

since the total and soluble N content is higher than that in the senescent tissues.
Paula (2015) used crop residues (i.e., leaves, branches, and bark) of 15N-enriched
A. mangium and E. grandis in eucalyptus seedlings to trace the path of the residue-­
derived N in the soil-plant system. Three months after the application of these resi-
dues, young leaves of eucalyptus seedlings were significantly enriched with 15N
when they received A. mangium residues, which was not the case when the plants
received E. grandis residues or unlabeled residues. This result shows rapid transfer-
ability of a large fraction of soluble N from the legume to other plants.
Direct N transfer from legumes through root exudation and mycorrhizal repre-
sents a substantial source of N during tree growth (Munroe and Isaac 2014). This
transfer is important because it occurs in the short term (e.g., hours, days), and even
trees distant from the source can benefit from the transferred N (Paula et al. 2015).
Paula et al. (2015) applied potassium nitrate enriched with 15N to the stem of A. man-
gium trees and observed values of 15N above natural abundance in eucalyptus tissues
located within a radius of up to 6.2 m around the acacia plants marked for 60 days
after the application. N transfer between plants is facilitated by the presence of both
arbuscular mycorrhizae and ectomycorrhizas associated with the vast majority of
plant species and can be modulated by source and drain relationship (He et al.
2003). These organisms are able to absorb mineral and organic forms of N derived
from N2-fixing species and assimilate N as needed before transferring to plants
growing in a consortium (He et al. 2003; Munroe and Isaac 2014). Ectomycorrhizae
can also act on the transfer of N between plants, as they can break down complex
organic compounds present in the soil and transform them into forms that are assim-
ilated by plants (He et al. 2003). Estimates of N transfer through mycorrhizae from
legumes to non-legumes vary between 20 and 50% of accumulated N (He et al. 2003).
Direct approaches to estimate N transfer involve the application of a nitrogen
source enriched with 15N to the nitrogen-fixing tree, and subsequent isotope tracing
in the tissues of the reference species (Chalk et al. 2014). The N2-fixing tree can be
labled with 15N via foliar absorption, via injection in the branches and stem, and by
root absorption, each one with its particularities (Yasmin et al. 2006; Chalk et al.
2014). Paula et al. (2015) used the 15N values observed in the fine roots of E. grandis
and A. mangium to calculate the N ratio of E. grandis derived from A. mangium and
concluded that the average N transfer reached values of approximately 43%. Based
on mass balance, the authors calculated the proportion of 15N injected into the stem
of A. mangium that was transferred to E. grandis trees within a radius of 6.2 m
around the acacia, which reached an estimate of N transfer of approximately 3%.
Other potential high-throughput N transfer routes involve leaf leaching, foliar
ammonia gas release, root leaching, and herbivory of nodules (Peoples et al. 2015).
The first two routes were studied by Paula (2015). At different dates after 15N appli-
cation in A. mangium trees, 15N was determined in the stemflow and throughfall
samples collected below the labled acacia, as well as samples derived from collec-
tors installed above the acacia to capture ammonia. The researcher observed that
there was no enrichment of these sources of N with 15N above the natural one, and
that both sources of N had negative values of δ 15N.
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 121

Although many advances are being made to understand the facilitation and the
ecological relationships involving the transfer of N between plants (mainly N2-­
fixing to non-N2-fixing species), it is also urgent that studies with key nutrients for
the process of decomposition, growth, and biological stabilization of N2 and stabili-
zation of soil organic matter, such as P, are initiated.

6.7  razilian Native Legume Tree Species with Potential

B
for Mixed Plantations

In this section, we present some Brazilian legume tree species with potential for
mixed planting with Eucalyptus spp. The N2-fixing legume tree species were cate-
gorized into two groups: “fertilizer” and “timber” species. The former one included
fast-growing species that have high rates of N2 fixation, which can be used to
increase the N and other nutrient levels through aboveground biomass pruning, litter
deposition, and/or root exudates and decomposition. In addition, they are species
that generally produce light to moderately heavy wood with lower commercial-­
value timber. The second group included the species which present longer rotation
than Eucalyptus spp. and produce wood for multiple uses with high commer-
cial value.

6.7.1 Fertilizing Legume Trees

The genera Enterolobium, Erythrina, Inga, and Mimosa include tree species with
high levels of nodulation in natural environments or under controlled conditions (de
Faria et al. 2006; Canosa et al. 2012; Lorenzi 1992). They can be suggested as spe-
cies of the Brazilian flora with the potential to be introduced in mixed plantations
with Eucalyptus spp. Table 6.3 lists some of these species.
In the genus Enterolobium, popularly known as “tamboril,” it is possible to dis-
tinguish E. maximum and E. contortisiliquum as potential species to be introduced
in the mixed plantations with Eucalyptus spp. E. maximum, an Amazonian species,
has wood with easy workability and good finishing, for use in boats, toys, household
utensils, and plates (Souza et al. 2002). E. contortisiliquum is seen along the
Brazilian east-coast, including the Atlantic rainforest and Caatinga biomes. It has
lightwood (density of 0.54 g cm−3 at 12% of moisture content), which can be used
in the manufacture of boats and crates. The flowers are mellifluous, and the fruits
contain saponin, a substance used in the manufacture of soap.
Inga and Erythrina are commonly used as arboreal components of the agrofor-
estry systems with banana, cocoa, and rubber trees in the state of Bahia and the
Amazon. Frequently, both genera have also been planted under different arrange-
ments of agroforestry systems in Latin America (Bolivia, Peru, and Colombia).
122 S. M. de Faria et al.

Table 6.3 Species of “fertilizer” tree legumes of Brazilian flora suggested for mixed plantations
with Eucalyptus spp.
Phytogeographical
Geographic distribution domains (Brazilian
Genus Species (Brazilian statesa) biomes)
Erythrina E. verna Vell. North (AC); Southeast (ES, Amazon, Atlantic
MG, RJ, SP) rainforest
E. poeppigiana North (AC, AM, PA, RO) Amazon
(Walp.) O. F. Cook
E. fusca Lour. North (AC, AM, AP, PA, RO) Amazon, Cerrado
Midwest (MT)
Inga I. edulis Mart. North (AC, AM, AP, PA, RO, Amazon, Caatinga,
RR); Northeast (BA, PB, PE); Cerrado, Atlantic
Midwest (MT); Southeast (ES, rainforest
MG, RJ, SP) South (PR, SC)
I. laurina (Sw.) Willd. North (AC, AM, PA); Amazon, Caatinga,
Northeast (BA, CE, MA, PB, Cerrado, Atlantic
PE); Midwest (DF, GO, MS, rainforest
MT); Southeast (ES, MG, RJ,
SP) South (PR)
I. cinnamomea Spruce North (AC, AM, AP, PA, RO) Amazon
ex Benth.
Enterolobium E. maximum Ducke North (AC, AM, PA, RO, RR); Amazon
Midwest (MT)
E. contortisiliquum Northeast (BA, CE, PB, PE, Caatinga, Cerrado,
(Vell.) Morong PI, RN); Midwest (DF, GO, Atlantic rainforest
MS, MT); Southeast (MG, RJ,
SP); South (PR, RS, SC)
Anadenanthera A. colubrina var. cebil Northeast (BA, CE, PB, PE, Caatinga, Cerrado,
(Griseb.) Altschul PI, RN, SE); Midwest (DF, Atlantic rainforest
GO, MS, MT);
Southeast (MG)
A. colubrina (Vell.) Northeast (BA); Southeast Caatinga, Cerrado,
Brenan var. colubrina (MG, RJ, SP); South (PR) Atlantic rainforest
A. peregrina (L.) Speg. North (AM, PA, RR); Midwest Amazon, Cerrado
var. peregrina (DF, GO, MS); Southeast
(MG)
A. peregrina var. Northeast (BA, PB); Midwest Caatinga, Cerrado,
falcata (Benth.) (MS, MT); Southeast (MG, Atlantic rainforest
Altschul RJ, SP); South (PR)
Mimosa M. scabrella Benth. Southeast (MG, RJ, SP); South Atlantic rainforest
(PR, RS, SC)
M. caesalpiniaefolia North (AM, PA, RO); Amazon, Caatinga,
Benth. Northeast (AL, BA, CE, MA, Cerrado, Atlantic
PB, PE, PI, RN); Midwest rainforest
(DF, GO, MS); Southeast (ES,
MG, RJ, SP); South (PR, SC)
a
Brazilian states abbreviations: AC Acre, AL Alagoas, AM Amazonas, AP Amapá, BA Bahia, CE
Ceará, DF Distrito Federal, ES Espírito Santo, GO Goiás, MA Maranhão, MG Minas Gerais, MS
Mato Grosso do Sul, MT Mato Grosso, PA Pará, PB Paraíba, PE Pernambuco, PI Piauí, PR Paraná,
RJ Rio de Janeiro, RN Rio Grande do Norte, RO Rondônia, RR Roraima, RS Rio Grande do Sul,
SC Santa Catarina, SP São Paulo, SE Sergipe
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 123

There are several species of Inga in the Brazilian flora that are generally adapted to
hot and humid climates. Many of them are responsive to pruning in the aerial part,
where all green biomass generated can be enclosed along the planting lines of
Eucalyptus spp. The trees of Inga spp. produce lightwood that can be used for coin-
age and energy. The fruits are edible and can be commercially exploited for the
regional markets. Similarly, the genus Erythrina also has trees with light- and soft-
wood, used mainly for crates, furniture linings, shoes, and toys.
Mimosa has smaller trees (varying from 5 to 15 m) distributed in several biomes.
M. scabrella, for example, is a species found in cold places or altitudes in the south
and southeast of Brazil. The wood from this genus has an average density of
0.67 g cm−3, and is widely used in interior finishes, in the manufacture of plywood
and packaging and for energy. M. caesalpiniaefolia however adapts well to warm,
dry, or humid climates. In the Brazilian Northeast, it is commonly cultivated. It is a
spiny tree, even though with non-spiny variants, that produces multiple stems,
requiring significant maintenance. Some of the tree characteristics are helpful, as
living fences. The wood is suitable for firewood, charcoal, cable tools, and external
uses such as wood posts. Its wood is long lasting under external conditions, even
without chemical treatment.

6.7.2 Timber Species

Among the trees of this group, we highlight the following genera: Anadenanthera,
Bowdichia, Centrolobium, Dalbergia, Hymenolobium, Plathymenia, and Tachigali
(Table 6.4).
Some species of Anadenanthera are known as “angicos” in Brazil. These are
fast-growing plants and can be found in several Brazilian regions. A. colubrina has
heavy woods (density ranging from 0.80 to 1.00 g cm−3) suitable for building
(indoor), planks, packaging, firewood, and charcoal. A. peregrina has a dense wood
(0.70 to 0.97 g cm−3) and is suitable for the manufacture of pieces of rafts, frames,
roof slats, rural constructions, and outdoor construction materials such as sleepers,
stakes, fence posts, and posts. In addition to the wood uses, the mixed plantations of
Anadenanthera with Eucalyptus offer honey from the flowers.
Species of the genus Bowdichia are popularly known as “sucupira” in Brazil.
B. nitida is an Amazonian species with the potential to reach heights of up to 35 m
in natural conditions. The most common uses include the timber for making furni-
ture, decorative laminates, bridges, and civil and naval constructions (Souza et al.
1997). The wood is very dense (exceeding 0.96 g cm−3) and dark brown in color.
B. virgilioides is distributed in the different Brazilian biomes and generally reaches
heights of about 20 m. The wood is of high density (0.91 g cm−3), is long-lasting,
and is used in construction (outdoor areas) and furniture.
The genus Centrolobium has some of the important timber species such as
C. tomentosum, C. robustum, and C. paraense, known in Brazil as “putumuju” or
“araribá.” The woods of these species are heavy, dense (over 0.75 g cm−3), and easy
124 S. M. de Faria et al.

Table 6.4 Timber species legumes with late rotations of Brazilian flora suggested for mixed
plantations with Eucalyptus spp.
Phytogeographical
Geographic distribution domains (Brazilian
Genus Species (Brazilian statesa) biomes)
Plathymenia P. reticulata North (PA); Northeast (BA, CE, Amazon, Caatinga,
Benth. MA, PI); Midwest (DF, GO, MS, Cerrado, Atlantic
MT); Southeast (ES, MG, RJ, rainforest
SP); South (PR)
Dalbergia D. nigra (Vell.) Northeast (AL, BA, PB, PE, SE); Atlantic rainforest
Allemãoex Benth. Southeast (ES, MG, RJ, SP);
South (PR)
Tachigali T. vulgaris North (AM, PA, TO); Northeast Amazon, Caatinga,
L. G. Silva & (BA, CE, MA, PI); Midwest (DF, Cerrado
H. C. Lima GO, MS, MT); Southeast (MG,
SP)
Centrolobium C. robustum Northeast (BA); Southeast (ES, Atlantic rainforest
(Vell.) Mart. ex MG, RJ, SP)
Benth.
C. tomentosum Northeast (BA); Midwest (DF, Caatinga, Cerrado,
Guillem. ex GO); Southeast (ES, MG, RJ, Atlantic rainforest
Benth. SP); South (PR)
C. paraense Tul. North (RR) Amazon
Hymenolobium H. modestum North (AM, PA) Amazon
Ducke
H. petraeum North (AM, AP, PA); Northeast Amazon
Ducke (MA)
H. excelsum North (AM, PA) Amazon
Ducke
Bowdichia B. virgilioides North (AM, AP, PA, RO, RR, Amazon, Caatinga,
Kunth TO); Northeast (AL, BA, CE, Cerrado, Atlantic
MA, PB, PE, PI, RN, SE); rainforest, Pantanal
Midwest (DF, GO, MS, MT);
Southeast (ES, MG, SP)South
(PR)
B. nitida Spruce North (AC, AM, AP, PA, RO, Amazon
ex Benth. RR)
a
Brazilian states abbreviations: AC Acre, AL Alagoas, AM Amazonas, AP Amapá, BA Bahia, CE
Ceará, DF Distrito Federal, ES Espírito Santo, GO Goiás, MA Maranhão, MG Minas Gerais, MS
Mato Grosso do Sul, MT Mato Grosso, PA Pará, PB Paraíba, PE Pernambuco, PI Piauí, PR Paraná,
RJ Rio de Janeiro, RN Rio Grande do Norte, RO Rondônia, RR Roraima, RS Rio Grande do Sul,
SC Santa Catarina, SP São Paulo, SE Sergipe, TO Tocantins

to work. The wood colors range from brown to yellow, with veins or orange spots.
The wood is employed typically in luxury carpentry and fine furniture, but it is also
used in civil and naval constructions, and in hydraulic work.
Dalbergia nigra, known as “jacarandá-da-Bahia,” produces one of the most
beautiful and premium woods of the Atlantic rainforest. Consequently, it happens to
be one of the threatened species facing extinction in the Brazilian forests. In Brazil,
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 125

there are other timber species of the same genus, for example, D. spruceana, which
is found in the Amazon. These species produce heavy (ranging from 0.80 to
1.00 g cm−3), smooth, fine-textured, natural-toned, dark-colored (sometimes blasted)
wood that offers an excellent finish to luxury furniture and interior decoration. It is
one of the well-known Brazilian woods and used in the manufacture of musical
instruments (piano, violin, and others).
Species of the genus Hymenolobium are known commercially as “angelim”,
although this vernacular name has also been attributed to other Amazonian legume
tree species, such as Dinizia excelsa Ducke (“angelim-vermelho, angelim pedra”),
Vatairea paraensis Ducke, Vatairea sericea (Ducke) Ducke, Vataireopsis speciosa
Ducke (“angelim-amargoso”), and Pithecellobium racemosum (Ducke) Killip
(angelim-rajado). However, only Hymenolobium and Pithecellobium species are N2
fixing. Some Hymenolobium species reach heights up to 40 to 50 m and 80 to
100 cm of diameter at breast height (DBH) in their natural habitats, with rectilinear
and cylindrical shafts up to 25 m in length. The wood has a reddish-brown core,
with darker brown spots due to oil-resin exudation and pale-brown sapwood. The
wood is of medium to high density (0.71 g cm−3), with easy workability, and offers
a good finish. It is currently one of the largest woods used in the Brazilian domestic
market, and commonly used in the manufacture of furniture and civil construction
(beams, rafters, frames, linings, and others).
Plathymenia foliolosa, popularly known as “vinhático,” is widely distributed in
Brazil. The vinhático trees reach a height between 15–30 m and 40–70 cm of DBH
under natural conditions. A striking feature of the adult trees is that the bark emerges
from the trunk as large plaques. The wood is light (density of 0.50 g cm−3) and has
easy workability and longer durability. The color of the wood ranges from yellow-­
gold to yellow-brown, and is therefore commonly used in luxury articles, furniture
and civil construction (decorative interior panels), and internal ship finishing.
Tachigali vulgaris, known as “tachi-branco or tachi-dos-campos,” has been
widely cultivated for over two decades in monoculture stands in northern Brazil
and has shown good silvicultural potential. Castro et al. (1990) found annual mean
increments (AMI) in height, DBH, and volume of 2.2 m year −1, 2.9 cm year−1, and
9.2 m3 year−1, respectively, when evaluating 3.5-year-old monocultures, estab-
lished with a spacing of 3 m × 3 m. Narducci (2014) found AMI of 2.53 m year−1
and height of 2.05 cm year−1 at DBH in 7.5-year-old monocultures planted with a
spacing of 4 m × 4 m. T. vulgaris presents a medium to high wood density
(0.60 g cm−3 to 0.74 g cm−3) which can be suitable for the production of sawwood
and roundwood, especially posts, beams, and civil construction, and for energy
purposes. It is considered to be moderately dense wood (0.65 g cm−3 to 0.81 g cm−3)
(Carvalho 2005).
126 S. M. de Faria et al.

6.7.3 Other Introduced-Potential Species (Trees and Shrubs)

In Brazil, some legume trees were introduced and have been cultivated/domesti-
cated by farmers and foresters. Such species could also be tested in different
arrangements of mixed-species plantations with Eucalyptus and/or other native spe-
cies, including the cultivation of shrubby legumes for green manure production. All
these species are listed in Table 6.5.

6.8 Final Considerations

In recent years, studies on nitrogen-fixing tree species have been intensified, includ-
ing in mixed-forest plantations. The ability to fix nitrogen and accumulate large
amounts of N as part of their biomass confers adaptive characteristics to the legumes
that excel over other species. There is a large diversity of legume trees, such as the
early and fast growers, and some which are slow growers but produce better qual-
ity timber.
Most studies on mixed-species plantations seem to be focused on Acacia and
Eucalyptus. From these studies, many technical recommendations are readily avail-
able for the productive sector, although its large-scale use is challenging. A. man-
gium and A. mearnsii seem to be the main N2-fixing species studied (Forrester et al.
2005; Bouillet et al. 2013). These species have shown great adaptation to South
American edaphoclimatic conditions and other tropical and subtropical countries.
Furthermore, both species have been widely cultivated in their native regions (i.e.,
Southeast Asia and Oceania). This is due to the multiple wood uses, which can be
applied to the production of cellulosic pulp, firewood, and charcoal. In Indonesia
and Vietnam, the branches and dead leaves are used as fuel and the leaves as fodder
for cattle due to their high protein content (Krisnawati et al. 2011). Some non-­
timber uses still include the production of honey (due to apiculture flowers and the
presence of extrafloral nectaries) (Tonini et al. 2010), glue, and tannin extraction
from the bark (mainly for A. mearnsii). The barks of A. mangium additionally pro-
vide a good substrate for edible mushrooms (Lim et al. 2011).
However, in Brazil, A. mangium behaves as a aggressive and invasive species,
which in part seems to be due to its broad N2-fixing capability even in marginal soils
with low nutrients (Souza et al. 2018; Le Maitre et al. (2011) Delnatte and Meyer
2012, Aguiar et al. 2014, Morais and Montagner 2015, see Chap. 11). Its capacity to
absorb P and the highly efficient nutrient recycling within the plants make it a strong
competitor for this element. Therefore, silvicultural programs must consider the
phosphate fertilization management in successive rotations that include these acacia
species.
In this context, we stimulate the test with native legumes from Brazil and in neo-
tropical region, in general, in order to generate information on optimal growth con-
ditions of these legumes. In Brazil, despite the high diversity of woody species,
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 127

Table 6.5 Other introduced-potential species (trees and shrubs) with potential to use in forest
planting
Potential
invasion
risk
reported in
Genera Species Origin Habit Brazila Uses
Acacia A. auriculiformis Ex Southeastern Woody YES+ Fertilizer/
Benth. Asia, Australia, timber
Papua New
Guinea
A. mangium Willd. Indonesia, Woody Yes+ Fertilizer/
Australia, timber
Papua New
Guinea
A. mearnsii Willd. Australia, Woody Yes Fertilizer/
Papua New timber
Guinea,
Tasmania
Acaciella A. angustissima (Mill.) Central Woody Yes Fertilizer
Kuntze America,
Colombia
Albizia A. lebbeck (L.) Benth. Southern Asia, Woody Yes+ Fertilizer/
South Africa, timber
Australia
Cajanus C. cajan (L.) Millsp. Probably from Shrubby No Fertilizer
India
Crotalaria C. grahamiana Wight & Probably from Shrubby No Fertilizer
Arn. India
C. juncea L. Asia Shrubby No Fertilizer
C. spectabilis Roth Asia Shrubby No Fertilizer
Falcataria F. moluccana (Miq.) Southeastern Woody No Fertilizer
Barneby and Grimes Asia, Papua
New Guinea
Gliricidia G. sepium (Jacq.) Steud. Central Shrubby/ No Fertilizer
America woody
Leucaena L. leucocephala (Roxb.) Central Woody Yes+ Fertilizer
Benth. America
Pithecellobium P. dulce (Roxb.) Benth. Mexico, Woody Yes Fertilizer
Central
America and
northern of
South America
Pseudosamanea P. guachapele (Kunth) Central Woody Yes+ Fertilizer
Harms America,
Colombia,
Ecuador, Peru,
Venezuela
(continued)
128 S. M. de Faria et al.

Table 6.5 (continued)

Potential
invasion
risk
reported in
Genera Species Origin Habit Brazila Uses
Sesbania S. grandiflora (L.) Pers. From Woody No Fertilizer
southeastern
Asia to
northern
Australia
S. sesban (L.) Merr. Africa, Asia Woody No Fertilizer
Tephrosia T. vogelii Hook. f. Tropical Africa Shrubby No Fertilizer
“+” means high
a

there are few long-term experiments on silviculture and management of native spe-
cies under mixed plantations. One of the pioneering works was conducted by Dr.
Renato de Jesus and his collaborators at the Reserva Natural Vale (Linhares, ES,
Brazil) since the 1970s (Rolim and Piotto 2018). In general, results have shown that
many native species (including N2-fixing trees) present great potential for reforesta-
tion and agroforestry systems, increasing the supply of high-quality timber and
reducing the pressure on remnants of the Atlantic Forest. Clearly, several barriers
must be overcome because many of the native species mentioned above require
further characterization and knowledge for their domestication, especially for peo-
ple relying on timber for their livelihood. Other barriers include the identification of
species adapted to the different Brazilian edaphoclimatic conditions, responses to
silvicultural treatments (i.e., thinning or pruning regimes), and need to ensure ade-
quate seed availability.
As for the benefits of BNF, it can be a major factor to enhance the productivity
and sustainability of a forest plantation. What we still need is the increased adoption
of inoculation of legume seeds during the seedling production and transplanting
stages. Selecting the appropriate strain and inoculating during these two stages have
been improving the symbiosis.
It is recommended that the species discussed in this chapter be prioritized in
future studies of Eucalyptus plantations mixed with N2-fixing legumes. At the time
of species selection, the farmer should opt for the availability of seeds and seedlings
in the region, as well as check for compatibility to the local climate.
This is an activity involving multilocation field trials and selection of genetically
superior material with the desired phenotype suitable for forest stands and for tim-
ber yield; particularly, the shape and size of the trunk may be key considerations.
Besides, additional studies are needed to understand the behavior and interaction of
these species in mixed plantations with Eucalyptus spp. and others non-N2-fixing
species in diverse Brazilian soil and climate conditions. A series of experiments,
collaborations by different institutions, and participation of forestry experts from
different regions would be immensely valuable.
6 Biological Nitrogen Fixation (BNF) in Mixed-Forest Plantations 129

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Chapter 7
Mycorrhiza in Mixed Plantations

Maiele Cintra Santana, Arthur Prudêncio de Araujo Pereira,

Bruna Andréia de Bacco Lopes, Agnès Robin, Antonio Marcos Miranda Silva,
and Elke Jurandy Bran Nogueira Cardoso

7.1 Introduction

The mutualistic association between plant roots and soil fungi, which results in the
enhancement of plant health, is denominated mycorrhiza. The term mycorrhiza
originates from Greek and was proposed by the German botanist Albert Bernhard
Frank, in 1885, in which “myco” means fungus and “rhiza” means root (Frank and
Trappe 2005). In this interaction, the plants, through photosynthesis, provide energy
and carbon for the survival and multiplication of symbiotic fungi (Smith and Read
2008; van der Heijden et al. 2015). In addition, the mycorrhizal hyphal system
increases the area of root exploration in the soil, being important mainly for the
efficient absorption of nutrients and water by plants (Cardoso et al. 2010; Smith and
Smith 2011).

M. C. Santana (*) · B. A. de Bacco Lopes · A. M. M. Silva · E. J. Bran Nogueira Cardoso

Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
e-mail: mcsantana@usp.br
A. P. A. Pereira
Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
Soil Science Department (Pici Campus), Federal University of Ceará, Fortaleza, Ceará, Brazil
A. Robin
Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
Eco & Sols, Univ. Montpellier, CIRAD, INRA, IRD, Montpellier SupAgro,
Montpellier, France

© Springer Nature Switzerland AG 2020 137

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_7
138 M. C. Santana et al.

Mycorrhizae are classified into seven types: arbuscular mycorrhiza (AM),

e­ ctomycorrhiza (ECM), ericoid mycorrhiza and orchidoid mycorrhiza, ectendomy-
corrhiza, arbutoid mycorrhiza, and monotropoid mycorrhiza (Harley and Smith
1983; Brundrett 2004). Most groups of vascular plants are able to form mycorrhizae,
while only a few families, such as Brassicaceae, Cyperaceae, and Proteaceae, do not
develop this association (Souza et al. 2006). Specifically, AM and ECM are the most
studied in forests due to their important role in the maintenance of biodiversity and
ecosystem productivity in agriculture and forestry (Berbara et al. 2006). Normally,
most plants associate only with one mycorrhizal type; however studies regarding the
occurrence and diversity of mycorrhizas in Brazil have shown that plants from the
genera eucalyptus and acacia are able to form, either alone or simultaneously, both
AM and ECM (Pereira 2015; Santana et al. 2016; Santana 2017). It has been assumed
that mycorrhizal colonization is restricted to the topsoil, considered the arable part
of the soil, and the mycorrhizal association in deeper regions of the soil profile is
poorly understood. However, recent research has shown that this type of coloniza-
tion can occur in deep soil layers, down to 8 m, as will be detailed below (Pereira
2015; Pereira et al. 2018; Robin, A. personal data).
Currently, in addition to conventional techniques, such as spore morphology and
root colonization rates, molecular technology has been widely used for the taxo-
nomic classification and characterization of mycorrhizal communities (Anderson
and Cairney 2004; Gasparotto et al. 2010; Clasen et al. 2018). Starting with the
extraction of nucleic acids from the fungi, it is possible to get information regarding
the structure of the fungal community, which can be accessed through analysis and
construction of cloned libraries, sequencing, and fingerprinting techniques (Lambais
et al. 2005; Gasparotto et al. 2010). These techniques have helped to understand the
diversity and ecology of mycorrhizal fungi and their impact on plant development.
Thus, our main objective of this chapter is to describe succinctly the most impor-
tant structures of arbuscular mycorrhiza and ectomycorrhiza, and to detail these
associations in pure and mixed eucalyptus and acacia plantations, highlighting the
main results obtained in Brazil. We hope that this information contributes to the
understanding of the interactions that occur in these planting systems, in order to
assist forest production and environmental sustainability.

7.2 Arbuscular Mycorrhizal Fungi (AMF)

The arbuscular mycorrhizal symbioses result from the association of arbuscular

mycorrhizal fungi (AMF), belonging to the phylum Glomeromycota with the root
system of more than 90% of the vascular plants (Wang and Qiu 2006; Willis et al.
2013). These fungi present an obligate biotrophic behavior because they depend on a
living host to fulfill their biological cycle. In this association, the host plant supplies
the fungus with more than 10% of the photosynthates produced and, in return, the
plants are benefited by improving their nutritional status, especially in soils where the
nutrient supply is low or unbalanced (Smith and Read 2008; Cardoso et al. 2010).
7 Mycorrhiza in Mixed Plantations 139

An interesting point is that AMF are not very selective with regard to their host
plants; that is, they show almost no host specificity (Santos et al. 2006; Smith and
Read 2008). Nevertheless, there is a great variability in the outcome or in the
­effectiveness of different host plant-AMF combinations, influenced by both the host
plant and the fungus, and modulated by edaphoclimatic conditions, especially P
(Cardoso et al. 2017). Thus, the growth-promoting effect of an AMF depends on the
level of available P in the soil. The more P, the less will be the positive effect of
AMF inoculation. This is doubtless one of the causes for AMF being extremely
effective in P-depleted tropical soils, much more than in soils of greater fertility. On
the other hand, even in the presence of mycorrhizas, a minimum of available phos-
phate in soils is required to result in satisfactory plant growth, and this minimum
varies according to the plant, endophyte, and soil characteristics. Mycorrhizal endo-
phytes colonize the roots much more extensively under low-P conditions. As soil P
concentrations increase, the root colonization decreases strongly (Nogueira and
Cardoso 2006; Cardoso et al. 2017).
The formation of AMF mycorrhiza starts with the exchange of signals between
the host plant and the AMF propagules, with the exudation by the roots of com-
pounds that stimulate the branching of the fungal hyphae. These hyphae, when they
enter in contact with the surface of the roots, differentiate into appressoria, and
penetrate through the epidermis (Lambais 2010). Within the roots, the hyphae may
grow inter- and intracellularly in the cortical tissue, not ever invading the meriste-
matic region and vascular tissues. These hyphae differ in arbuscules or hyphal coils,
structures that morphologically describe the two types of AM, Arum type and Paris
type (Gallaud 1905). The Arum type is the most common, identified by the growth
of inter- and intracellular hyphae and the production of intracellular arbuscules in
the cells of the root cortex. The Paris type is defined by cell-to-cell growth of intra-
cellular hyphal coils (Smith and Smith 2011).
A prominent feature of the Arum-type morphology is the intercellular growth of
hyphae in a longitudinal manner through the root. Arbuscules arise on short side
branches from these intercellular hyphae, typically at right angles to the main root
axis (Smith and Smith 2011). Coils of the Paris type of mycorrhiza often, but not
invariably, become arbusculate; that is, they develop arbuscule branches from one
or more loci on the coil (Gallaud 1905; Smith and Smith 2011; Dickson 2004;
Requeña et al. 2007). Arbuscules and hyphal coils are extremely important struc-
tures in the process of exchanging metabolites and nutrients between the symbi-
onts, but the mechanisms controlling their development and functioning are little
known (Lambais 2010).
Other characteristic components of some AM are vesicles, lipid-rich structures
whose function is a nutrient reserve (Moreira and Siqueira 2006), but they do not
occur in all AMF species. In AMF genera as Gigaspora and Scutellospora, that do
not present such structures, normally one can find extraradical organelles with an
equivalent function, called secondary cells. Besides, AMF produce extraradical
­fungal spores present in the soil and, in some cases, in the roots (Smith and Read
2008). AMF spores vary in size from 22 to 1050 μm (Stürmer 2012), and it is
through their descriptions that the identification of AMF species traditionally is
140 M. C. Santana et al.

c­ arried out (Schenck and Perez 1990; INVAM (http://invam.caf.wvu.edu)). The MA

does not produce macroscopic morphological alterations in the host roots, so that it
is ­necessary to treat them by means of clarification and dyeing processes and to
examine them under the microscope (Siqueira et al. 2002).
Another feature is the presence of a minimum number of spores in the substrate
to result in root colonization, the infection potential. This potential likewise depends
on the biotic and abiotic conditions, which modulate the colonization intensity
(Santana 2017; Steffen et al. 2010; Moreira and Siqueira 2006; Smith and Read 2008).

7.3 Ectomycorrhizal Fungi (ECMF)

Ectomycorrhiza is a symbiotic relationship that occurs between fungi belonging to

the phyla Basidiomycota and Ascomycota (Clasen et al. 2018), with roots of various
species of Gymnosperms and Angiosperms (Brundrett 1991). We estimate that there
are more than 5000 fungal species that form ECM, predominantly with tree species
of temperate climatic regions (Futai et al. 2008). In tropical regions, most tree spe-
cies form AM; however, the study of ECM in these regions is driven by the exten-
sive use of exotic species in reforestation programs such as Pinus, Eucalyptus, and
Acacia (Kasuya et al. 2010).
In ECM symbioses, fungi also use energetic organic compounds, and in turn
promote the mineralization of organic forms of the nutrients and solubilize minerals
through the production of organic acids, making these elements available for absorp-
tion (Shah et al. 2016). The formation of ECM changes the environment of the
­rhizosphere, which becomes unfavorable for most pathogens of the root system
(Garbaye 1991). ECM symbiosis is characterized by presenting a fungal mantle, a
hyphal layer formed externally to the root epidermis, and a Hartig net, with growth
of the hyphae in the intercellular spaces of the root cortex (Agerer 1995; Vesk et al.
2000; Brundrett 2002). Extending from the mantle there are fungal rhizomorphs,
similar to plant roots, essential for the connection of the fungus with the soil to
produce fruiting bodies (Smith and Read 2010).
The fungal mantle helps in the transfer of nutrients to the plants and acts as a
mechanism of protection against pathogens (Peterson and Bonfante 1994). In the
mantle, there also occurs the synthesis of reserve compounds such as glycogen, poly-
phosphates, and proteins (Peterson and Bonfante 1994). Starting at the rhizomorphs
the hyphae extend outwardly in all directions through the soil, forming a dense net-
work connecting different plants, conducive to the exchange of organic and inorganic
nutrients. It also helps the roots to assess an increased soil volume for water and
nutrients (Brundrett 2002; Shah et al. 2016). The Hartig net growing in between the
cortex cells has a great contact interface with the plant and is the site of nutrient
exchange between the symbionts. In angiosperms, the Hartig net is generally limited
to only a few more external plant cell layers in the cortex, whereas in gymnosperms
it may comprise the intercellular spaces of all cell layers, though never surpassing the
outer limit of the cortex imposed by the root endodermis (Kasuya et al. 2010).
7 Mycorrhiza in Mixed Plantations 141

Unlike AMF, ECMF are not obligate biotrophs and can be cultivated on some
culture media. ECM modifies the morphology of the plant roots and may inhibit the
formation of root hairs, which are replaced by fungal hyphae (Kasuya et al. 2010).
The ECM roots can take different forms, as nodular, pyramidal, bifurcated, and
coralloid, among others, with a highly variable color spectrum of the fungal myce-
lium (black, red, yellow, brown, white, etc.), which will equally define the external
coloration of the root mantle (Agerer 2001; Tedersoo and Brundrett 2017). Variations
in mantle structure, surface ornamentations, staining, and presence of rhizomorphs
are used, along with chemical and immunological tests, to characterize the ECM
and for identification of the associated fungus (Clasen et al. 2018), although nowa-
days there is opening up of the opportunity of molecular technology for the taxo-
nomic classification of these fungi (Suz et al. 2008).

7.4  M and ECM Symbiosis in Pure and Mixed Plantation

A
of Eucalyptus sp. and Acacia sp.

The occurrence of mycorrhiza in eucalyptus species was mentioned for the first time
in 1917 by van der Bijl (Barros et al. 1978), but the interest in this association began
to gain prominence with the first attempts to classify and describe the structure of
mycorrhiza in eucalyptus by Chilvers and Pryor (1965). The work of these research-
ers complemented by others, such as Levisohn (1958), shows that apparently all
species of eucalyptus are able to form mycorrhiza. From this period on, the study of
the effect of mycorrhizal fungi on eucalyptus growth and survival has been addressed
in the literature. Researchers have shown that symbiosis provides a great success of
these plants in forest plantations (Chen et al. 2007, 2014; Futai et al. 2008; Souza
et al. 2008; Chiquete 2011; Bini et al. 2018).
Similar to eucalyptus, acacia plants also associate symbiotically with mycorrhizal
fungi (Pereira 2015; Santana 2017). Besides that, acacia species with few exceptions
nodulate and fix nitrogen with root nodule bacteria in the range of 20 to
300 kg ha−1 year−1 (Dommergues 1987). Mycorrhiza enhances nutrient absorption,
particularly P, and water uptake by acacia species and improves their nitrogen fixation,
which enables them to establish in marginalized lands in the tropics (Requeña et al.
2001). These associations contribute to their tolerance to drought, and induce resis-
tance against soil pathogens (Smith and Read 2008). These associations, in general,
enable many of the acacia species to perform well in degraded soils with high acidity,
high salinity, high aluminum saturation, and low soil fertility (Craig et al. 1991).
As we have seen, the roots of Eucalyptus and Acacia can be colonized by
mycorrhizal fungi and there have been reports that these plants can be colonized
by both types of mycorrhiza, AM or ECM either alone or together. Pereira (2015)
and Santana (2017), through morphological characterization, reported coloniza-
tion of AM and ECM in both eucalyptus and acacia roots in pure and mixed planta-
tions in Brazil. While eucalyptus and acacia roots can establish symbioses with
both AMF and ECM fungi, several studies show a succession in the establishment
142 M. C. Santana et al.

of the two fungal communities. Symbiosis with AMF fungi is predominantly pres-
ent when trees are young, followed by symbiosis with ECM fungal communities
(Bellei et al. 1992; Oliveira et al. 1997). The two symbioses can, however, be
observed at the same time. This ability to form both types of symbiosis is very
interesting from a nutrient acquisition point of view, with the AMF symbiosis
being especially recognized for their assimilation of P, and the ECM symbiosis
may play a more important role in the assimilation of N (Read 1991).
Bini et al. (2018) studied the root colonization rates by AMF in Eucalyptus gran-
dis and Acacia mangium, in monocultures and consortia, at 7, 14, and 20 months
after planting, and found that there was a medium-to-high AMF colonization rate
(above 34%), especially at 14 months. In monocultures of A. mangium (A) there
were the highest colonization rates in all sampling times, although at 14 and
20 months there was no significant difference between monocultures and consortia
(A. mangium + E. grandis (A + E) and E. grandis + A. mangium (E + A)). In pure
E. grandis (E) plantations, there was a lower AMF colonization rate. When evaluat-
ing the same treatments, however, at 48 months, Pereira et al. (2018) found lower
AMF colonization rates, with mean percentages varying between close to 0 and
10%. In A. mangium, at this time, there was a still greater decline in AMF root colo-
nization although high percentages of ECM were observed. At 48 months, however,
the root colonization of Acacia by AMF regressed strongly, while ECM showed
high colonization rates (Table 7.1).
In a different field experiment, similar to that of Bini (2012) and Pereira (2015),
Santana (2017) showed that, at 24 months, the ECMF colonization rate is higher
(49% in the 0–10 cm layer of soil and 12% in the 20–50 cm) when compared to the
colonization rate by AMF (30% in the 0–10 cm layer and 10% in the 50–100 cm
layer) (Fig. 7.1). These data are similar to those reported by Pereira (2015), who
found higher ECM values in relation to AMF in all evaluated plants. This difference
in symbiotic fungal communities according to the age of eucalyptus and acacia
plantations could have consequences also in the carbon cycle. Indeed, recent studies
have shown a difference in rate of decomposition between tree species associated
with AMF fungi or ECM fungi, with the litter of the AMF trees decomposing faster
(Midgley et al. 2015; Taylor et al. 2016). Variations of exudation rates have been
detected, and trees associated with ECM exude more carbon than AMF trees (Yin

Table 7.1 Percent root colonization by AMF or ECMF in pure or mixed plantations of Eucalyptus
grandis (E) and Acacia mangium (A) at different times after transplanting of seedlings
Months after transplantation
AMF ECM
Treatments 7 14 20 48 48
A. mangium (A) 51 aA 53 aA 45 aB 7.1 bC 33.3 bB
E. grandis (E) 35 cB 45 bA 38 bB 9.3 aC 52.3 aA
A. mangium in consortium (A + E) 42 bB 52 aA 44 aB 2.0 cC 34.6 bB
E. grandis in consortium (E + A) 43 bB 50 abA 42 abB 0.7 dC 33.0 bB
Here we summarize the data obtained by Bini (2012) and Pereira (2015)
Adapted from Bini (2012) and Pereira (2015), cited by Cardoso et al. (2017)
7 Mycorrhiza in Mixed Plantations 143

Fig. 7.1 Colonization by AMF in a mixed plantation (E+A) (a) and ECMF (b) in Eucalyptus
growing in consortium (CE), Acacia in consortium (CA), Eucalyptus (E) and Acacia (A) in mono-
culture along a soil depth gradient (cm) (Santana 2017)

et al. 2014; Liese et al. 2018). The differences in traits between AMF and ECM
fungi (such as the amount of rhizomorphs and the presence of pigments) (Aguilar-­
Trigueros et al. 2014; Churchland and Grayston 2014) can have important impacts
on soil carbon storage and a better understanding of the impact of associations
between the two mycorrhizal communities is an important issue.
Despite the fact that AMF colonization was found in eucalyptus roots planted in
a consortium with acacia, Santana (2017) did not find arbuscular mycorrhiza in
Acacia mangium plants in this forest system (neither in pure nor in mixed stands
with eucalyptus) (Figs. 7.1 and 7.4c). A. mangium, besides forming symbiosis with
AMF, also associates symbiotically with nitrogen-fixing bacteria (NFB), forming a
tripartite symbiosis: AMF–plant–NFB (Carvalho and Moreira 2010). As both
microorganisms of this symbiosis depend on the C sources offered by the plant for
their survival, the costs of maintaining the tripartite symbiosis for the plant are
­considerable (Mortimer et al. 2008). In this way, the plant needs mechanisms that
allow it to control both symbioses according to its needs. In a study with plants
inoculated with AMF or NFB, in which inoculation with the second symbiont was
done 20 days after inoculation with the first symbiont, it was possible to observe
that the pre-­establishment of NFB suppressed subsequent formation of AMF and
vice versa (Bethlenfalvay et al. 1985).
In the experiment performed by Santana (2017), we reported the formation of
NFB nodules formed, in addition to ECM in roots of A. mangium (Fig. 7.2).
Furthermore, it was found, through chemical and multivariate analyses, that N and
P concentrations in the root correlated negatively with AMF root colonization, and
acacia plants presented high mineral nutrient concentrations when compared with
Eucalyptus roots. These data may be the explanation for the absence of mycorrhiza,
probably indicating that there was no need for AMF colonization at this stage of
acacia development. However, when in optimal conditions the tripartite leguminous
symbiosis corresponds to a maximal return in growth and productivity of the plant,
as occurred in an experiment with soybeans as test plants (Cardoso 1985), which
144 M. C. Santana et al.

Fig. 7.2 Root colonization by ectomycorrhizal fungi (A) ECM associated with roots of Acacia
mangium involving the fungus Cenococcum sp., (B) ECM associated with Eucalyptus grandis
probably involving Pisolithus sp. fungi. Photo A taken by photo camera and photo B taken by
binocular stereoscopic microscope with 40-fold magnification. NOD Nitrogen-fixing bacterial
nodule (Santana, M.C., personal data)

corroborated the results of a previous study with a similar outline of Bethlenfalvay

et al. (1985).
Analyzing the total number of AMF spores and colonization of A. mangium
roots, Santana (2017) observed that the presence of spores in the soil did not
­correlate with the intensity of root colonization. This result is in agreement with the
data of Steffen et al. (2010), who observed that the number of spores in the substrate
did not correspond to the degree of colonization of E. grandis roots. According to
Moreira and Siqueira (2006) and Smith and Read (2008), the presence of mycor-
rhizal spores in the soil or substrate will result in nutritional and adaptive benefits to
the host plant, if the biotic and abiotic conditions of the site allow colonization.
Through the morphological analysis of AMF spores, Santana (2017) found the
fungi Glomus macrocarpum, Acaulospora mellea, Racocetra sp., and Gigaspora
sp. (Fig. 7.3). These fungi were considered of common occurrence in areas with
eucalyptus plantations (Gomes and Trufem 1998) and A. mangium (Caproni et al.
2005). Cavagnaro et al. (2007) found, in an experiment with plants of Lycopersicon
esculentum, that different species of the genus Glomus can form either Arum- or
Paris-type mycorrhiza, and reported that the genera Gigaspora and Scutellospora
formed mycorrhiza of the Paris type in this experiment.
Santana (2017) demonstrated the formation of Paris-type mycorrhizae in roots of
E. grandis in monoculture or in a consortium with A. mangium (Fig. 7.4). Complete
absence of arbuscules or of coils in eucalyptus roots was also reported by Campos
et al. (2011) in another survey, while Pereira et al. (2018) reported the presence of
Paris-type mycorrhizae in eucalyptus roots. However, Malajczuk et al. (1981)
observed the presence of both types of mycorrhizae, with hyphal coils and arbus-
cules in another plantation, in Eucalyptus diversicolor and Eucalyptus marginata.
Since there is still a great knowledge gap regarding the functional aspects involved
in both types, we suggest that, in future studies, the morphotype of the fungus and
eventual successional stages should also be reported and not just the presence or
absence of the symbiosis (Berbara et al. 2006).
7 Mycorrhiza in Mixed Plantations 145

Fig. 7.3 Spores of arbuscular mycorrhizal fungi. (a) Gigaspora sp. spore found in a consortium
of Eucalyptus and Acacia, in the 0–10 cm soil layer (20×). (b) Glomus macrocarpum spores, found
in the same plantation, in the 10–20 cm soil layer (10×) (Photos: Denise de Lourdes C. Mescolotti
(USP-ESALQ) Santana (2017))

Fig. 7.4 Arbuscular mycorrhizal colonization. In a–c there are hyphae (h), vesicles (v), and spores
(e) although no arbuscules. In d–f the presence of hyphal coils (hc), g shows a root without colo-
nization. A and G with 10-fold magnification; b–f with 40-fold magnification (optical microscope)
(Santana 2017)

Many ECM fungi have a broad host range while others are more specific and
colonize certain hosts or host genera (Molina et al. 1992). For AM fungi, so far no
convincing evidence was presented demonstrating that these are host specific,
although host preferences and host selectivity have been widely reported (Helgason
et al. 1998; Vandenkoornhuyse et al. 2003; Torrecillas et al. 2012). A high-­throughput
sequencing study (using the technology 454) carried out on pure eucalyptus or
­acacia plantations in the Congo (Pointe-Noire) on the AMF fungi community
revealed the predominant presence of the genus Rhizophagus associated with the
146 M. C. Santana et al.

Fig. 7.5 Colonization of E. grandis and A. mangium roots by the strain Pisolithus sp. 45, after
90 days of inoculation. Microscopic images from the transversal root cuttings show the Hartig
nets. For acacia roots, fungal cells appear in blue (Uvitex fluorescent dye to stain the intercellular
cortex cell spaces). Photos: Yves Prin (Cirad, UMR LSTM, France) and Ranieri Ribeiro Paula
(USP-ESALQ) (Robin A., personal data)

roots of acacia (approximately 80% of Rhizophagus sequences associated with

­acacia roots against 18% of sequences associated with eucalyptus roots). In opposi-
tion, the genus Gigaspora was mainly associated with eucalyptus roots (approxi-
mately 60% of Gigaspora sequences associated with the roots of eucalyptus against
8% of these sequences associated with acacia roots) (Robin A., personal data).
When the same ECM fungus colonizes the roots of both species, a different colo-
nization of root tissues was observed between the roots of Eucalyptus and Acacia.
A study made in controlled conditions showed that the same strain of Pisolithus sp.
45 could colonize both Eucalyptus and Acacia roots. However, interestingly, a
microscopic cross section clearly showed a difference in colonization. Pisolithus
penetrates only the first few layers of the epidermis of the eucalyptus roots whereas,
for the acacia, the fungus reaches the endodermis (Fig. 7.5).

7.5 Mycorrhiza in Deep Soil Layers

Few studies were conducted on mycorrhizal fungi associated with roots in deep soil
layers, despite the growing interest in studies of microbial communities in deep
soils (Li et al. 2014; Gocke et al. 2017; Pereira et al. 2017; Zheng et al. 2017), with
studies in mixed plantations being even rarer. A recent survey demonstrated the
presence of AMF fungal spores in deep soil layers down to 8 m in pure and mixed
7 Mycorrhiza in Mixed Plantations 147

Eucalyptus grandis and Acacia mangium plantations in Brazil (Pereira et al. 2018)
and in the rhizosphere of Faidherbia albida in Senegal, where the AMF spores were
detected as deep as at 34 m below soil level (Dalpé et al. 2000). Pereira et al. (2018)
showed AMF root colonization of Eucalyptus and Acacia for the 0–100 cm soil with
colonization rates between 6 and 25%; however they found only about 10% below
1 m and 5% or 6% below 3 m. This weak AMF colonization may be partly due to
the plants being already over 1 year of age, a period in which commonly the AMF
are substituted gradually by ECMF in Eucalyptus. Nevertheless, these results
­indicate that one should take into account mycorrhizal symbiosis in the deeper
­layers of soil, and not only in the first 30 cm, as is most commonly done. The pres-
ence of ECMF propagules in deep soil has also been described (Santana et al. 2016),
as well as the presence of typical ECM structures in Eucalyptus roots down to 6 m
deep (Lambais et al. 2017).
The minirhizotron method is well suited for root observations and has already
been used to study the dynamics of ECMF (McCormack et al. 2017), but it has
aroused some doubts about the method itself perhaps being the reason for this find-
ing on deep soil mycorrhization, due to contamination of deeper regions by surface
soil. Recently, a new sampling method for deep soil layers was developed by
­sampling fine roots and ECM root tips during the digging of pits, layer by layer, to
avoid contaminations between two continuous layers. This research demonstrated
for the first time the presence of already well-developed ECM symbioses on deep
roots (Robin A. personal data). In this study, the authors showed the mycorrhizal
presence of Pisolithus on eucalyptus at a depth of 4 m. Visual observations were
confirmed by molecular sequencing. The diversity study (by ITS Illumina sequenc-
ing) showed a strong impact of the depth on the intraspecific diversity of the fungus
Pisolithus, with the presence of a reservoir of biodiversity associated with the
deeper roots. The observation of ectomycorrhizal Acacia roots (by Pisolithus or
Scleroderma) down to 1 m deep (Santana 2017) highlights the importance of evalu-
ating deeper layers equally for acacia mycorrhizal colonization. The stratification
between eucalyptus and acacia roots as a function of depth found in mixed planta-
tions (Laclau et al. 2013; Germon et al. 2018) possibly could detect deep root
mycorrhization, perhaps with different mycorrhizal communities when evaluating
pure or mixed plantations between these two tree species.

7.6  nderstanding the Concept of Common Mycorrhizal

U
Networks (CMN) in Mixed Plantations of Eucalyptus
and Acacia: Prospects for Future Research

The concept of mycorrhizal networks, defined as a common mycorrhizal mycelium

linking the roots of at least two plants (Simard et al. 2012), is perfectly applicable
in mixed plantations of eucalyptus and acacia. Common mycorrhizal networks
have been shown to facilitate the transfer of carbon (Simard et al. 1997), nitrogen
(He et al. 2009), and water (Egerton-Warburton et al. 2007; Prieto et al. 2016).
148 M. C. Santana et al.

Concerning the nitrogen cycling by CMN, normally we find an overwhelming

occurrence of the transfer of N compounds from the leguminous N-fixing tree to the
non-fixing eucalyptus. This has also been studied for annual plants (Moyer-Henry
et al. 2006; Jalonen et al. 2009), although nitrogen transfers were demonstrated
between Casuarina cunninghamiana and Eucalyptus (He et al. 2005), highlighting
its great value for eucalyptus, one of the most outstanding species in forestry world-
wide. Transfers through CMN between Acacia and Eucalyptus have been studied
involving AMF (Meng et al. 2015) or ECMF (He et al. 2005). Many studies were
conducted under controlled conditions, for example in the greenhouse, while in situ
in the field direct demonstrations of transfer are more difficult. An in situ study
using fungicides showed 15N transfer via mycorrhizal networks (Montesinos-­
Navarro et al. 2016). In eucalyptus and acacia plantations, N transfer was demon-
strated in situ (Paula et al. 2015). An interesting experiment with a leguminous tree
from the Mimosa group in the Atlantic Forest, nodulated by the beta-Rhizobium
Burkholderia and inoculated by AMF, also demonstrated the synergic action of
these two agents together (Lammel et al. 2015).
Mendes Filho et al. (2010) set up a pot experiment in a greenhouse, with exotic and
native leguminous trees using cassiterite mine spoil as substrate. The substrate was
very poor in microorganisms and even poorer in energetic organic matter, since it
showed an almost absence of respiration when tested using a direct soil respiration
test, but still somewhat more when applying the glucose-induced respiratory test. To
this substrate, distributed in 2 L pots, we applied two main treatments, with or without
organic compost (OM), and all pots were inoculated with a Rhizobium or Burkholderia
strain with specificity for the corresponding leguminous tree. Then, each one of those
main treatments was subdivided into four sub-treatments, i.e., inoculation of AM
fungi, fertilization with P, or application of both, besides a control without any further
treatment, resulting in eight treatments altogether (AMF, P, AMF + P, and control
(OM+) and AMF, P, AMF + P, and control (OM−)), with four replicates. Right after-
wards the seeds of the corresponding tree were planted in each pot.
After 1 month of growth under a constant watering regime, we took photos of the
experiment, which demonstrate that some growth only occurred in the presence of
compost. Acacia mangium (exotic) grew vigorously in AMF (OM+) and AMF + P
(OM+) and showed a much poorer growth in control and P (OM+). In the treatments
without compost (OM−) A. mangium showed only a little growth in the s­ ub-­treatment
AMF + P and still less in AMF. Mimosa caesalpiniaefolia (native tree) responded in
a similar way, but a real satisfactorily growth pattern only appeared in AMF (OM+)
and in AMF + P (OM+), with a little growth in P (OM+). The minimal growth in
some other sub-treatments should be neglected because the seedlings will never
develop satisfactorily (Fig. 7.6).
These results show that in a soil of low fertility, especially when highly eroded,
decapitated, or containing residues of heavy metals, organic matter would be the
most fundamental ingredient for the development of such trees, but we only detected
a real adequate development when they also were provided with AMF. In the case
of A. mangium, even when P was not given, the mycorrhiza alone scavenged all
necessary P from the depleted substrate. Nevertheless, an incipient growth was
observed when growing with compost and receiving P fertilization, as well as in the
7 Mycorrhiza in Mixed Plantations 149

Fig. 7.6 The legumes A. mangium (exotic) and M. caesalpiniaefolia (native), inoculated with the
respective rhizobia, were planted on a very poor and exhausted mine spoil with or without organic
compost (OM), AMF, P or both, and a control (Mendes-Filho et al. 2010; Cardoso and Andreote
2016; Cardoso et al. 2017)

substrate without compost, but when receiving P and AMF inoculation. The Mimosa,
however, seems to be more sensitive to negative soil conditions, with real adequate
development only in the presence of AMF + P or AMF (OM+). In the absence of
mycorrhiza, but in the presence of P (OM+) growth was just incipient.
Obviously, trees of the family Fabaceae will only develop satisfactorily when
­inoculated with the right rhizobia. Since this fact is well known already for a long
time by microbiologists, we did not use rhizobial inoculation as a treatment.
Instead, the adequate rhizobial strain was inoculated together with the seeds in
each pot, since this is by far the most fundamental condition for legume growth,
especially in poor ­substrates. In this study, however, we proved that mycorrhizae
are also an indispensable factor for the rhizobia, because they cannot nodulate
plant seedlings in the absence of P. Yet OM acts simultaneously as a chemical,
physical, and biological ­factor of soil fertility. It acts as a chemical factor, contrib-
uting with some macro- and micronutrients for the plants and regulating the pH;
as a physical factor, providing a more adequate structure of the substrate; and
finally as a biological factor, furnishing the energetic substances necessary for the
nutrition and multiplication of microorganisms, since these are also indispensable
for soil and plant health, breaking down the complex molecules, and providing
mineral nutrients for the plants.
150 M. C. Santana et al.

7.7 Final Remarks

The study of mycorrhizal fungi in pure and mixed eucalyptus and acacia plantations
is still incipient; however the results have been promising, especially for mixed
plantations with both species. We have shown that the mycorrhizal root colonization
of these plants differs when in intercropping. These effects are also dependent on
several edaphic-climatic factors and can be affected by plant age, since their type
and intensity are variable from site to site. Likewise, we have yet an important
knowledge gap regarding the functional aspects involved in the mycorrhizal
­symbiosis, mainly for nutrient transfer between trees. For example, although Paula
et al. (2015) showed the N transfer from acacia to eucalyptus roots, it would be
­difficult to guarantee its mediation through the mycorrhizal hyphal system, and the
mechanisms remain to be studied to know if a part of this transfer could be due to
mycorrhizal networks. For the future, we suggest a major focus on the fungus
­morphotype analysis for ECM symbiosis, as well as on the eventual successional
processes from AM to ECM in the later stages of forest plantations. We also need to
go beyond diversity approaches and to study more the functional aspects of these
symbioses, and not only taking into account the first few centimeters of soil, with
researches in the total depth of the soil profile. Implementing a holistic view of the
mycorrhizal community in pure and mixed Eucalyptus and Acacia plantation will
help the producers to get a more effective and sustainable production, reducing
agrochemicals and other external inputs.

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Chapter 8
Mesofauna and Macrofauna in Soil
and Litter of Mixed Plantations

Maurício Rumenos Guidetti Zagatto, Luís Carlos Iuñes Oliveira Filho,

Pâmela Niederauer Pompeo, Cintia Carla Niva, Dilmar Baretta,
and Elke Jurandy Bran Nogueira Cardoso

8.1 General Introduction

The soil fauna comprises the invertebrate community that lives permanently or at least
in one of their development stages in soil or litter (Zagatto et al. 2017). These inverte-
brates may be classified according to the body diameter as microfauna, mesofauna,
and macrofauna (Swift et al. 1979; Baretta et al. 2011). The soil microfauna comprises
those invertebrates with body diameter smaller than 0.2 mm, while mesofauna lies
between 0.2 and 2.0 mm, and macrofauna comprises the larger invertebrates with
body diameter between 2 and 20 mm (Lavelle 1997; Oliveira Filho et al. 2018).
The soil macrofauna comprises the larger invertebrates, called “ecosystem engi-
neers,” since they affect the soil structure, building galleries and enlarging pores, as
the earthworms and termites, while many of them mix organic matter with the min-
eral superficial layers of the soil profile. Still others move tons of soil while building
their nests sometimes connected by kilometers of underground galleries, as ants and
termites (Bardgett and Van der Putten 2014; Brown et al. 2015; Pereira et al. 2017b).
The soil mesofauna comprises mainly mites and springtails, besides several
insects, myriapods, oligochaeta, crustacea, and others, which live mainly in the lit-
ter or on the soil surface. These small invertebrates actively participate in the initial

M. R. G. Zagatto (*) · E. J. Bran Nogueira Cardoso

Department of Soil Science, University of São Paulo, “Luiz de Queiroz” College of
Agriculture, Piracicaba, SP, Brazil
L. C. I. Oliveira Filho · P. N. Pompeo · D. Baretta
Santa Catarina State University, Chapecó, SC, Brazil
C. C. Niva
Embrapa Cerrados, Brazilian Agricultural Research Corporation, Planaltina, DF, Brazil

© Springer Nature Switzerland AG 2020 155

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_8
156 M. R. G. Zagatto et al.

fragmentation of organic matter and, consequently, favor microbial decomposition,

nutrient cycling, and soil aggregation (Barbercheck et al. 2009; Lavelle et al. 1997).
They also may be fungivorous, vegetarian, coprofagous, predators, parasitic, etc.
Soil fauna abundance and diversity are modulated by vegetation, weather, mois-
ture, temperature, and agrochemical and fertilizer inputs, among other factors.
These characteristics make them excellent bioindicators, since the presence or
absence of several invertebrate groups and their quantity may reflect soil health or
environmental degradation (Anderson 2009; Cardoso et al. 2013). The native eco-
systems present great diversity and low dominance and, consequently, higher resis-
tance and resilience than agricultural ecosystem (Zagatto et al. 2019b). In natural
ecosystems, certain species present a greater tolerance to environmental stress and
the higher species diversity in such ecosystems increases the functional redundancy
(McCann 2000).
Due to the several functions performed by the invertebrates in soil, they are
related to ecosystem processes and services as C sequestration, greenhouse gas
mitigation, pest and disease control, and soil water storage. These aspects modify
plant production, the habitat function of soil for other organisms, and the air and
water flows in soil (Van Der Putten et al. 2004; Wagg et al. 2014; Creamer et al. 2016).
Eucalyptus cultivation is favored by tropical climate and this genus is planted in
many regions of the world because of its rapid growth cycle and production of
multipurpose wood (Ibá 2015). However, intensive cultivation leads to the deple-
tion of N and other soil nutrients, requiring a high input of mineral fertilizers to
avoid a decrease in the production rates (Gonçalves et al. 2008). Thus, the consor-
tium of Eucalyptus with N-fixing trees allows for a decrease in fertilizer use,
enriching the soil with N due to high biological nitrogen fixation (Forrester et al.
2006; Laclau et al. 2008, Chap. 6). Recently, in Brazil, intercropped plantations of
Eucalyptus grandis (Eucalyptus) and Acacia mangium (Acacia) demonstrated high
sustainability in comparison with Eucalyptus monocultures, favoring the microbial
community, especially the phylum Proteobacteria, which contains most species
involved in biological nitrogen fixation, as Rhizobium with A. mangium (Pereira
et al. 2017a).
Moreover, mixed plantations of E. grandis and A. mangium deposit great amounts
of litter on the soil surface (Chap. 3), which may serve as habitat and food for
microorganisms and soil fauna. The formation of a litter layer helps to avoid soil
heating and soil erosion and consists of a great organic reservoir that releases sev-
eral nutrients to the soil solution, modulated mainly by weather, soil fauna, and
microorganisms (Bachega et al. 2016).
Therefore, this chapter intends to clarify the effect of N-fixing tree introduction
in Eucalyptus monocultures (especially of the mix E. grandis and A. mangium), on
the soil faunal community. To our knowledge, there are no studies on soil and meso-
fauna in Brazil, especially not in mixed cultures of Eucalyptus and Acacia.
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 157

8.2 Effect of Forest Plantations on Soil Macrofauna

In forest management, some specific practices can cause changes in soil invertebrate
biodiversity and consequently in the ecosystem performance, because they partici-
pate in ecosystem processes at different scales, both temporal and spatial, including
organic matter decomposition, regulation of soil and nutrient losses, or bioturbation.
Different forest management systems influence the soil macrofauna, which is
important to maintain soil properties, because they are responsible for the creation
of biogenic structures that promote changes in soil physical characteristics, as well
as the availability of resources to other organisms (Brown et al. 2015; Pereira et al.
2015). Similarly, tree plantations may vary in structure and composition, and these
variations may alter soil macrofauna communities (Warren and Zou 2002).
Forest and agricultural practices can have profound effects on population levels
and species composition of various groups of organisms. Among the most affected
by plantations of exotic species are insects such as beetles and ants, given their high
sensitivity to changes in ecosystems (Aliaga et al. 2017). In this sense, many studies
have evaluated these and other groups of soil macrofauna in different forest and
agricultural land-use systems and demonstrated how land use and soil management
impact these communities.
Warren and Zou (2002) evaluated the abundance and biomass of soil macroinver-
tebrates in Leucaena leucocephala, Casuarina equisetifolia, and E. robusta plants,
being 9 years old, at a degraded site in Puerto Rico. The nutrient concentrations and
the permanent litter stocks on the forest floor were also determined to examine the
relationship between litter chemistry and soil macroinvertebrates. Leucaena planta-
tions had greater abundances and biomass of millipede species than Casuarina and
Eucalyptus. The biomass of the earthworms did not differ between the plantings.
Millipede biomass was highly correlated with the N concentration and C/N ratio of
the litter. The results found by the authors suggest that plantations of tree species
differ in their influence on soil macrofauna, and the biomass and abundance of soil
fauna can be regulated through the careful selection of tree species for planting in
degraded tropical lands.
Rosa et al. (2015), studying the Plateau region of Santa Catarina (Brazil), aimed
to evaluate the effect of land-use systems on the distribution of soil macrofauna and
its relationship with soil chemical and physical attributes. In that study, native for-
est, Eucalyptus plantation, and perennial pasture favored edaphic biodiversity and
were considered more stable than the crop-livestock integration and no-tillage sys-
tems with greater anthropogenic intervention, which reduced the macrofauna groups
of the soil. The authors collected the fauna using soil monoliths (area 0.25 m by
0.25 m), which were excavated following the standard Tropical Soil Biology and
Fertility (TSBF) sampling protocol (Anderson and Ingram 1993), using a sampling
grid with nine points in each area and three true replicates of each land-use system.
The fauna group that contributed the most to separate the eucalyptus plantation
from the crop-livestock integration and no-tillage was Isoptera (termites) and from
the native forest was Formicidae. The diversity measured by the Shannon-Wiener
158 M. R. G. Zagatto et al.

index was higher in the native forest, followed by the eucalyptus plantation, both in
winter and summer.
Souza et al. (2016) carried out a similar study with the soil macrofauna in the
Eastern region of Santa Catarina and found similar results, where they evidenced the
eucalyptus plantation as a system with greater stability for the biodiversity of the soil
fauna, together with the native forest and perennial pasture, when compared to sys-
tems with annual crops. As a result, greater densities of individuals in eucalyptus
plantation and perennial pasture (in summer) were found than in other systems,
resulting in higher values of diversity. The most important groups of soil macrofauna
to differentiate land-use systems were Formicidae, Coleoptera, and Oligochaeta.
Kamau et al. (2017) evaluated the soil macrofauna at sites after different periods
of conversion of primary forests to cropland, considering dominant tree species in
the region (Croton megalocarpus, E. grandis, and Zanthoxylum gilletii), in
Kapchorwa, Uganda, and demonstrated the importance of the diversity of tree cover
in agricultural landscapes for soil macrofauna conservation. The authors sampled
the fauna by the soil monolith method to verify if the spatial variation in the soil
macrofauna abundance is affected by the age of cultivation, tree species, and dis-
tance from the trunk of the tree. The results showed a greater abundance of macro-
fauna in the soil after 16–62 years of cultivation than in the first 10 years, although
this varied with the tree species and macrofaunal group. The abundance of earth-
worms was higher below the canopy of Z. gilletii; beetles were found in higher
numbers under E. grandis and C. megalocarpus than under Z. gilletii; higher num-
bers of termites and centipedes were found under E. grandis after 16 years of culti-
vation. The quality of organic residues from trees has shown an important effect on
macrofauna abundance and spatial distribution, indicating that the increasing diver-
sity of tree species in agroecosystems can play an important role in maintaining
biodiversity and ecosystem services (Kamau et al. 2017).
As observed in these studies, some groups of the soil macrofauna present greater
contribution to demonstrate changes in the environments, in spite of seasonal effects.
When evaluating families of Coleoptera they found low abundances in eucalyptus
plantations; however, higher values of the diversity index of Shannon-Wiener were
found in this system (Pompeo et al. 2016). The authors sampled Coleoptera using the
same sampling technique in five agricultural and forest systems in the Plateau region
of Santa Catarina. As seen in Fig. 8.1, some families were more associated with the
eucalyptus plantation, and in winter the eucalyptus and native forest systems were
related to a larger number of families, with Curculionidae and Chrysomelidae being
the most associated ones. The families Staphylinidae and Phalacridae were related to
the native forest. In summer, the native forest system was different from the other
systems, and showed relations with a greater number of families, especially
Staphylinidae, Chrysomelidae, and Leiodidae; in the eucalyptus plantation system,
there was an association with Tenebrionidae, Phalacridae, and Curculionidae.
Bartz et al. (2014) studying the same land-use systems in municipalities of the
West and Plateau regions of Santa Catarina evaluated the richness of earthworm
species collected by soil monoliths and qualitative random samplings using allea-
tory excavations. In all systems, 24 species were identified, with 19 native species,
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 159

Fig. 8.1 Principal component analysis of Coleoptera families distinguishing land-use systems in
winter (left) and summer (right), and environmental variables, used as explanatory variables, in the
Southern Santa Catarina Plateau (Pompeo et al. 2016). NF native forest, EST Eucalyptus stands,
PA perennial pasture, CLI crop-livestock integration, NT no-tillage, OM organic matter, TP total
porosity, MWD mean weight diameter, Bio biopores, Anobi Anobiidae, Carab Carabidae, Scydm
Scydmaenidae, Curcu Curculionidae, Chrys Chrysomelidae, Phala Phalacridae, Staph
Staphylinidae, Dryop Dryopidae, Leiod Leiodidae, Scara Scarabaeidae, Psela Pselaphidae, Silva
Silvanidae, Teneb Tenebrionidae, Chelo Chelonariidae, Ptilo Ptilodactylidae

including several ones that were new to science. Considering both regions together,
native species accounted for 90%, 89%, and 80% of the species richness in native
forest, eucalyptus plantation, and perennial grassland systems, respectively, while
in annual cropping systems native species accounted for 65% and 60% of the total
wealth in crop-livestock integration and no-tillage. In the western region, native
forests and no-tillage assemblages were composed exclusively of native species,
while in grazing and crop-livestock integration they represented 75% and 58%. The
Plateau assemblies were composed of 100% native species in eucalyptus plantation
and pasture, 88% in native forest, and only 67% and 54% in crop-livestock integra-
tion and no-tillage. These results highlight the importance of systematic surveys
because prior to this study little was known about the impacts of forest and agricul-
tural land use on earthworm populations in this region of Brazil.

8.3  esofauna Community in Mixed Plantations

M
of Eucalyptus and Acacia: Effects of Soil and Litter
Quality

The soil and litter samples for mesofauna assessment in pure and mixed plantations
of E. grandis and A. mangium were collected at the Experimental Station of Forest
Sciences located in Itatinga, São Paulo state, Brazil (23°02′01”S and 48°97′30”W).
160 M. R. G. Zagatto et al.

Fig. 8.2 Principal component analysis for soil quality variables based on microbiological, physi-
cochemical, and mesofaunal attributes in pure and mixed plantations of Acacia mangium and
Eucalyptus grandis under lower soil moisture (left—water soil content = 4.8%) and higher soil
moisture (right—water soil content = 8.6%)

The soil was classified as a Geric Rhodic Ferralsol (FAO) with a texture of 84%
sand, 4% silt, and 12% clay (Bini et al. 2013). The climate in this region is Cfa
(Köppen classification), with an annual rainfall of 1350 mm, mostly (75%) concen-
trated between March and October (Laclau et al. 2008).
In soil under mixed plantations of Acacia mangium and Eucalyptus grandis, we
can find the coexistence of some organisms originally belonging exclusively to
Acacia mangium or to Eucalyptus grandis, as is the case of Enchytraeidae, Isopoda,
and Thysanoptera (Zagatto et al. 2019a). This finding suggests that pure plantations
of Acacia mangium and mixed plantations of Acacia and Eucalyptus present better
soil conditions for soil fauna. The order Thysanoptera for example comprises some
predators which require a well-established food chain for their development (Blasi
et al. 2013; Melloni and Varanda 2015; Mound 2005). Enchytraeidae and Isopoda,
on their turn, actively comminute the organic matter and stimulate the microbial
activity and, consequently, the nutrient release to the soil solution (Paoletti and
Hassall 1999; Van Vliet et al. 2004; Filser et al. 2016).
Recent research shows that soil moisture is one of the main abiotic factors
responsible for the development of those invertebrates. In periods of severe water
scarcity, a positive correlation was found between the abundance of soil mesofauna
groups and soil microbiological attributes under pure and mixed Eucalyptus grandis
and Acacia mangium plantations. In the period of higher rainfall, a great indepen-
dence of the microbiological, mesofauna, and soil chemical variables was the rule
(Fig. 8.2). Therefore, we postulate that periods of water scarcity provide a profound
interaction between soil mesofauna and microorganisms, which favors their
survival. During water stress there is also a great feeding difficulty because the
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 161

Fig. 8.3 Mesofaunal density in soil and litter. Values followed by different letters indicate differ-
ences between soil and litter at the same sampling date (Tukey’s test at 5% significance)

decomposition of soil organic matter and the metabolic activities become much
slower than in periods of water abundance.
Microorganisms and fauna in the soil probably build up important interactions for the
ecosystem functioning; however little is known about this relation (Creamer et al. 2016),
when studying the network of biotic interactions in the soil of several land-use systems
in Europe. The authors found strong correlations between nematodes and arbuscular
mycorrhizal fungi (AMF) in arable soils, between nematodes and Archaea and Archaea
and bacteria in grasslands and between enchytraeids and AMF in forests. They also
reported changes in these synergic relations due to changes in soil organic carbon con-
tents and pH. Thus, in acid soils with less than 2% of organic carbon enchytraeids, col-
lembolans and archaea showed strong connections, while in soils close to neutrality
(pH 5–7) there was a greater correlation among mycorrhizae, archaea, and bacteria.
In periods of severe water scarcity, a higher density of mesofauna was present on the
soil surface, below the litter layer, while in the moist period a much higher density of
invertebrates inhabited the litter itself in forest plantations of Eucalyptus grandis and
Acacia mangium (Fig. 8.3). These data suggest the preference of the mesofauna for soil
below the litter where there is some moisture preservation during drought while the
litter is already straw-dry. The litter however is chosen whenever it contains enough
moisture. In periods of drought and high solar irradiation, the litter covers and protects
the soil against excessive desiccation and maintains soil temperature in suitable ranges
for the invertebrates’ development in soil (Choi et al. 2006; Derpsch et al. 2010; Peña-
Peña and Irmler 2016). In addition, our data suggest that there is a great interaction
between soil mesofauna and microorganisms in soil during a drought season (under
low soil and low litter moisture) (Fig. 8.2). This condition allowed higher mesofauna
abundance in soil than in litter at this same sampling period (Fig. 8.3). We were sur-
prised that such a small difference in moisture, with very low values, made a huge
162 M. R. G. Zagatto et al.

Fig. 8.4 Redundancy analysis (RDA) between response variables (biological litter attributes—
grey vectors) and explanatory variables (chemical litter attributes—black vectors) in pure E. gran-
dis (E) and A. mangium (AC) plantations, and a mixed system between them (M)

difference in the soil mesofauna habitat preference. Apparently, these invertebrates are
extremely sensitive to weather conditions, since the values for soil moisture typify a dry
soil in both cases.
The litter of Eucalyptus grandis and of Acacia mangium show deep differences
in their chemical constitutions (Pereira et al. 2018), with Acacia litter presenting a
lower C/N ratio and higher contents of several other nutrients, making it more ade-
quate and palatable for the mesofauna (Kaneda and Kaneko 2011) (Fig. 8.4).
Conversely, the higher C/N ratio and Mn contents of Eucalyptus litter correlate
negatively with all groups of fauna sampled. Therefore, the more easily decompos-
able organic material of Acacia litter favors the soil faunal community, considering
also that coprophagy between the different faunal groups is very intense (Kautz
et al. 2002; Teuben and Verhoef 1992).
The rhizosphere of Eucalyptus grandis can exude some volatile compounds, which
result in toxic effects for soil fauna (Zhiqun et al. 2017). In the Eucalyptus rhizosphere,
many such chemical groups were identified, as 2,4-dimethyl heptane, 2,2,4,6-pentam-
ethyl heptane, and 2,4-di-tert-butylphenol, which cause changes in the acetylcholines-
terase (enzyme related to neuronal synapses); superoxide dismutase (related to
superoxide radical changes in H2O2 and O2); and glutathione-S transferase (related to
tissue protection against oxidative stress) (Zhiqun et al. 2017). Hence, it is possible that
these compounds are also responsible for the lower mesofauna abundance and diversity
found in pure Eucalyptus grandis plantations (Fig. 8.3). Nevertheless, more studies are
necessary in order to verify if such compounds are also emitted in the rhizospheres of
mixed plantations and in pure plantations of Acacia mangium.
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 163

8.4  pringtails and Beetles in Forest and Agricultural

S
Systems: An Approach to Morphotypes

Springtails or collembolans are small arthropods belonging to the class Hexapoda.

These organisms usually are less than 2 mm wide and live in moist habitats, eating
fresh organic matter, especially in the topsoil layers. On the other hand, beetles are
larger organisms, much related to chemical and physical soil attributes, since they
mix organic matter with soil clay particles (Filho et al. 2016; Brown et al. 2015).
Springtails and beetles are good bioindicators, since these faunal groups are con-
ditioned by management, weather, and soil chemical, physical, and biological attri-
butes. In addition, these organisms comminute the plant wastes and the soil organic
matter, accelerating the decomposition processes. Therefore, they are considered
soil quality indicators due to their capacity to modify the soil properties and due to
their great sensitivity to changes in the soil (Nichols et al. 2008; Korasaki et al.
2012; Filho and Baretta 2016).
The predominant use and management of the soil in Brazil involve a drastic
modification of the native forest by its fragmentation and conversion into agricul-
tural production systems and forest residues. Consequently, after intervention, the
functions of soil organisms and ecosystem services (as nutrient cycling, water qual-
ity, biodiversity maintenance, food production, among others) are affected.
An assessment of the functional and structural biodiversity of some of the soil
fauna groups, considering the impact of different management systems, is neces-
sary, in the interest of biodiversity preservation and ecosystem services provided by
organisms (Van Capelle et al. 2012). Considering the growing interest in under-
standing the ecosystem functions where springtails and beetles act, a major limita-
tion is the lack of taxonomists available. The differentiation of organisms using
specific traits can be useful, especially due to the lack of taxonomists able to iden-
tify the biodiversity, constituting an opportunity to minimize the taxonomic insuf-
ficiency of these taxa in Brazil.
Thus, an alternative approach is morphotyping, which analyzes morphological
traits and has been adapted for soil invertebrates (Oliveira Filho et al. 2016; Pey
et al. 2014; Pompeo et al. 2017; Santos et al. 2018). The objective is to group
­organisms of each species according to their degree of adaptation to the soil, clas-
sifying the eco-morphological groups according to their habitat (edaphic,
hemiedaphic, and epigeic) (Fig. 8.5) and morphotypes (life form) within each
group. Due to the difficulties imposed by the lack of knowledge, an approach using
functional characteristics has great possibilities of helping to understand both the
functional role in the ecosystems and the effects of habitat modifications on the
community structure (Fountain-Jones et al. 2015).
Thus, several studies have been carried out with this type of approach in Europe
involving different land-use systems and soil fauna groups (Gardi et al. 2008; Menta
et al. 2018a, b; Parisi 2001; Parisi et al. 2005). In Brazil, this approach has been used
to verify differences between forests and agricultural systems (Machado et al. 2019;
Pompeo et al. 2017; Santos et al. 2018).
164 M. R. G. Zagatto et al.

Fig. 8.5 Change of eco-morphological groups of springtails and beetles living inside the soil or
living on the soil surface (modified from Filho and Baretta (2016)). Colored bars indicate the exact
habitat (or depth of the soil) to which epigeic (green bar), hemiedaphic (dark brown), and edaphic
(light brown) specimens are best adapted. Although the specimens have a preferred depth that best
fits their needs, they may sometimes migrate vertically in the soil profile for some abiotic factors
(e.g., humidity and temperature) and biotic factors (e.g., lack of prey or other food)

According to Machado et al. (2019) and Santos et al. (2018), evaluating the
springtail communities by monitoring their morphological traits was efficient for
the comparison of the different land-use systems in two regions of Santa Catarina
state (Brazil), showing correlations between their communities and physical and
chemical soil properties. These two studies presented 16 edaphic morphotypes, 25
hemiedaphic, and 5 epigeic, totaling 46 morphotypes collected in the two regions.
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 165

In general, both studies showed that the eucalyptus plantation presented the low-
est values of abundance and richness of morphotypes when compared to areas of
native forest, pasture, integrated crop-livestock, and no-tillage systems. Higher
springtail abundance and richness were determined in the land-use systems without
anthropological actions and soil management due to better ecological equilibrium,
with increases of the food sources due to a higher diversity of plants. Thus, the low
quality of the litter and the exudates of the Eucalyptus rhizosphere can be an impor-
tant factor that limits the abundance and richness of morphotypes (Machado et al.
2019; Santos et al. 2018).
These studies show that soil attributes may explain the presence of several mor-
photypes in the areas (as determined by pH and potential acidity (H + Al), biopores,
bulk density, C/N, Ca/Mg and Mg/K ratio, metabolic quotient, micro- and macropo-
rosity, microbial biomass carbon, microbial basal respiration, organic matter, soil
moisture, total organic carbon, and total porosity). However, only on the plateau,
microporosity did explain the abundance of the morphotypes in eucalyptus planta-
tions. In this case, this correlation may account for the identified morphotypes being
mainly edaphic and hemiedaphic. This variable is important to explain the activity
and establishment of the various hemiedaphic and epigeic morphotypes at this site.
Pompeo et al. (2017), when carrying out a study with the soil coleopteran mor-
photypes in forest and agricultural land uses in the Santa Catarina Plateau, in areas
of Mixed Ombrophylous Forest (Atlantic Forest), evaluated the diversity of
Coleoptera and their relationships with the land-use systems and edaphic properties
in winter and summer. In this case, the native forest presented greater richness and
abundance of morphotypes, as well as greater diversity in summer, proving to be the
most stable among the studied land uses. This system was associated with a greater
amount of morphotypes, and the soil properties related to carbon dynamics contrib-
uted to explain this distribution.
The Eucalyptus stands (EST) presented lower diversity and abundance of cole-
opteran morphotypes than native forest (Fig. 8.6). Though presenting smaller values
than the other land-use systems, they did not differ significantly from pasture, crop-­
livestock integration, and no-tillage (Pompeo et al. 2017). Thus, the authors corre-
late the low density of beetles in EST to the lower plant diversity of these sites, since
Eucalyptus is an exotic species, usually grown in monoculture. Eucalyptus stands
also provide forest litter of lower quality than that of native forests, as already dis-
cussed above, therefore providing a less attractive environment for some beetles.

8.5  nchytraeids in Forest and Agricultural Sites:

E
The Dramatic Difference Between the Dataset
Among Tropical and Temperate Regions

Enchytraeids are close relatives of the earthworms but not as well known world-
wide. They live in all types of soils as long as they have a minimum of moisture,
organic matter, and oxygen (Schmelz et al. 2013). Their small body size, generally
166 M. R. G. Zagatto et al.

Fig. 8.6 Coleoptera density (individuals per m2) and abundance (individuals per trap) in native
forest (NF), Eucalyptus stands (EST), perennial pasture (PA), crop-livestock integration (CLI), and
no-tillage (NT) in winter (left) and summer (right) on the Southern Santa Catarina Plateau (Pompeo
et al. 2017). Mean values followed by the same letter are similar by the Kruskal-Wallis test
(p < 0.05; n = 135); ns: nonsignificant difference

not more than 4 cm, and their whitish semitransparent body make them not so evi-
dent to be seen in soil with the naked eyes. When in high abundance in crop soils it
is not rare that unsuspected farmers take enchytraeids as a pest, confounding them
with nematodes, leaving them highly concerned about the health of their crops.
However, their roles in soil are correlated with specific attributes of their larger rela-
tives (earthworms), contributing to the decomposition of organic matter, building up
of soil porosity and soil formation, mixing of organic matter, and regulation of
microbial activity (Didden 1993), though in a lower scale because of the small body
size, at least when in low abundance (Pelosi and Römbke 2016).
These small organisms play key roles in some particular natural ecosystems, such
as coniferous forests, peatlands, moorlands, and inselbergs whose soils are acidic,
rich in organic matter, and generally humid, either in the Northern or in the Southern
hemisphere (Vaçulik et al. 2004; Schmelz et al. 2013; Carrera and Briones 2013). In
these ecosystems, they may show extremely abundant populations reaching hun-
dreds of thousands of individuals per square meter. The few data available on enchy-
traeids in the tropics suggest that their abundance can be much lower (>10,000) than
in temperate regions (Römbke 2007; Schmelz et al. 2013). Conversely, some studies
showed enchytraeid abundance reaching 44,000 individuals per square meter in a
mixed Araucaria forest in Southern Brazil and a maximum average of 12,000, when
determined by wet extraction (Schmelz et al. 2013; Niva et al. 2015).
The high abundance of enchytraeids reported in temperate regions is often associated
to a community dominated by Cognettia sphagnetorum, a species, which proliferates
rapidly with asexual reproduction by fragmentation of the body and regeneration of the
8 Mesofauna and Macrofauna in Soil and Litter of Mixed Plantations 167

lost parts (Nurminen 1967; Huhta et al. 1986; Schlaghamerský 2013). These forests
with acidic soil very often present low occurrence of earthworms (Huhta 1984; Graefe
and Beylich 2003) and may harbor enchytraeid communities composed in a habitat with
more than 90% of Cognettia (Huhta 1984). The data available from South America so
far show that the community of enchytraeids is quite different from the ones in the
Northern hemisphere. For example, the genus Cognettia, which is common in European
countries, has never been sampled in Brazil, and many species of Guaranidrilus and
Hemienchytraeus are abundant in South America (Schmelz et al. 2013; Niva et al. 2015;
Pelosi and Römbke 2016) but almost not found in Europe (Schmelz and Collado 2010)
or North America (Schlaghamerský 2013). On the other hand, Enchytraeus, Fridericia,
Marionina, and Achaeta are present in both continents (Schlaghamerský 2013; Schmelz
et al. 2013; Niva et al. 2015; Pelosi and Römbke 2016). According to Pelosi and Römbke
(2016), some species of the first two genera may be cosmopolitan or peregrine, and
Fridericia seems to occur more in anthropogenic landscapes, such as pastures or crop-
lands, and less in forests. It was also reported that the density and the distribution of
enchytraeids do change with the different successional stages of the Atlantic Forest and
soil types (cambisoil vs. gleysoil) (Römbke et al. 2007). The genus Enchytraeus, for
example, was less frequent in primary forests than in less advanced stages of succession
or pasture, while Guaranidrilus was slightly more frequent in primary forests. Another
study, in the Araucaria mixed forest on cambisoil, shows that 34% of their population
consisted of Guaranidrilus, the dominant genus.
It seems that, in Brazil, enchytraeid abundance can reach numbers similar to those
found in temperate regions, however with a distinct species and genus composition
(Schmelz et al. 2013). Silva et al. (2006) found extremely contrasting densities of
enchytraeids when comparing an area with natural Cerrado to areas with conventional,
no-tilling, integrated crop-livestock, and pasture systems. In one of the sampling dates,
while in Cerrado there were more than 3000 enchytraeids per square meter; in the other
systems there were less than 10, using the TSBF method for sampling. However, in
general, the no-till, pasture, and crop-livestock systems favored enchytraeid popula-
tions reaching not more than 270 individuals per square meter. Assis (2015) found that
enchytraeid density and richness were higher in a native mixed Araucaria forest than in
conventional maize crop, while organic and conventional horticulture areas were some-
what in an intermediary position between the two. This author found Guaranidrilus
and Tupidrilus only in the forest, while Enchytraeus and Fridericia were the most
abundant ones in cultivated areas, either organic or conventional, confirming the
hypothesis that these genera are more common in anthropogenic areas, and he also
found a possible negative relation between phosphorus soil content and genus diversity.

8.6 Conclusions and Outlook

We believe that the soil fauna correlates with physical-chemical and microbiological
soil processes, since soil invertebrates continuously fragment the soil organic matter
and plant wastes, which facilitates many other processes in soil, such as microbial
168 M. R. G. Zagatto et al.

decomposition, nutrient cycling, and water-holding capacity; however the interaction

between mesofauna and microorganisms is strongly conditioned by soil moisture.
Eucalyptus plantations may exert some allelopathic effect in soil, once many research-
ers show an inhibition in the development of a diversified and abundant invertebrate
community. In this sense, more research is needed in order to find out effectively
which allelopathic substances are produced and what is the magnitude of this effect in
relation to the provision of soil ecosystem services. Mixed plantations of Eucalyptus
grandis and Acacia mangium share faunal groups which originate either exclusively
from pure plantations of Acacia mangium or from Eucalyptus grandis, improving the
soil quality, although the richness and diversity of such plantations differ from native
forests. Therefore, more diversified mixed plantations may be the key for a higher soil
fauna diversity and, consequently, for a better soil health, although perhaps these
diversified systems are generally adopted in restoration sites. For production sites and
silvicultural management however it may require greater adaptations.

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Chapter 9
Bioindicators of Soil Quality in Mixed
Plantations of Eucalyptus and Leguminous
Trees

Arthur Prudêncio de Araujo Pereira, Daniel Bini,

Emanuela Gama Rodrigues, Maiele Cintra Santana,
and Elke Jurandy Bran Nogueira Cardoso

9.1  oil Quality Indicators: Definitions, Applications

S
and Challenges

9.1.1 Definitions

Soil quality has an important role in both society and environment considering sev-
eral ecosystem services provisioned through soils (e.g., food, feed, fiber, climate
moderation through C cycling, waste disposal, water filtration and purification,
elemental cycling) (Lal 2015). Soil quality is commonly defined as the capacity of
a soil to function within ecosystem and land-use boundaries to sustain biological
productivity, maintain environmental quality, and promote plant and animal health
(Doran and Parkin 1994, 1996). This concept has been revised and it is proposed to
discuss soil use rather than soil functions. Therefore, soil quality assessment would

A. P. A. Pereira (*)
Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
Soil Science Department (Pici Campus), Federal University of Ceará,
Fortaleza, Ceará, Brazil
e-mail: arthur.prudencio@usp.br; arthur.prudencio@ufc.br
D. Bini
State University of the Central West, Guarapuava, PR, Brazil
E. G. Rodrigues
North Fluminense State University, Campos dos Goytacazes, RJ, Brazil
M. C. Santana · E. J. Bran Nogueira Cardoso
Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil

© Springer Nature Switzerland AG 2020 173

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_9
174 A. P. A. Pereira et al.

provide the scientific tools for evaluating the management of soil resources, also
considering the societal demands of the various benefits that soils can provide to
humankind if well managed. Therefore, the responsibility to maintain the quality of
the soil could be clearly assigned to the user of the soil (Bünemann et al. 2018).
Additionally, several authors have proposed a link between soil functions and
ecosystem services (ES) as the capacity of soils to deliver ES is determined largely
by the soil functions (Greiner et al. 2017; Adhikari and Hartemink 2016). This link
is a concept that has been considered a challenging yet promising approach for fos-
tering the communication of nature’s capital (Drobnik et al. 2018). According to Lal
(2015), the soil quality must be preserved or restored to guarantee these services and
also to enhance long-term productivity and improve the environment. Thus, this
author suggests that the strategy is to produce “more from less” by reducing losses
and increasing soil-, water-, and nutrient-use efficiency.
Measuring soil quality is an exercise in identifying inherent and dynamic soil
properties which are responsive to management, are capable of being precisely
measured within certain technical and economic constraints, and also are defined
with respect to the delivery of ecosystem services (Bünemann et al. 2018).
In order to achieve an improvement in productivity and sustainability of pure or
mixed Eucalyptus plantations, a different management is needed, based on a novel
approach to measure soil quality which demonstrates the interrelationship between
soil biota diversity and activity, improvements in nutrient cycling and consequently
soil fertility, increase in the organic matter quality, and increase in wood productiv-
ity. All these aspects are necessary as a guide in the search for sustainable practices
(Pereira et al. 2018a; Bini et al. 2013a; Gama-Rodrigues et al. 2008).
The role of soil biota for the functioning, integrity, and long-term sustainability
of natural and managed terrestrial ecosystems is slowly increasing towards an ade-
quate recognition, since these organisms are essential components of litter decom-
position, nutrient cycling, soil aggregation, and growth of plant communities
(Bender et al. 2016; Lal 2015). Soil microbial biomass is a labile fraction of the soil
organic matter (SOM) and plays a crucial role in the maintenance of soil fertility
and availability of plant nutrients (Jenkinson 1981). The microbial biomass is a
sensitive indicator of organic matter dynamics because the microbial fraction
changes comparatively fast and differences are detectable before they occur in total
organic matter (Cardoso et al. 2013; Gama-Rodrigues and Gama-Rodrigues 1999).
Although microbial biomass only constitutes an average of 2–5% of the soil organic
C and 1–5% of the total soil N, it is the most important component of SOM, control-
ling the nature and rate of organic matter transformations (Jenkinson 1981; Smith
et al. 1990). Moreover, it plays a critical role in soil C cycling and accounts for
roughly half of the soil surface CO2 efflux through heterotrophic soil respiration
(Hanson et al. 2000; Högberg et al. 2001).
The litter-soil system comprises the habitat for the majority of species living on
the planet, while the horizontal and vertical heterogeneity of both soil and litter can
boost spatial variability in the distribution and activity of this biota (Coleman and
Whitman 2005). The relationship between environmental attributes and biota of the
litter-soil system becomes extremely important because any change in the soil or
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 175

litter attributes affects the biota, and consequently the development of the plant
community (Bini et al. 2013b; Zaia et al. 2012; Zagatto et al. 2019).

9.1.2 Applications

In this study, we are going to show some soil quality assessments with a focus on
the provision of ecosystem services in the litter-soil system of pure and/or mixed
Eucalyptus plantations.
Studying the interrelationships between microbial and soil chemical attributes
Pereira et al. (2018a) were able to explore the microbial influence on C and N
cycling and how it can discriminate between intercropped and pure Eucalyptus
plantations. The study showed high efficiency of the microbial biomass in incorpo-
rating C and N, and improved organic matter (OM) cycling in mixed systems with
Acacia mangium. It also showed the potential of longer maintenance of Acacia resi-
dues in the labile fraction of soil OM when compared to Eucalyptus treatments.
Thus, the study concluded that mixed plantations promote a more efficient use of C
and N by microbial communities, thereby increasing the plant nutrient availability
in soils with low levels of OM. The same authors undertook an investigation to
evaluate interactions between the bacterial community and biological functions
involved in C and N cycles in the soil and litter layers resulting from pure or mixed
Eucalyptus grandis and Acacia mangium plantations. This study showed a signifi-
cant increase of bacterial community diversity and functional gene abundance,
which improved C and N cycling in the soil and in the litter interface of a pure
Acacia plantation, as well as in the intercropped plantation. Thus, the authors con-
cluded that mixed plantations are a better alternative than using mineral N fertilizers
for long-term soil health, as mineral N can reduce the abundance of functional
genes, bacterial diversity, and microbial activities (Pereira et al. 2019).
The interrelationship between soil C, N, and P; litter C, N, P, lignin content, and
polyphenol content; and microbial biomass and activity was examined by Bini et al.
(2013a) in pure and mixed plantations of Eucalyptus grandis and Acacia mangium
before and after senescent leaf drop. This study showed a stronger relationship
between litter contents and microbiological soil attributes, as well as the important
role played by the maintenance and quality of litter in regulating microbial biomass
and activity in soils. The authors concluded that the synergism between the two tree
species in the intercropped plantation established a new equilibrium in the soil
microbiota after 20 months, maintaining and stimulating biogeochemical cycling as
requirement for the sustainability of the intercropped plantations.
Changes in forest litter and soil where the native forest was replaced by eucalyp-
tus plantations in four southeastern areas of Brazil were studied by Gama-Rodrigues
et al. (2008). The authors observed that the interrelationship between litter and soil
microbial attributes was sensitive to show the dissimilarity between eucalyptus sites
and native forest. The study of these interactions also enabled observing that the
impact of native forest conversion into eucalyptus stands varied in accordance with
the site-specific characteristics that had been analyzed.
176 A. P. A. Pereira et al.

Another study related to the interaction between microbial and chemical soil
attributes showed that the soil organic C and total N stock were more relevant to
explain the dissimilarity between eucalyptus stands of different ages than the soil
microbial attributes. On the other hand, both the microbial litter attributes and cel-
lulose, lignin, and N content of litter were relevant to show the differences between
those eucalyptus stands. Thus, the litter quality had a direct influence on litter
microbial activity and microbial biomass C and N, which suggests a close relation-
ship between C and N immobilization or mineralization and litter quality
(Barreto 2008).
Zagatto et al. (2019) evaluated the density and diversity of soil mesofauna and its
interaction with microbiological and chemical soil attributes in pure Acacia man-
gium (AC), Eucalyptus grandis (EU), and mixed E. grandis and A. mangium planta-
tions (M). The authors found that the higher soil quality in pure Acacia plantations
and in mixed plantations was due to the interaction between microbial activity and
structure of the soil mesofauna community, which contributed to the increase in soil
nutrients.
The interrelationship between arbuscular mycorrhizal fungi (AMF) root coloni-
zation, enzymatic activity, and soil and litter C, N, and P in both pure and mixed
plantations of Acacia and Eucalyptus was evaluated by Bini et al. (2018). The
results showed that the intercropped plantation increased the AMF colonization
and the activity of acid and alkaline phosphatase. They also found negative correla-
tions between root colonization and litter C/N and C/P ratios, and a positive cor-
relation with soil acid phosphatase activity and soil N and P concentrations.
Altogether, this means that intercropped systems with higher root colonization
rates generate litter of better quality improving P cycling and P nutrition in soil
and, therefore, the health and productivity of these forests. A study was carried out
with the purpose to evaluate interactions between the structure and richness of soil
bacteria, fungi, and archaea; the functional groups of nitrifying, denitrifying, and
nitrogen-fixing bacteria; and their relationship with soil chemical changes in pure
and mixed Eucalyptus and Acacia plantations. The results showed a distinct micro-
bial community in mixed plantations with positive effects on soil phosphorus and
nitrate content, which potentially reduces the demand for mineral fertilization
(Rachid et al. 2013).
Additionally, Santos et al. (2018) studied the interaction between litter produc-
tion, decomposition, and soil microbial activity in a pure and intercropped
Eucalyptus and Acacia plantation. In this study, the more diverse litter composition
in the mixed plantation provided a more balanced N and P supply, which in turn was
able to sustain high microbial activity levels with positive consequences on litter
decomposition and boosting nutrient cycling efficiency, being a sustainable option
to offset the high nitrogen export from successive monoculture-based silvicultural
systems.
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 177

9.1.3 Challenges

Seeking high productivity has made forest production a simplistic practice, with
high fertilizer and pesticide applications producing detrimental environmental
impacts. Nowadays, public concern in environmental issues is growing. This
imposes the following question: How is it possible to achieve high ecological pro-
ductivity by optimizing ecosystem services in low-input forest systems?
The interrelationship between soil and litter attributes (biological, microbial,
chemical, and physical) has hitherto provided the fundamental context on how to
improve ecosystem services. However, a mechanistic understanding of these rela-
tionships and to decide whether they are in relation to the soil as an ecosystem in
itself or as part of a larger ecosystem in nature are undeniably complex and remain
elusive.
A challenge in soil ecology is to develop multivariate hypotheses to describe not
only interrelations between litter and soil attributes or between litter and soil fauna,
but also the direct and indirect relations between attributes and fauna in the litter-­
soil system. There is a complex interconnection between the edaphic environment
and productivity (Oliveira et al. 2018; Eisenhauer et al. 2015) (Fig. 9.1). This is a

Fig. 9.1 Hypothetical model of interactions and processes mediated by soil biota for sustainable
forest production
178 A. P. A. Pereira et al.

very important consideration. It even would justify a scientific study conducted by

a multidisciplinary team to elucidate this intricate chain of interactions and the eco-
logical interdependencies between land use, biodiversity, and ecosystem services,
which will enable an increase in the productive capacity of soils. It could be the start
of a basis of technological modifications for sustainable production, both economi-
cally and environmentally.
Thus, forest production would bring net benefits from ecosystem services, which
are a source of revenue for producers who are attentive to sustainable business, and
would guarantee the demands of future generations. It would increase competitive
advantages, and finally it would remove trade barriers imposed because of environ-
mental reasons.

9.2  iological Properties in Forest Ecosystems: Why Are

B
They Important for Eucalyptus Plantation?

9.2.1 Forest Habitats: A Brief Description

Natural forests are considered a specific ecosystem, representing high wood pro-
duction and comprising huge habitats that support the microbiome life, which is
dynamic and quickly responds to anthropogenic and environmental changes
(Baldrian 2017). Moreover, reactions to the microbiome metabolism can occur in
the most diverse plant organs and locations, such as leaves, flowers, seeds, fruit,
wood, inside (endophytic) or on the tree surface (phyllosphere), as well as below-
ground (soil, roots, rhizosphere, and mycorrhizosphere) (Baldrian 2017). Even
more important, habitats differ in properties such as nutrient availability, major
environmental conditions, processes, and dynamics, which together can alter the
microbiome dynamics. The forest microbiome research has been highly focused on
soil habitats, emphasizing tree roots and their symbionts, while litter and other habi-
tats have been greatly underexplored, mainly in pure and mixed plantations (Pereira
et al. 2018a, b).
The forest environment has specific properties that differentiate it from other
(e.g., agricultural systems and implanted forest) (Navarrete et al. 2015). One of the
most important features is the huge effect of the dominant trees on the surrounding
habitat, which can regulate aboveground and belowground interactions (Wardle
et al. 2004). The trees interact with microbial activities and composition, and this is
mediated by bulk soil and litter chemistry (Augusto et al. 2015; Šnajdr et al. 2013;
Urbanová et al. 2015). Here, we include organic matter contents, soil pH, nitrogen
transformations, and other macro- and micronutrients (Fierer and Jackson 2006;
Lauber et al. 2008; Prescott and Grayston 2013; Rousk et al. 2010; Tedersoo et al.
2016; Urbanová et al. 2015). These effects seem to be extremely dependent on for-
est management (Tedersoo et al. 2016), and all drivers are combined by stochastic
effects on microbiome assembly (Bahram et al. 2016), which can contribute to the
dynamics of microbiomes in different forest habitats (Štursová et al. 2016).
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 179

9.3 Native and Planted Forest Environments

Planted forests are subject to multiple modes of disturbance, such as insect attacks,
fires, and nutritional imbalances in soil, among others. In addition, this system is
also significantly changed by many anthropogenic factors, as climate change or
environmental pollution, water deficit, and management practices, which together
may easily shift the balance of carbon and nitrogen cycling processes (Trumbore
et al. 2015).
Soils under native forest have characteristics that differentiate them in numerous
aspects from the planted forestry and agricultural soils (Fig. 9.2). For example,
around 50% of the C fixed by trees is allocated in the soil through their root activity
(Högberg et al. 2001), while the litter layers are important organic matter sources
for the system, governing important stages of ecosystem services and nutrient
cycling (Baldrian 2017). Besides the C contents, one of the most notorious effects
of tree influence is the low pH of the soil solution, potentiated by the release of
organic acids through root system exudation (Motavalli et al. 1995). In addition,
there is a large root extrusion of enzymes that degrade organic matter which makes
biogeochemical cycling very active in this environment, with increases in C and N
contents above- and belowground (Fig. 9.2, Chap. 2).
Natural forests can provide several ecosystem services that are fundamental for
the maintenance of the surrounding environment, mainly in soil protection (Lal
2014), biogeochemical cycling of nutrients (Laclau et al. 2010), maintenance of
microbial biodiversity, meso- and macrofauna (Cardoso et al. 2013), and organic

Fig. 9.2 Major differences between a natural forest and an implanted forest ecosystem. Arrows
pointing upwards in (a) indicate better soil health than in (b), arrows pointing down, where the
opposite is true
180 A. P. A. Pereira et al.

matter quality (Pereira et al. 2018a) among others (Fig. 9.2a). The preservation of
natural forests and its functioning is becoming an evermore important subject, even
for the common citizen. For example, in natural forests prevails a phenomenon that
has been gently called the “Wood Wide Web,” or either “The Forest Internet,”
responsible for permitting the existence of forests on our whole planet, a system that
biologically interconnects all the trees in a forest, resulting from interactions of
fungi, bacteria, and plants (including also some other macro- or microorganisms).
Fungi and bacteria furnish nitrogen and phosphorus to the plants and receive in
exchange carbon sources, moisture, and protection.
This is the result of millions of years of joint evolution, a real biological network
which guarantees protection to all participating entities, which has been studied for
over 30 years, starting even before there was a consolidation of the human Internet.
Steidinger et al. (2019) showed the first map of these interconnections, demonstrat-
ing that, without this system, extensive forests would probably not exist. In tropical
regions, where the predominating soils are generally very poor and acidic, with
deficiencies in phosphorus and organic matter, such associations are even more fun-
damental for forest survival. This paper (about the “Wood Wide Web”) includes
about 200 scientists worldwide, among which seven Brazilian universities, with all
earlier findings about the Wood Wide Web and its eventual risk of extinction due to
deforestation and global warming (Steidinger et al. 2019). In planted pure forests,
however, this web does not exist, while forest consortia composed of two, or even
better multiple, tree species are prone to develop such a system, therefore being
much more sustainable.
On the other hand, the conditions that occur in the planted forest ecosystems,
such as in Eucalyptus plantations, differ strongly from their natural state, mainly in
terms of diversity and functionality in the soil-plant-(micro)-biota interface
(Fig. 9.2b).
In planted forests (monocultures) we find deposition of a unique litter type,
which may present low nutrient availability (high C/N ratio) (Mercês et al. 2016;
Snowdon et al. 2005). Moreover, when compared to natural systems, the depletion
of mineralizable nutrients may occur over time (mainly due to wood exportation),
and the type and quality of exudates secreted by the roots are extremely selective
(Churchland and Grayston 2014) (Fig. 9.2b). Thus, forest plantations may differ in
some soil properties and determine different soil temperatures, aeration gradients,
porosity percentages, and soil water storage capacities (Baldrian 2017). This behav-
ior can promote more homogenous conditions for microbial communities, making
them less diverse and less efficient in the use of available resources, leading to nega-
tive plant-soil feedbacks (PSF) (Mariotte et al. 2017), or “soil fatigue” (Huang et al.
2013). In this sense, little emphasis was placed on studies to minimize PSF using
intercropping systems to improve biological functions in different forest niches
(Wang et al. 2017).
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 181

9.4  he Mixed or Consortiated Forest System with N2-Fixing

T
Trees: Brief Importance of Biological Functions for Soil,
Plant Health, and Nutrient Cycling

There are around 3 trillion trees on planet Earth (Crowther et al. 2015), which are
responsible for covering a large part of the soil surface covered by vegetation. This
large volume of biomass is extremely important, especially in the regulation of the
world’s climate, and the health of soil and bodies of water (Kirilenko and Sedjo
2007). However, trees are closely dependent on the microbiome to survive, which
provides nutrients essential for their development, such as N, P, and K (primary
macronutrients), through organic matter cycling in the soil (Baldrian 2017). For
example, it is estimated that N2-fixing bacteria and mycorrhizal fungi are responsi-
ble for providing up to 75% of the nitrogen and 80% of the phosphorus that forests
use during their life cycle (Van Der Heijden et al. 2008). In addition, all organic
matter transformation steps depend on the activity of microorganisms (Singh 2018).
Acacia trees form symbiotic relationships with N2-fixing bacteria (Chap. 6) and
provide a key reservoir of N, C, and P for the surrounding ecosystem (Bini et al.
2013a; Paula et al. 2018; Pereira et al. 2018a; Taylor et al. 2017). In this sense, it is
possible to integrate trees of high economic value (Eucalyptus) and trees of high
ecological value (Acacia) in an intercropped system (Laclau et al. 2008; Pereira
et al. 2017; Rachid et al. 2015) (Fig. 9.3) and improve the ecosystem services pro-
moted by the plant-soil microbiome.
Recent studies have shown the N2-fixing potential around 90–120 kg ha−1 year−1,
as well as the direct transfer of N of the roots of A. mangium to the E. grandis roots
(Bouillet et al. 2008; Paula et al. 2015, 2018). In this sense, Eucalyptus plants would
provide financial benefits and those of A. mangium, immeasurable ecological gains
(Fig. 9.2). In this case, the availability of N can occur for Eucalyptus also after
senescence of Acacia plant tissues (litter, fine roots, and nodules), root exudation, as
well as cell death of organisms of the soil microbiota, providing N through mineral-
ization processes (May and Attiwill 2003; He et al. 2003; Chalk et al. 2014).
However, in spite of the diverse benefits of this association, studies evaluating the
interactions at the soil-plant-microbiome interface in this type of forest manage-
ment remain poorly understood.
The increase of N in the soil promoted by A. mangium sometimes is able to pro-
mote a significant increase in E. grandis productivity, even in the absence of the
application of mineral fertilizers (Laclau et al. 2008), although this is very depen-
dent on the climatic and edaphic conditions. In a review published by Forrester et al.
(2006), a meta-analysis of 18 studies showed that several trials with mixed cultures
were significantly more productive than monocultures, with fewer cases showing
the opposite. For example, 11 years after the implantation of a mixed E. globulus
and A. mearnsii plantation, mixed stands between species were more productive
than monocultures in terms of aerial biomass, volume of wood produced, and C
allocation in soil, with higher N and P cycling rates in litter (Forrester et al. 2004).
182 A. P. A. Pereira et al.

Fig. 9.3 Intercropped Eucalyptus and Acacia plantations. Upward arrows mean that soil health is
better than in pure plantations, and the opposite is true for downward arrows. Belowground net-
works representing the mycorrhizal associations (endo- and ectomycorrhiza, and dark septate
endophytes) and interactions between the two plants

9.5  oil Microorganism Processes and Nutrient Cycling

S
in Forest Plantations

Natural or planted forest sustainability shows a great dependence on geochemical,

biochemical, and biogeochemical cycling. By definition, geochemical cycling is
characterized by the inputs and outputs of mineral elements between the ecosystem
and the environment. Biochemical cycling refers to the translocation of nutrients
inside the plant, such as the process of nutrient translocation. Finally, biogeochemi-
cal cycling involves the processes of nutrient transfer between the soil and plant
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 183

systems, with nutrient uptake by plants until their return to the soil via mineraliza-
tion and decomposition processes or root exudation (Switzer and Nelson 1972).
Thus, nutrient cycling is related with abiotic and biotic factors to maintain the eco-
system equilibrium. In general, nutrient inputs in ecosystems come from the air,
rainfall, weathering process, biological N fixation (BNF), organic matter mineral-
ization or decomposition, and throughfall. On the other hand, outputs are repre-
sented by erosion, runoff, volatilization, leaching, and nutrient removal during the
forest harvest (Lavelle et al. 2005).
Commercial forests, as eucalyptus, are established commonly in poor soils and
depend on nutrient cycling for their main sustainability. Appropriate management
can promote the nutrient cycling, with ecological and economic benefits (Forrester
et al. 2005b; Laclau et al. 2008). Thus, the ecological intensification promoted by
mixed plantations favors processes of nutrient cycling and increases plant biomass
and environmental sustainability (Forrester et al. 2005a). Leguminous trees inter-
cropped with a nonleguminous tree (e.g., Eucalyptus) confer advantages to impor-
tant microbial processes related to biogeochemical and geochemical cycling of C
and nutrients, mainly N and P (Forrester et al. 2005b; Bini et al. 2013a, 2018;
Baldrian 2017; Pereira et al. 2018b). In mixed plantations the microorganisms are
the protagonists in nutrient cycling, based on three processes: BNF, mycorrhizal
colonization, and decomposition or mineralization of organic matter (Ward and
Jensen 2014; Bini et al. 2013a; Liang et al. 2017; Pereira et al. 2019).
Nitrogen-fixing bacteria present in leguminous trees promote BNF. These bacte-
ria are of great value to promote N cycling in mixed plantations with nonlegume
tree species. The fixed atmospheric N is first immobilized within the leguminous
trees, and afterwards it is translocated and only then it becomes available for other
trees (Parrotta et al. 1996; Khanna 1997; Forrester et al. 2006). The fixed nitrogen
can be shared with nonlegume trees (a) via root exudation of the legume species; (b)
by transfer of N through hyphal networks of mycorrhizal fungi that connect legumi-
nous and nonleguminous plants; and (c) through the decomposition and mineraliza-
tion of plant tissues of the legume species (Frey and Schüpp 1993; He et al. 2003;
Forrester et al. 2006). This process is related to increases in N cycling in mixed
stands. There is a high potential of BNF in mixed plantations, with approximately
20 g N m−2 year−2, where more than 90% of N is derived from this process (Binkley
1992; Nygren et al. 2012). In mixed plantations of A. mangium and E. urophylla ×
grandis, Tchichelle et al. (2017b) found an amount of biologically fixed N four
times higher than the total amount of commercial nitrogen fertilizer application at
the beginning of the rotation. According to this author, 16% of the N present in the
eucalyptus comes from the BNF promoted by Acacia. Moreover, N cycling tends to
increase because there is a stimulation of the incorporation of N derived from the
soil into the trees.
N and P cycling seems to be favored in mixed plantations. Of great biological
importance, the available P needs special attention in tropical soils. In these soils
there is inorganic P fixation onto iron or aluminum oxides (Hinsinger 2001), which
makes planting of leguminous trees critical, since they demand great amounts of P
to sustain BNF processes (Hinsinger 2001; Inagaki et al. 2011). This is the reason
184 A. P. A. Pereira et al.

why legumes require more P than nonleguminous plants, such as eucalyptus

(Binkley 1992; Koutika et al. 2016). A strategy for P acquisition in poor soils for
legumes and eucalyptus is their great capacity of association with arbuscular mycor-
rhizal fungi (AMF) and ectomycorrhizae (Pagano and Scotti 2008; Mendes-Filho
et al. 2009; Jimu et al. 2017; Bini et al. 2018). In general, these fungi can access P
sources and other nutrients in soil through their hyphal network, even when the P
ions are located further away from the plant roots, which cannot get access to them
(He et al. 2003). In this sense, P cycling in mixed plantations seems to be dominated
by the high mycorrhizal capacity of the leguminous species involved, which posi-
tively influences a higher colonization in the eucalyptus tree (Khanna 1997;
Aggangan et al. 2010; Bini et al. 2018).
Pereira et al. (2018a) found colonization of eucalyptus roots by AMF at 0–50 cm
depth, a fact stimulated by the presence of A. mangium. According to Bini et al.
(2018), two strategies are important for P cycling in mixed plantations: mycorrhiza-
tion by AMF and high activities of the phosphatase enzymes. E. grandis when inter-
cropped with A. mangium has higher activity of acid and alkaline phosphatases than
in pure plantations. However, P cycling is probably extremely fast, since it was not
possible to detect significant differences between the P available in the soil in pure
and mixed plantations, although there was a higher concentration of P in the trees
(Bini et al. 2018). Thus, it is possible that other soil microorganisms also are active
in improving fast P cycling. In addition, nutrient cycling is maximized by fungal
networks that connect one plant to another, transferring nutrients between them
without passing through the soil, a phenomenon that can occur between different
plant species (Simard et al. 2003; Bini et al. 2018).
Among the three processes mentioned above, the process of decomposition and
mineralization of organic matter is probably the main pathway for nutrient cycling
in ecosystems and the most responsible for forest sustainability (Rahman et al.
2013). Soil organic matter results, largely, from the decomposition of animal and
plant residues deposited on and under the soil. It is the main source of C, nutrients,
and energy for soil microorganisms and plants (Brady and Weil 2009).
In tropical and subtropical soils, this is more evident, since it has a relationship
with physical, chemical, and biological attributes of the soil, which makes the main-
tenance and management of organic matter fundamental for the productive capacity
of forest soils in the long term (Switzer and Nelson 1972). Soil organic matter is
produced during the fixation of C by photosynthesis, which generates organic com-
pounds that can be comminuted by root exudates or deposits of fragments of senes-
cent plants on the soil, called litter (Brady and Weil 2009; Rahman et al. 2013). For
this reason, it is fundamental to create adequate edaphic conditions by stimulating
biological processes as the degradation and mineralization of organic matter. Litter
is first fragmented by soil mesofauna and, subsequently, by heterotrophic fungi and
bacteria, which contribute to the formation of soil organic matter or humus, repre-
sented by stable or labile fractions, such as microbial biomass (Lavelle et al. 2006;
Rahman et al. 2013).
Microbial biomass is the living part of the organic matter of the soil, being a
source and sink of nutrients and, therefore, considered the organic matter that
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 185

p­ resents a fast cycling (Kaschuk et al. 2010). Bini et al. (2013a), in pure and mixed
plantations of A. mangium and E. grandis, detected that the microbial biomass
served as a sink of C and nutrients until 14 months of planting and after 20 months
became the source of these elements. Litter microbial biomass can represent an
important pool of C and nutrients, because it shows a greater capacity to be a nutri-
ent sink than the microbial biomass of the soil (Gama-Rodrigues et al. 2011; Bini
et al. 2013b).
Bini et al. (2013b) showed that the litter microbial biomass drained approxi-
mately 94% more N than the soil microbial biomass in pure and mixed plantations
of A. mangium and E. grandis. Litter enters the decomposition and mineralization
process by the action of several microorganisms by means of exuding many specific
enzymes (phosphatases, cellulases, ligninases, ureases, etc.). Thus, part of the C is
recycled into the atmosphere as CO2, while N can be mineralized as NH4+ and then
converted to NO3−, while other elements such as P and S and several micronutrients
can be transformed into mineral forms that are absorbed by plants. Only a small
portion of this C is stabilized in the form of humus, which is still a source of C and
nutrients, but whose mineralization rate is lower (Rahman et al. 2013).
It is important to highlight the fact that litter is the main source of soil organic
matter, being a major component of the biogeochemical cycling process of nutrients
in forest ecosystems (Rahman et al. 2013). Monocultures produce nondiversified
litter, originated by only one type of plant residue. In contrast, mixed plantations
produce more heterogeneous organic material (Binkley et al. 1992; Richards et al.
2010) with higher quality especially in mixes with legumes. Litter is the main vehi-
cle to transfer C, N, P, and Ca from the trees to the soil; other elements as K are
returned mainly through throughfall, and for Mg, it is variable for different forests
(Cole and Rapp 1980; Bini et al. 2013b; Santos et al. 2017). However, there are
variations in the rate of decomposition and mineralization of organic wastes. High
levels of lignin, polyphenols, cellulose, and high C/N and C/P ratios characterize the
recalcitrant residues, which make it difficult to recycle nutrients (Bini et al. 2013b;
Rahman et al. 2013). Furthermore, the quantity and quality of the litter also depend
mainly on the tree species and the soil attributes which govern nutrient availability.
In general, after closing of the canopy, eucalyptus produces a litter that is rela-
tively poor in nutrients, due to high C/N and C/P ratios, with high percentages of
cellulose (Gama-Rodrigues and Barros 2002; Paul et al. 2004; Bini et al. 2013b;
Pereira et al. 2018b), contributing little to the replacement of soil nutrients. On the
other hand, leguminous trees provide greater incorporation of organic matter and
nutrients to the soil, due to their higher leaf quality and lower C/N and C/P ratios,
favoring decomposition processes (Forrester et al. 2006; Richards et al. 2010; Bini
et al. 2013a; Pereira et al. 2018a). However, although N-fixing legumes favor the
increase of N, it is important to understand that the higher N and P contents do not
always result in faster degradation of A. mangium residues, in comparison with
E. grandis (Bini et al. 2013b). High lignin concentrations in the litter can reduce the
decomposition rate of legumes (Wedderburn and Carter 1999; Prescott 2010; Bini
et al. 2013b; Rahman et al. 2013).
186 A. P. A. Pereira et al.

According to Bini et al. (2013a) and Bachega et al. (2016), litter decomposition
of A. mangium was slower than that of E. grandis, even though containing higher N
and P concentrations. In mixed plantations, however, there are improvements in lit-
ter quality, since the lignin concentration of the mixture decreases (Bini et al. 2013b;
Santos et al. 2017). Santos et al. (2017) reported that the deposition of N and K via
litter was higher in stands of mixed species of Acacia and Eucalyptus than in
Eucalyptus monocultures. In addition, P, Ca, and Mg depositions were even higher
in mixed plantations than in Acacia monoculture. Tchichelle et al. (2017) found that
soil N mineralization was higher in Acacia monocultures and mixed plantations,
being 82% and 52% higher, respectively, than in E. grandis monoculture. These
results suggest faster nutrient cycling in the mixture due to microbial decomposition
processes (Pereira et al. 2019). Similar data were reported when higher N and P
contents were observed in litter at mixed plantation (Li et al. 2001; Forrester et al.
2005b; Voigtlaender et al. 2012 Bini et al. 2013a, and other authors). With the
increase of plant age the process of N translocation in leaves decreases and soil N
contents increase (Richards et al. 2010; Santos et al. 2017).
In mixed stands mycorrhizae and BNF are important microbial processes for N
and P inputs. The absorption of nutrients via roots or mycorrhizae increases plant
biomass, and such nutrients are translocated and later reabsorbed from senescent
tissues. Finally, after dropping back to the soil the plant residues are equivalent to
litter deposition; this is when the initial decomposition and mineralization process
is renewed, providing nutrients in the inorganic form to replenish the soil and to be
reabsorbed by the plant. Thus, sustainability and nutrient cycling depend on micro-
bial action. Microorganisms are involved in geochemical cycling and biogeochem-
istry, being the actors of decomposition and mineralization of organic matter, while
BNF and mycorrhization complement nutrient cycling. Furthermore, in mixed plan-
tations (and perhaps in most forestry environments) litter represents the main com-
partment to generate new mineral nutrients for plants. In any plan for forest
implementation, this must be considered seriously since long-term nutrient losses
can be economically and environmentally unfavorable or even calamitous for
silviculture.

9.6 Final Remarks and Future Perspectives

Research-related bioindicators of soil quality with pure and mixed forests are only
just a beginning. The achievement of sustainable Eucalyptus forest systems that
meet the wood production demands and maintain an intimate relationship with bio-
diversity is an important challenge of the twenty-first century. Although our ability
to describe major bioindicators in this type of forest remains incomplete, we have
already created an integrated view of very important processes mediated by micro-
organisms and their diversity, mainly on nutrient cycling. We know very little about
how to exploit the multifunctionality and multicomplexity of natural ecosystems
and apply them to increase soil health, yield, and sustainability of forest e­ cosystems.
9 Bioindicators of Soil Quality in Mixed Plantations of Eucalyptus… 187

Understanding the dynamics of the bioindicator function is a complex but very

important challenge because this relationship is one of intense mutual cooperation.
There is a clear need for intensive studies in the setting up of experimental trials that
consider multiple regions and to make relationships between them, even if these
studies are initially descriptive. Focusing on the Eucalyptus and Acacia bioindica-
tors of soil quality at the geographic scale will undoubtedly represent an important
and valuable future field of work in the sustainability of these forest plantations. We
must know the bioindicator ecology and applications, so we can make appropriate
predictions of how forest ecosystems will respond to management changes, envi-
ronmental changes, and climatic events in the coming decades.

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Chapter 10
Ecosystem Services in Eucalyptus Planted
Forests and Mixed and Multifunctional
Planted Forests

Fabiano de Carvalho Balieiro, Luiz Fernando Duarte de Moraes,

Rachel Bardy Prado, Ciro José Ribeiro de Moura, Felipe Martini Santos,
and Arthur Prudêncio de Araujo Pereira

10.1 A Brief State of the Art of Native and Planted Forests

Forests act as a source of food, fuel, and medicine for more than a billion people
around the world (FAO 2018). In addition forests hold more than three-quarters of
the world’s terrestrial biodiversity, provide many products and services that contrib-
ute to the socioeconomic development, and are particularly important for hundreds
of millions of people in rural areas (FAO 2018). According to this report (Global
Forest Resource Assessment, FRA) the world’s forest area decreased from 31.6 to
30.6% between 1990 and 2015, but at a slower pace in recent years (FAO 2018).
On the other hand, planted forests have their area increased year after year, albeit at
a slower pace in recent years. The average annual rate of increase between 1990 and
2000 was 3.6 million ha. The rate peaked at 5.9 million ha per year for the period
2000–2005 and slowed to 3.3 million ha per year between 2010 and 2015
(FAO 2018).

F. de Carvalho Balieiro (*) · R. B. Prado

EMBRAPA Soils, Brazilian Agricultural Research Corporation, Rio de Janeiro, RJ, Brazil
e-mail: fabiano.balieiro@embrapa.br
L. F. D. de Moraes
EMBRAPA Agrobiology, Brazilian Agricultural Research Corporation, Seropédica, RJ, Brazil
C. J. R. de Moura
Federal University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
F. M. Santos
Federal Rural University of Rio de Janeiro, Seropédica, RJ, Brazil
A. P. de. Araujo Pereira
Department of Soil Science, University of São Paulo, “Luiz de Queiroz”
College of Agriculture, Piracicaba, SP, Brazil
Soil Science Department (Pici Campus), Federal University of Ceará, Fortaleza, Ceará, Brazil

© Springer Nature Switzerland AG 2020 193

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_10
194 F. de Carvalho Balieiro et al.

Land-use change leads to the destruction and fragmentation of forests, with neg-
ative impacts on the biogeochemical cycles of nutrients, increasing the risk of inva-
sion of species and bringing significant losses of biodiversity (Myers et al. 2000;
Rodrigues et al. 2009; Brockerhoff et al. 2013; Newbold et al. 2015). The interfer-
ence of human activities that influence climate also pressures these natural ecosys-
tems (Sala et al. 2000; Bonan 2008; Ballester et al. 2010; FAO 2018). A study by
Mcneill and Mcneill (2003) observed that the loss of average abundance of the
planet’s original biodiversity was around 73% in 2002 and that this should reach a
level of 84% by 2050. For Newbold et al. (2015), the loss of local species richness
above 20% could substantially undermine the contribution of biodiversity to eco-
system function and services and, consequently, human well-being.
In Brazil, native forests are among the most biodiverse and threatened ecosystems
on the planet (Myers et al. 2000). As part of the group of 24 biomes with an excep-
tional concentration of endemic species and with alarming habitat loss, the Atlantic
Rainforest and Cerrado biomes, for example, were placed on the list of global
hotspots. According to the authors, in only 1.4% of the terrestrial surface, these 24
biomes harbor more than 44% of all vascular plant species and 35% of all vertebrate
species (mammals, birds, amphibians, and reptiles). Data from Ribeiro et al. (2009)
indicate that the Atlantic Rainforest has only 11.4–16% of its original coverage. The
Amazon, despite its huge area, has had its deforestation monitored by the National
Institute for Space Research (INPE) since 1988. According to the records presented
by the National Forestry Information System (2017), for the period 2016–2017, the
increase in the deforested area was equal to 662,400 ha, contrary to the trend of
decreasing deforestation in previous years (2002–2011). In 2016, land-use changes
accounted for 51% of Brazilian total greenhouse gas emissions, equivalent to 1.17
billion Mg (=106 g) CO2 equivalent (CO2e) (Brandão Jr et al. 2018). Deforestation
was the main source of emissions in relation to land-use changes, with the Amazon
biome contributing 602 million Mg CO2e (52%) of the sector’s emissions in 2016,
Cerrado 21% (~248 million Mg CO2e), and the Atlantic Rainforest also 21%.
Despite the continuous degradation of native forest ecosystems, forest cover has
increased in several countries as the result of regeneration in abandoned agricultural
areas and forest plantations for commercial or restoration purposes (Chazdon et al.
2016). However, as pointed out by the author, based on the nature of the data and
methodology used, he cannot infer about the return of biodiversity and ecosystem
services lost with the conversion of forest to other land uses or degradation. Planted
forests emerge as an alternative to biomass production since they occupy a reduced
area (~2%) globally (FAO 2010). In Brazil alone, these forests occupy more than
seven million ha (IBÁ 2017). Although heavily criticized on environmental aspects,
these forests represent alternative sources of raw material, energy, and income for
farmers. Thousands of direct and indirect jobs, investments in local infrastructure,
and foreign exchange for the country are due to forestry business. In Brazil, about
BRL 10 billion was generated for the communities around the business units of the
sector (http://www.iba.org/statisticaldata).
About the relationship between ecosystem services (ES) and management of
planted forests we can say that, on different scales, companies and research, exten-
sion, and education institutions have studied, monitored, and proposed management
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 195

and land-use alternatives capable of reversing the processes of degradation of natu-

ral resources or even increasing the supply of goods and services provided by them
(Brockerhoff et al. 2013; Ferraz et al. 2013; Gonçalves et al. 2013).
Water regulation, maintenance of soil fertility, regulation of climatic conditions, and
erosion control are some of the ESs provided by planted forests when well managed. In
most of the tropical regions, planted forests are highly productive monocultures due to
the uniformity of plots and management (Gonçalves et al. 2013; Liu et al. 2018), but
mixed (with poor diversity as reported in this book) and multi-­diversified or multipur-
pose plantations can make the production of wood and fibers environmentally and
socially fairer. Rural development, natural resource management, biodiversity conserva-
tion, and ecological restoration are concepts that should guide the activities of industrial
or family enterprises involved in the forestry business (Lima et al. 2012a; Liu et al. 2018).
This chapter provides a conceptual basis and application of the ES approach to
planted forests and forest plantations in three distinct Brazilian production environ-
ments: short-rotation intensive Eucalyptus plantations; low-diverse mixed planta-
tions and high-diversity mixed plantations; or multipurpose plantations. These three
systems differ in terms of area occupied, technological level adopted, and purpose.
The first system is represented by great paper, pulp, and coal companies in the
forestry business, which occupy more than seven million ha and are present in at least
15 states. They play an important role in the economy and in the generation of jobs
and income (IBÁ 2017). It is currently one of the most advanced agricultural activities
in Brazil, thanks to investments in research in the areas of plant breeding, genetic
improvement, and appropriated site management practice (Gonçalves et al. 2013).
The second management system is represented by less complex mixed plantations
with low diversity of species. Within this category, the most studied plantations in Brazil
are a mix of leguminous trees associated with diazotrophic bacteria (such as Acacia
mangium) and non-N2-fixing species (such as Eucalyptus), which are mentioned in this
book, and the less diverse plantations for the purpose of restoring severely impacted
degraded areas (Franco and Faria 1997; Parrotta and Knowles 1999; Chaer et al. 2011;
Balieiro et al. 2018; Franco et al. 2018). In terms of area, these plantations are basically
experimental plantations or small areas undergoing restoration in mining areas. The last
commented category is mixed multipurpose plantations. This can be subdivided into
two subclasses, for restoration purposes, with the possibility of using part of the planta-
tion for commercial/extractive purposes (restricted-use areas) and agroforestry systems.

10.2 Ecosystem Services

10.2.1 Background and Conception

According to Hermann et al. (2011), the concept of ecosystem services dates back to
the late 1960s and 1970s, highlighting the value of society over the roles of nature
(King 1966; Helliwell 1969; Ehrlich and Ehrlich 1970; Dee et al. 1973; Ehrlich et al.
1977; Bormann and Likens 1979). In the same way, in the 1970s, 1980s, and 1990s,
other scientists already drew the attention of society to the economic dependence
196 F. de Carvalho Balieiro et al.

on natural capital (Westman 1977; De Groot 1987; Daily 1997 and Costanza and
Folke 1997), where natural capital is the natural stock of natural assets that generates
a flow of goods or services that are useful or profitable to man over time (Costanza
and Daly 1992). This concept has persisted up to now, with small variations in the
scope of environmental economy. For Gómez-Baggethun and De Groot (2007), from
an ecological perspective, natural capital cannot be conceived only as a stock or
aggregation of natural elements, but as encompassing all ecosystem processes and
interactions, which determine its integrity and ecological balance.
Daily (1997) was one of the first authors to approach the concept of ecosystem
services as “the services provided by natural ecosystems and the species that com-
pose them, in sustaining and fulfilling the conditions for the permanence of human
life on Earth.” The definition of Daily (1997) is similar to that of Millennium
Ecosystem Assessment (MEA 2005), where ecosystem services are “the benefits
that human beings derive from ecosystems,” and it has been used in the literature in
general, with small variations (Nicholson et al. 2009).
The ES approach has some advantages that can be highlighted: working on mul-
tiple scales, connection between science and politics, emphasizing social and eco-
nomic aspects related to human well-being, aiming to promote the multifunctionality
of ESs, and providing financial or nonfinancial compensation to those who work in
favor of ecosystem services, among other aspects.
Furthermore, the literature on this theme has increased exponentially (Fisher
et al. 2009), especially after the launch of the Millennium Ecosystem Assessment
(MEA 2005), which proposed to evaluate ESs and the benefits derived directly and
indirectly from ecosystems.
The MEA was requested by UN Secretary-General Kofi Annan in 2000 and was
conducted between 2001 and 2005, involving more than 1300 scientists and 95
countries (TEEB 2010). It aimed to assess the consequences that changes in ecosys-
tems bring to human well-being and the scientific basis for actions needed to
improve the preservation and sustainable use of these ecosystems. This unique
effort to systematize information on ecosystem services and its contribution to
human well-being demonstrates that the international community recognizes the
need for and urgency of adopting innovative measures to protect ecosystems, align-
ing preservation with economic development (Andrade and Romeiro 2019).
After 2005, several authors worked in this area; they produced data for the clas-
sification, evaluation, quantification, mapping, modeling, and valuation of e­ cosystem
services, in order to subsidize decision-making in relation to ecosystems (Wilson
and Carpenter 1999; Heal 2000; De Groot et al. 2002, 2010; MEA 2003, 2005;
Turner et al. 2003; De Groot 2006; Fisher et al. 2009; Rounsevell et al. 2010;
Dominati et al. 2010; Ferraz et al. 2013; among others).
There are several global initiatives to promote research, development, and public
policies focused on the provision of ecosystem services, such as The Economics of
Ecosystems and Biodiversity (TEEB), the Natural Capital Project, Intergovernmental
Platform on Biodiversity and Ecosystem Services (IPBES), Ecosystem Services
Partnership (ESP), Knowledge and Learning Mechanisms on Biodiversity and
Ecosystem Services (EKLIPSE), Europe Ecosystem Research Network (Alter-Net),
and Water Funds.
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 197

In Brazil, many studies have been and still are developed on biodiversity preserva-
tion and environmental conservation in the different biomes, due to the rich biodiver-
sity and natural resources of the country and the processes of degradation due to
different anthropogenic pressures. The number of publications and interest specifi-
cally on the ES theme are also increasing (see Ferreira et al. 2012; Brockerhoff et al.
2013; Ferraz et al. 2013, 2014; Prado et al. 2016; Periotto and Tundisi 2018).

10.2.2 Classification of Ecosystem Services

In terms of services provided by ecosystems, three categories are generally consid-

ered: regulation, provision (supply), and cultural (MEA 2003; Hein et al. 2006). In
addition, another category of support services has been widely used in MEA (2003),
but the latter has not been widely used in ecosystem assessment because of the
double meaning or overlap with other service categories (Fisher and Turner 2008).
It should be mentioned that, based on the work on environmental accounting car-
ried out by the European Environmental Agency (EEA), an international classifica-
tion system for ESs has been developed since 2009, called the Common International
Classification of Ecosystem Services (CICES), which is currently in its V5.1 ver-
sion (Haines-Young and Potschin-Young 2018). This initiative, in direct contribu-
tion to the United Nations Statistics Division (UNSD), a review of the Environmental
Economic Accounting System (SEEA), aimed to establish an internationally stan-
dardized ES classification system. The idea of establishing an international classifi-
cation is from the need to standardize the description of the ESs so as to enable the
establishment of methods of environmental accounting, mapping, and evaluation
for ESs that may be replicable and comparable.
The CICES classification used as its starting point the typology suggested by the
Millennium Ecosystem Assessment (MEA 2005), which, with the exception of the
category of support services, considered the other three categories of services: provi-
sion, regulation, and cultural. The support services category was deliberately excluded
because, as an intermediary service, relations between the ecosystem and environmen-
tal accounting in this case are not explicit. Thus, CICES, adopting a pragmatic view,
chose to emphasize the final outputs of processes that effectively benefit and have
direct and explicit value to people (Haines-Young and Potschin-Young 2018). However,
as the authors themselves warn, the intermediary and support services should not be
ignored or neglected. The classification presented below will be MEA (2005).

10.2.2.1 Support Services

For MEA (2005), support services are those required for the production of the other
ESs. They differ from the basic categories insofar as their impacts on man are indi-
rect or occur in the long run. Examples are primary production, atmospheric oxygen
production, soil formation and retention, nutrient cycling, water cycling, and habitat
provision. Forests are great natural assets that provide these services.
198 F. de Carvalho Balieiro et al.

The cycles of several key nutrients for life support have been significantly altered
by human activities over the past two centuries, with positive and negative conse-
quences for other ecosystem services, as well as impacts on human well-being.
Forests are responsible for maintaining biodiversity. In Brazil, the ecosystem
services were threatened by actions of deforestation and fires, associated with the
dynamics of land use, agricultural and livestock expansion, and urban areas.
According to the Ministry of the Environment, the loss of natural environments is
estimated at between 15 and 18% in the Amazon biome; 50% in the Cerrado,
Pampas, and Caatinga biomes; and 88% in the Atlantic Forest biome (Ferreira et al.
2012). Sparovek et al. (2010) estimated an environmental liability of 21–30 million
hectares, which have to be restored in Brazil.
Natural ecosystems provide habitat and food requirements for a wide range of
arthropod predators and parasitoids, insectivorous birds, and microbial pathogens
that act as natural enemies of agricultural pests and thus provide biological control
services (Tscharntke et al. 2005). An ecosystem service that has been greatly com-
promised by the suppression of forests is pollination by reducing habitats for birds
and insects, compromising the ESs of regulation and provision.

10.2.2.2 Regulation Ecosystem Services

This relates to the regulatory characteristics of ecosystem processes, such as main-

tenance of air quality, climate regulation, erosion control, purification and regula-
tion of water flow, self-purification of water (process of degradation of nutrients
contained in water bodies due to sources of pollution, usually sewage), regulation of
human diseases and pests in agriculture, pollination, and mitigation of natural dam-
ages. These services are derived almost exclusively from regulatory ecosystem
purposes.
Unlike provisioning services, their assessment does not occur by their “level” of
production or quantity available, but by the analysis of the ability of ecosystems to
regulate certain services.
Forests play an essential role in regulating services, for it is through them that
climate regulation, for example, is affected by deforestation and burning practices,
drastically impacting climate change and its effects on the economy and the quality
of life of society.
Forests also participate in water regulation and carbon sequestration. Water regu-
lation is an ecosystem service that is highly related to the management of produc-
tion systems, either through the direct use of water in irrigated systems or because
of the changes they impose on the physical-biotic environment of the river basins
that interfere with the water, hydrological, and climatic cycles. On the other hand,
the deforestation caused for the implantation of agricultural systems can alter the
regional precipitation regimes, through the changes in the evapotranspiration flows
of clouds. The local climate can then become drier, not only impacting ecosystems
but also compromising water security (Vergara and Scholz 2010).
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 199

Many studies estimated the potential of forests to sequester carbon, which is an

ecosystem service regulator (Lal 2005; Jandl et al. 2007; Sedjo and Sohngen 2012).
In times of climate change, they disagree on whether the carbon forest balance in
future will be positive or negative (in photosynthesis or respiration) and heat up the
backstage of research (Bonan 2008; Bellassen and Luyssaert 2014; Nottingham
et al. 2015).
In this sense, planted forests, when well managed and with mixed plantations,
can also contribute to the regulatory services mentioned here, as will be presented
in the subsequent items.

10.2.2.3 Provision (Supply) Services

For MEA (2005), these services include products obtained directly from natural or
seminatural ecosystems (agriculture), such as food and fiber; wood for fuel and
other materials that serve as a source of energy; genetic resources; biochemical,
medicinal, and pharmaceutical products; ornamental resources; and water.
Data from world food production illustrate the increase in the generation of pro-
visioning services. According to MEA (2005), between 1961 and 2003 food pro-
duction increased by more than 160%, with cereal production increasing 2.5 times,
beef and sheep production increasing 40%, and production of pork and poultry meat
increasing 60% and 100%, respectively.
Forests, in addition to the provision of water and food, are able to provide medic-
inal products, fiber, wood, and energy. Due to the richness of Brazilian biodiversity,
native vegetation is a source of food resources in all Brazilian biomes. Many native
plants are now domesticated and widely used in the country, such as palm heart,
cassava, pepper, peanut, guaraná, pineapple, and cacao (Prado and Murrieta 2015),
while others are more regional, such as pine nuts in the Araucaria Forests.
Products derived from plant extraction can be classified as timber and non-­
timber. In 2016, the value of non-timber products (BRL 1.9 billion) was 4.6% higher
than in 2015 and 18% higher than in 2014 (SNIF 2017), with 86.5% (BRL 1.6 bil-
lion) corresponding to extractive activities in native forests. Non-timber products
(as waxes, saponin, honey, or food products) generally are extracted by traditional
populations and family farmers. Food products, such as açaí, native erva mate, and
Brazil nut, generated in 2015, respectively, $480, $396, and $107 million Brazilian
Reals, while waxes (carnauba powder), oilseeds (babaçu nuts), and fibers (piassava)
each generated more than $195, $107, and $101 million Brazilian Reals in 2015
(SNIF 2016).
Brazil is the third largest exporter of forestry products (e.g., timber, pulp, paper,
resins, tannins, gums), accounting for 3.64% of the total global market volume
(FAO stat; data for 2016). Forest products generally rank fourth in the ranking of the
value of national agribusiness exports, only behind soybeans, meat, and sugar-­
alcohol complex. Therefore, native and planted forests definitely contribute to this
national scenario of ES provision.
200 F. de Carvalho Balieiro et al.

10.2.2.4 Cultural Services

These include cultural diversity, as the very diversity of ecosystems influences the
multiplicity of cultures, religious and spiritual values, generation of (formal and
traditional) knowledge, and educational and aesthetic values, among others. These
services are closely linked to human values and behaviors, as well as to social insti-
tutions and patterns, characteristics that make their perception different among
groups of individuals, making it difficult to evaluate their provision (Andrade and
Romeiro 2019).
Still, according to Andrade and Romeiro (2019), societies have developed an
intimate interaction with the natural environment, which has shaped cultural diver-
sity and human value systems. However, the transformation of natural ecosystems
into cultivated landscapes with more homogeneous characteristics associated with
economic and social changes, such as rapid urbanization, improvement and cost
reduction of transportation conditions, and intensification of globalization, has
weakened the links between ecosystems and cultural diversity/identity.
On the other hand, the use of ecosystems for recreation and tourism purposes has
increased, mainly due to population growth and greater availability of time for lei-
sure, mainly of the populations with greater purchasing power and greater access to
infrastructure, which facilitate access to cultural services. Ecological tourism, for
example, corresponds to one of the main sources of income for some countries that
still have a large part of their ecosystems conserved.
Forests contribute effectively to cultural services, since they make up landscapes
with a greater diversity of flora and fauna, which becomes an attraction for humans.
They also contribute to water regulation and provision, as well as keeping water bodies
such as rivers, lakes, waterfalls, and other pristin services, enabling recreation and
tourism. In addition to these benefits, forests are associated with diverse believes reli-
gions, and spiritual aspects of traditional peoples such as indigenous people and others
living in forests, factors that are related to cultural ecosystem services (ES). Kreye
et al. (2017) present a discussion about forest-related, cultural ES.
It should also be highlighted that in order to show the ES provided by natural and
planted forests, many studies have been carried out, based on different methodolo-
gies, aiming at their quantification and valuation. Masiero et al. (2019) present a
manual with several methods for quantifying and valuating ESs from forests.

10.3  cosystem Services of Monoculture, Intensely Managed

E
Planted Forests

Over the past 50 years, eucalypts went from being a risky investment in Brazilian
silviculture to a global forestry success story, perhaps compared to the achievement
of Henry Wickham, responsible for the expatriation of the rubber tree to Kew
Gardens and then to its final scale in Malaysia.
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 201

Due to its geographical origin and anatomical characteristics that imply growth
stresses that hinder drying, in addition to its wood being considered of moderate
durability against rotting fungi and termites (Silva et al. 1995), Eucalyptus was
viewed with distrust at the time of the introduction of the industrial plantations. But
what is eucalypts for? This was a relevant question years ago, and it is with it that
the book by Higa et al. (2000) entitled “Eucalyptus Plantation in Small Rural
Properties” begins. The publication presents the genus Eucalyptus spp. for small
properties, and argues:
Eucalyptus involves more than 600 species that are adapted to different climates and soils
and can be used for different purposes. Eucalyptus can be planted as ornamental trees in
parks and gardens; the leaves can be used in floral arrangements and for extracting oil and
the flowers are used for honey production. The most common use is the use of wood such as
firewood, poles, fences, rural buildings, production of saw wood, panel manufacturing and
paper and pulp manufacturing.

Eucalypt is the most planted forest crop in Brazil and is a raw material for indus-
trial and domestic use. Currently, more than 91% of all wood produced for industrial
purposes in Brazil comes from this essence, generating 510,000 jobs directly and 3.7
million indirectly, and contributing to the GDP with BRL 71 billion (IBÁ 2017).
Since its introduction in Brazil in 1909 by Edmundo Navarro de Andrade, in the
state of São Paulo, Eucalyptus came to fulfill one of the four types of ecosystem
services, the provisioning.
Its introduction and naturalization were a huge success and, in addition to sup-
plying the Brazilian and world fiber market, eucalypt is also a source of energy and
timber for Brazilian forestry companies, considerably reducing the pressure on the
native forests, guaranteeing the conservation of the genetic patrimony associated
with these forests.
It cannot be denied that in addition to provisioning, Eucalyptus provides other eco-
system services important to our society, regulating environmental conditions by car-
bon sequestration; providing cultural services such as spaces for recreation and a
socioeconomic identity factor; and finally supporting services that influence the for-
mation of soil and habitats, nutrient cycling, and oxygen production, among others.
Regarding support services, the forest sector currently protects and conserves
almost six million hectares, in areas of permanent preservation (APPs, 30%), legal
reserve areas (RL, 67%), and private reserve areas (RPPN, 3%), which contribute
directly to the conservation of biodiversity, soil, and water (IBÁ 2017). According
to a database of the main companies in the sector and organized in their 2017 report
on the biomes of the Atlantic Forest and Cerrado, of the species threatened with
extinction in the national territory, 38% of the mammals and 41% of the birds were
found in areas belonging to Brazilian forest companies (IBÁ 2017). Around the
world and in Brazil, planted forests represent an increasing proportion of the global
forest area and partly compensate for the loss of natural forest in terms of forest
area, habitat for biodiversity, and ecological function (Brockerhoff et al. 2013;
Ferraz et al. 2013).
The performance of planted forests in terms of environmental benefits is highly
dependent on their management plan, especially with respect to the hydrological
202 F. de Carvalho Balieiro et al.

regulation of micro-basins, since their growth and productivity are related to impor-
tant social (hydrosolidarity and land-use conflicts) and environmental (climate
change and biodiversity) issues (Lima et al. 2012b; Ferraz et al. 2013). Recently,
Cassiano (2017) monitored the hydrological regime and water quality in three
micro-basins (one micro-basin with age and species in mosaic management, two
with conventional eucalypt management), demonstrating that the mosaic was more
adequate in the regulation of the hydrological regime and water quality in relation
to conventional management of eucalypt-planted forests. Ferraz et al. (2013) stud-
ied examples of forest management alternatives at macro- (theoretical thresholds
for the management of evapotranspiration) and meso-scales (using data from a
catchment experiment) that contribute to improve water conservation in forest land-
scape areas in Brazil. Their results suggest that for effective water conservation in
Eucalyptus spp. plantations the scales of evaluation must be considered. At regional
scale, the natural climatic constraints of water availability should drive the choice
of more water-efficient species/varieties and forest management, while at the meso-­
scale the proportion of native forest in the landscape plays a crucial role in reduc-
tion and regulation of water use. In other words, mosaic management could stabilize
flows from plantation areas. Figure 10.1 summarizes the theoretical potential of
different forest landscapes to provide some hydric ecosystem services (adapted
from Ferraz et al. 2013).
In micro-basins, generalized clear cutting can increase the concentration of nutri-
ents and suspended sediments in the waters of the micro-basin, leading to losses of
the natural nutritional capital of the soil, water quality, and storage capacity of the
reservoirs and damages to productivity in medium and long terms (Lima et al.
2012b). The water quality indicators that were most affected by the clear cutting of
eucalypt in monitored micro-basins are turbidity, color, and electrical conductivity
(Câmara et al. 2000).
Water consumption in Eucalyptus plantations is not very different from the con-
sumption of other species that have the same growth rate. That is, the greater the
biomass production, the greater the water consumption to provide growth. However,
there are differences within and between species in the efficiency of water use (bio-
mass produced per unit of water consumed), due, for example, to physiological
mechanisms that reduce transpiration as in cases of reduction in leaf area index in
regions of greater water deficit (Fig. 10.2).
Management strategies considering selected genotypes and plant spacing can
also increase the water security of commercial forests. Wood biomass at tighter
spacing is generally higher (47–57 kg tree−1 at a planting density of 591 trees ha−1
vs. 13–24 kg tree−1 with 2949 trees ha−1) but exhibited trees present lower leaf water
potentials resulting in a trade-off between productivity and potential water stress
(Hakamada et al. 2017). Of the genotypes tested, the E. urograndis clone presented
the best performance from the lowest to highest planting density, while the hybrid
E. grandis × E. camaldulensis, the worst. In other words, for both industry and
­family farmers they will be less vulnerable to climate change (water stress) under-
standing the interaction between planting density and genotypes. The authors expect
that for lower water availability, regional potential water stress will be higher with
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 203

Fig. 10.1 Mosaic of eucalyptus forest plantations (on the upper plateau) and native forest in lower
part of the landscape close to the stream (Internet photo)

total stand (stem wood) biomass productivity increase, and the opposite would be
true in areas with higher water availability.
Another important factor to consider in the water balance is the fact that forests,
despite being innate water consumers, also intercept rainfall and in the case of euca-
lypt, due to leaf characteristics such as leaf area, allow more water to reach the for-
est floor, when compared to the Pinus genus, for example (Paula Lima et al. 2013).
Companies are also striving to adopt more sustainable practices. Management
techniques as leaving plant residues on the soil (ground or not), planting seedlings
directly on the straw, and desiccating undergrowth rather than revolving the soil, all
have led to minimized soil erosion. Likewise, rational use of pesticides, management
of fertility and crop health, and planning and maintenance of roads and roadways
within the areas also contributed to the mitigation of erosive processes, significant
improvements in soil and water quality, and biodiversity conservation (Chaer and
Tótola 2007; Brockerhoff et al. 2013; Gonçalves et al. 2013). All of these actions
contribute to the environmental regularization of properties and forest certification by
the Forest Stewardship Council (FSC) and the Program for the Endorsement of Forest
Certification (PEFC), represented in Brazil by the National Forest Certification
Program (Cerflor), with strict monitoring indicators and biodiversity management.
204 F. de Carvalho Balieiro et al.

Fig. 10.2 Performance variation of expected ecosystem services linked to water conservation pro-
vided by different forest cover management systems (adapted from Ferraz et al. 2013; illustration
by F.C. Balieiro)

Despite these advances, production of planted forests in detriment of other eco-

system services is advancing in some companies, but this vision must change, espe-
cially under the logic that increasing the area of planted forests will not compensate
for loss of biodiversity and scenic or cultural services (for example) due to the loss
of natural forest cover. To give an example, because it is extremely sensitive to weed
competition, the control of weeds (Zen 1987; Tarouco et al. 2009) and invasive or
pioneer species is difficult to give up given the sensitivity of Eucalyptus to resources
in the initial stage of establishment. On the other hand, as detected by Stallings
(1990) in the Atlantic Forest biome, more than 50% of the species of mammals and
birds found in primary forest were found in eucalypt areas with understory vegeta-
tion and, on the contrary, none of them in plantations without this vegetation. In
other words, the production logistics of the sector must be rethought, since the mix-
ing of tree species (mixed plantations) can improve the performance of the
Eucalyptus stand, with gains in several other ecosystem services.
An important aspect to be considered in relation to the environmental services of
Eucalyptus as well as its impacts, is the scale at which species of this genus are
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 205

planted. Another point concerns the species, since the choice of the appropriate spe-
cies will influence the quality and quantity of the ecosystem service.
Regarding the ecosystem services of the soil associated with Eucalyptus planta-
tions, it is worth mentioning that soil carbon stocks and organic matter increases
have been comparable to natural ecosystems (Fialho and Zinn 2014). Although
some changes in soil and climate behavior may be evident (Cook et al. 2016), forest
ecosystems retain more of this soil asset than the Brazilian agricultural sector.
According to the Brazilian Institute of Geography and Statistics, IBGE, agricultural
activities cover an area of about 350 million hectares, of which approximately 172
million hectares are destined to pasture and with more than 50% of these areas in
some state of degradation (Macedo et al. 2013). These degraded areas could be
managed by the forest sector with many other environmental gains.
The management of Eucalyptus as well as any other silvicultural activity implies
a permanent culture with cycles varying from 5 to 20 years of rotation, with fire
being banned from these areas, unlike poorly managed pastures that sometimes
burn in one cycle of fire-free cutting of Eucalyptus, thus avoiding emissions of
greenhouse gases and soil degradation.
In summary, the planting of Eucalyptus may be the opportunity for the conver-
sion of exclusively agricultural landscapes to agroforestry such as agrisilviculture,
silvipastoral, and agrosilvopastoral systems. After all, eucalypt is recognized by
farmers as a commodity, being adopted as a more familiar crop, as opposed to plant-
ing native species which, although more advantageous in providing ecosystem ser-
vices, is not easily accepted in rural areas.
Thus, the adoption of Eucalyptus and appropriate management can promote the
transition to natural forest restoration through the regeneration of pioneer and early
native species in its understory, which may facilitate the succession of forests
(Parrotta et al. 1997), and thus the provision of ecosystem services.

10.4  cosystem Services in Low-Diversity, Mixed-Planted

E
Forests

Low-diversity (with up to five species), mixed-planted forests are common in pro-

grams for the restoration of severely degraded areas, such as mining areas (Franco
and de Faria 1997; Parrotta and Knowles 1999; Singh et al. 2006; Franco et al.
2018), or in areas under environmental restoration where the availability of seed-
lings or seeds is low (Rodrigues et al. 2009). In Brazil and in other countries such as
Australia, the USA, Congo, and Costa Rica, plantations that associate N2-fixing trees
and non-N2-fixing tree species have gained importance in the last years. These
mixed plantations have been studied under different experimental designs (Forrester
et al. 2006; Kelty 2006), and most of them concentrate on the use of exotic species
(Forrester et al. 2006; Liu et al. 2018; Marron and Epron 2019). Most of the results
brought to this point are derived from the other chapters, especially from the experi-
ence with Eucalyptus and Acacia mangium in Brazil.
206 F. de Carvalho Balieiro et al.

The provision of timber for energy or industrial purposes (paper and pulp)
through mixed Eucalyptus and N2-fixing species may reach higher levels
than Eucalyptus monocultures (Binkley et al. 1992; Kaye et al. 2000; Forrester
et al. 2013; Koutika et al. 2014; Santos et al. 2016). However, this fact cannot be
generalized (Marron and Epron 2019). Based on data from experiments in five loca-
tions in Brazil and one in the Congo, the global production of timber from mixed
plantations was higher in poorer and sandy soils and where the climate favored the
development of the legume (Acacia mangium) (Santos et al. 2016). A very recent
meta-analysis by Marron and Epron (2019), with 148 case studies around the world,
showed that plant mixtures have a significantly positive global effect, with mixed-­
tree plantations being 18% more productive than the non-N2-fixing monocultures,
and this effect was significantly different from zero (null) under temperate condi-
tions (24% more productive) but not under tropical conditions (12% more produc-
tive). They attributed these findings to nitrogen availability (generally less in
temperate climate). However, as cited above, the marked success of the mixture is
more evident in sites with low biomass production potential.
Comparing with the national average of eucalyptus productivity in monocultures
(~20 Mg ha−1 year−1) (Stape et al. 2010; Gonçalves et al. 2013), and the possibility
of opening markets for other types of raw material, the rural producer and the indus-
try would have more income and business options when handling mixed planta-
tions. Considering that one half of the pasture area is in some degree of degradation
(Oliveira et al. 2004), and that sandy soils cover around 10% of the Brazilian
­territory, these mixed plantations can provide additional gains in timber, and of
several other ecosystem services for the property or countryside. The possibility of
using timber or non-native species can also bring even greater benefits resulting
from the conservation of native biodiversity.
One of the main concerns regarding successive rotations of tropical Eucalyptus
plantations is the soil nitrogen (N) balance, which generally becomes negative with
multiple rotations due to a combination of high N exports from timber harvests and
low doses of N fertilizers that are typically applied (Corbeels et al. 2005; Laclau
et al. 2010). Thus, N inputs are required to sustain satisfactory forest production,
which is accomplished generally by nitrogen fertilizer applications (e.g., urea,
ammonium sulfate, and ammonium nitrate). Plantation of Eucalyptus in consortium
with N2-fixing trees is a valuable and sustainable technique, because it can provide
an increase in the N availability for Eucalyptus trees, obtain high timber productions
even without the use of N fertilizers (Voigtlaender et al. 2012; Santos et al.
2016), with low greenhouse gas emissions, especially the nitrous oxide (N2O), orig-
inating from N fertilizations (Silveira 2018). Tchichelle et al. (2017) showed that
soil N mineralization was 82% higher under Acacia mangium monoculture and
53% higher under mixtures with A. mangium and E. grandis than in E. grandis
monoculture, although differences in N stock and C:N ratio in the 0–25 cm soil
layer between the two pure treatments were not significant. The higher N mineral-
ization rate in pure legume tree plantations or in mixed plantations, when compared
to Eucalyptus monocultures, has also been observed in other studies in the tropics
(Bernhard-Reversat 1996; Parrotta 1999; Forrester et al. 2005).
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 207

In terms of N2O emissions in mixed plantations established in the Southeast

region, Santos et al. (in preparation) detected very low emissions of nitrous oxide
from sandy soil (except in some periods of prolonged rainfall). This is due to the
absence of mineral fertilization at the fifth year of the plantation and the fact that
the soil in the experimental area has a low water retention capacity. However, when
analyzing the accumulated emissions, these were higher in the A. mangium envi-
ronment, in relation to E. urograndis, and with intermediate values for the mixed
plantations (E. urograndis + A. mangium). In recently established tree plantations
on medium-textured Oxisols (clay content ranging from 34 to 42%), in central-
western Brazil, Silveira (2018) observed the same emission pattern, with low aver-
age flows in the dry period. This was explained by the low availability of inorganic
nitrogen in the soil and due to the absence of microanaerobic sites within the
microaggregates of the soil, and higher flows during the wet season. However, the
application of N fertilizer (via urea) in the E + N treatment resulted in an increase
in N2O fluxes that began to be noticed a few days after application of N, coinciding
with the highest rainfall event after application of N, when soil moisture content
increased. It has been speculated that several years later, far from the initial phase
of forest growth, when fertilization and soil-tillage operations cease and the N
emissions are usually very low, the enrichment of N in the soil provided by the
legume might raise the emissions of N2O, in relation to Eucalyptus monocultures
(Rachid et al. 2013). However, many more studies must be encouraged before this
can be corroborated as a fact. In addition, we believe that the low nitrous oxide
emission probably is ­compensated by higher C sequestration by the soil and no N
fertilizer application in mixed plantations, but these balances have not been
obtained yet.
The sequestration of atmospheric C by mixed-planted forests is another ecosys-
tem service of these forests. This service is proportional to the growth rates of these
plantations, which can vary with factors such as planting structure, composition,
age, climatic condition, and soil type (Cook et al. 2016; Brandani et al. 2017;
Marron and Epron 2019). The total amount of C sequestered by these plantations
varies with the proportion of the total allocated in woody tissues and the end use of
this biomass. Thus, uses for civil construction, wooden posts, furniture, and handi-
crafts increase the mitigating potential of the planted forests. On the other hand, if
the use is for energy purposes, the sequestration becomes temporary. Carbon
sequestration through soil is strongly related to the conversion to other uses for
mixed plantings, or for more conservative management of soil and crop residues.
Soil organic matter plays a role in a series of processes and properties from which
several essential ecosystem services emerge, such as nutrient filtration, waste recy-
cling, water filtration and storage, and flood control, among others (Dominati et al.
2010). As already presented in several chapters of this book, mixed plantations with
non-N2-fixing trees and N2-fixing species can sequester more C than pure planta-
tions of non-N2-fixing trees, such as Eucalyptus. However, this effect is particularly
dependent on the development and type of interactions of the species, as well as on
the local edaphoclimatic conditions (Balieiro et al. 2008; Voigtlaender et al. 2012,
2019; Koutika et al. 2014; Rocha et al. 2019).
208 F. de Carvalho Balieiro et al.

Erosion control and flood mitigation are ecosystem services provided by all
kinds of forests. This includes mixed plantations, with planting on the remnants of
the previous crop, because of the rapid covering of the soil by the plants (<2 years),
and efficient exploitation of the soil mass resulting from complementarity and/or
competition of aerial and underground niches (Chaer and Tótola 2007; Laclau et al.
2013; Silva et al. 2015; Santos et al. 2016). They protect the soil against the impact
of raindrops, preserving and stabilizing the soil structure. Soil losses in
Eucalyptus and Acacia plantations are usually low (<2.0 Mg ha−1), reducing associ-
ated losses of nutrients from these plantations.
The expected improvements of the microbial activity, due to litter introduction of
N2-fixing legumes are conditioned by the structural quality of the litter produced by
the species, the litter stoichiometry (N:P ratio), and the increase in the diversity of
intercropping tree species, but divergent results can be found in the literature, in
terms of decomposition, as discussed in Chap. 4.
Recent research has increased our understanding of the interactions that occur
between microbiome-soil and microbiome-plant in mixed-plantation systems, par-
ticularly using Acacia mangium trees as a model plant (Rachid et al. 2015; Pereira
et al. 2017; Fonseca et al. 2018; Bini et al. 2018). The search for specific roles in
natural ecosystems and applying them in agriculture (Andreote and Silva 2017), as
in the case of mixed-forest plantations, can increase the sustainability of planted
forests. Studies with microorganisms associated with the soil-plant interface in
Eucalyptus breeding programs have been neglected for years and we still know very
little about this plant-microbiome interaction. In a forest system, trees are ­dependent
on the microbiome to survive, which provides nutrients essential to their develop-
ment, such as N, P, and K (primary macronutrients), by cycling organic matter in the
soil. It was estimated that N2-fixing bacteria and mycorrhizal fungi are responsible
for furnishing up to 80% of all phosphorus and 75% of all nitrogen that forests use
in their life cycle (van der Heijden et al. 2013).
A recent study evaluating a mixed-cultivation system between E. grandis and
A. mangium on a 4-year-old and sandy-textured red-yellow Latosol
(Ferralsol) showed strong influence of the composition of plants on the microbial
community structure of the soil, both at the surface (0–20 cm) and at the subsurface
(20–800 cm) (Pereira et al. 2017). In this study, the structure of the bacterial com-
munity was completely different when comparing with the pure treatment of
E. grandis and the mixed treatment of the same species, suggesting that the acacia
plants are the main modulators of the structure of the microbial community of the
soil (Pereira et al. 2017). It is still unclear which effects are due to this behavior, but
this may have occurred due to the production of root exudates by A. mangium and,
mainly, by changes in soil chemical attributes that occur in the root region, espe-
cially high levels of carbon and nitrogen (Rachid et al. 2013; Pereira et al. 2018).
Similarly, a mixed plantation of E. urograndis and A. mangium at 3 years of age
installed in a Haplic Planosol (0–10 cm) of sandy texture (90% sand) showed,
through the PCR-DGGE technique, profiles of bands with significant differentia-
tion in the soil bacterial community structure (Rachid 2013). In this study, the
bacterial community showed the effect of each isolated plantation, which presented
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 209

a community structure with its own characteristics, and community integration in

the mixed treatment. In other words, the mixed treatment bacterial community had
characteristics of both species, where the intermediate position leads to the belief
that there is a balance in the influence of each species in relation to the community
structure (Rachid et al. 2013). Thus, the influence of the plant composition of the
mixed plantations between Eucalyptus and Acacia seems to be variable, becoming
differentiated according to the edaphoclimatic factors of the place, the soil layer
sampled, and the age of the stands. Because such studies were introduced relatively
recently, learning about the changes in the soil microbial community in different
regions, in contrasting soil and climate conditions, becomes necessary in future
research.
Among the fungal types, two main classes are predominant in forest ecosystems,
saprophytic and symbiotic fungi. In this sense, the roots of the trees can perform
associations with the most varied types of fungi, such as arbuscular mycorrhizal
(AMF) and ectomycorrhizal (ECM) fungi (Bonfanti and Anca 2009). Several types
of mycorrhizal fungi present specificity for a single tree species (Lang et al. 2011).
However, Eucalyptus and Acacia roots have the ability to associate with both AMF
and ECM and, in some cases, with both types of symbionts at the same time (Pereira
et al. 2018; Bini et al. 2018).
Bini et al. (2018) published possibly the first evaluation of AMF effects on a
mixed cropping system. A study by Bini et al. (2018), on the dynamics of AMF dur-
ing the first 20 months after planting pure and mixed stands of E. grandis and
A. mangium, showed that the colonization by AMF in E. grandis roots was
­significantly higher, when the trees were grown in mixed systems with A. mangium.
They also identified a strong correlation between AMF colonization rates and acid
and alkaline phosphatase activities in soil, which are produced in greater quantity in
forests containing A. mangium.
In this aspect, with the greater plant diversity, the materials deposited on and
within the soil have the possibility of intensifying the nutrient cycling (Laclau
et al. 2010).

10.5  cosystem Services of High-Diversity, Mixed

E
Plantations: Multifunctional Planted Forest

Distinct types of forests—natural and planted forests or reforested areas—may pro-

vide ecosystem services at different levels; assessing the different aspects of forest
state, related biodiversity, and landscape context becomes essential to monitor the
forest and to estimate its contribution to the provision of ecosystem services (Chazdon
et al. 2016). Since multiple-use forests (accounting for almost 20% of tropical forest
area) are those that allow both production and conservation, in order to provide a
great extent of ecosystem services, planted forests are expected to be multifunctional
(Sloan and Sayer 2015).
210 F. de Carvalho Balieiro et al.

As described in Chap. 11 of this book, to be considered multifunctional planted

forests, high-diversity mixed-plantation forests must focus beyond forest structure
or species composition, targeting also ecological functioning, which may enhance
the provision of a wider variety of ecosystem services. Ecosystem multifunctional-
ity requires greater numbers of species, since different tree species were found to
influence different functions (Hector and Bagchi 2007). Besides providing ecosys-
tem stability, the provision of ecosystem services by biodiversity also meets human
society needs (Mori et al. 2013).
The evidence that the conservation of biodiversity is essential to provide ecosys-
tem services has led to the discussion of changes on both production systems and
rural landscapes. Deforestation and cropping remain the major causes of degrada-
tion of natural ecosystems (Rey Benayas and Bullock 2012; Sloan and Sayer 2015;
Curtis et al. 2018), leading to the challenge of proposing land uses to provide a wide
range of ecosystem services while conserving biodiversity in agricultural land-
scapes (Rey Benayas and Bullock 2012; Mori et al. 2013).
Agricultural intensification also causes biodiversity loss (Clough et al. 2011),
and the consequent loss of ecosystem functions sustaining ecosystem services (Mori
et al. 2013). In order to provide a full range of services, we need high-diversity-­
based production systems, planned to target the inclusion of ecosystem functions. In
a perspective from the biodiversity and ecosystem functioning (BEF) theory, apply-
ing response-and-effect traits into the assembling of a planted forest will help for an
optimal ecosystem multifunctionality (Mori et al. 2013; Laughlin 2014), leading to
improved conservation priorities and a more resilient ecosystem to face negative
effects of climate changes (Mori et al. 2013).
In order to have more multifunctionality in the rural landscape in the tropics,
mixed-planted forests are so an alternative to traditional cropping and allow a good
balance between production (as wood quality) and ecological benefits, like nutrient
cycling; further, mixed plantations with higher diversity may contribute to a more
efficient use of soil water (Amazonas et al. 2018). As commented above, adding
plant functional traits to mixed-planted forests may be effective for increasing multi-
functionality (Blesh 2018). The Eucalyptus-Acacia mixing model may supply nitro-
gen to the field, since Acacia species are N2-fixing trees. Including biological nitrogen
fixation (BNF) may supply nitrogen (N) to farm fields; in forest restoration, N2-fixing
cover crops have been used for weed control, contributing to enhance the multifunc-
tionality of the ecosystem (Blesh 2018). When Eucalyptus is combined with a mix-
ture of native trees in a high-diversity arrangement, the whole system was found to
be more efficient in the use of soil water, which may suggest that such an agroeco-
system may adapt to climate change conditions (Amazonas et al. 2018).
A meta-analysis showed that biodiverse agroforestry systems improve the provision
of ecosystems in comparison to simple (low diversity) agroforestry systems and con-
ventional production systems (Santos et al. 2018). Biodiverse agroforests were found
to reduce biodiversity loss and negative impact on the provision of ecosystem services
(Santos et al. 2018). The design and associated sustainable management of agrofor-
ests can avoid the removal of forest cover, optimizing both biodiversity and crop
production benefits (Clough et al. 2011; Lescourret et al. 2015; Damour et al. 2018).
10 Ecosystem Services in Eucalyptus Planted Forests and Mixed and Multifunctional... 211

The diverse layer consisting of multiple-use tree species is the main factor respon-
sible for the effective provision of ecosystem services (Lescourret et al. 2015).
Biodiverse agroforests are a type of high-diversity planted forests very highly
recommended to improve biodiversity levels and provision of ecosystem services,
supporting the planning of a biodiversity-friendly agricultural landscape (Santos
et al. 2018; Clough et al. 2011). Agriculture intensification is a cause for land-
scape simplification, and land-use planning must seek multifunctional landscapes,
providing goods and services, offering food security and actions for biodiversity
conservation (O’Farrell and Anderson 2010).
Multifunctionality is the capacity of a landscape to provide multiple socioeco-
nomic and ecological benefits (Hölting et al. 2019). Despite being unusual, it is
important to understand how biodiversity in agricultural landscapes provides mul-
tiple ecosystem services, which may help enhancing landscape complexity
(Birkhofer et al. 2018). Multifunctional, complex landscapes are expected to reduce
biodiversity loss and maintain a balanced supply of ecosystem services (Frueh-­
Mueller et al. 2018), and multifunctional planted forests play an essential role in
meeting those goals. Studies indicate that landscape management actions taken to
conserve biodiversity will always promote an enhancement in the provision of eco-
system services (Birkhofer et al. 2018).
A strategy adopted to promote complex landscapes is the concept of land spar-
ing, when biodiversity actions are allocated separately from production. On the
other hand, land sharing may consist of biodiversity-based agricultural practices,
with land uses or production systems that provide ecosystem services without
decreasing agricultural production (Rey Benayas and Bullock 2012). High-diversity
planted forests used for forest restoration is a good example of a land use based on
the principle of land sharing used to reduce biodiversity loss and environmental
health increase (Rey Benayas and Bullock 2012).
Beyond the arrangement of species in planted forests based on high biodiversity,
the landscape approach may support the design of land management to achieve
socioeconomic and ecological benefits in areas where land use traditionally com-
petes with biodiversity conservation (Sayer et al. 2013). The achievement of multiple
benefits depends on how stakeholders (farmers) are motivated to contribute to a
wider range of ecosystem services (Frueh-Mueller et al. 2018). Incentive mechanism
as payments for ecosystem services (PES) is a way to stimulate high and balanced
provision of ecosystem services in productive landscapes, offering the opportunity
for local stakeholders to participate in the decision-making process (Frueh-Mueller
et al. 2018). PES may encourage farmers to keep the forest cover and enhance the
permeability of the landscape (Tscharntke et al. 2011). Farmers have the chance to
make choices for multispecies cropping system designs, selecting plant species and
creating multifunctional agroecosystems, managing for crop yield and provision of
ecosystem services (Damour et al. 2018). Multifunctional landscapes try to hold
social and ecological dimensions in the management of a more complex landscape
(Lescourret et al. 2015).
Multifunctional planted forests are able to provide economic besides ecological
benefits, by either restoring or conserving biodiversity and related ecosystem services.
212 F. de Carvalho Balieiro et al.

However, that approach presents some challenges as well, since it is necessary to

ensure that, besides providing ecosystem services, multifunctional planted forests
must support the needs of different stakeholders (Bullock et al. 2011). The assessment
of studies focusing on the definition of multifunctionality indicated that about 33% of
studies assessed ecological and socioeconomic variables in equal shares and inte-
grated the perspectives of the stakeholders as well (Hölting et al. 2019).
High-diversity-based planted forests may ensure the provision of multiple ser-
vices, since farmers have a clear understanding of how the ecosystem design and
associated management practices can do that. In the landscape approach, the
exchange of knowledge and experience among stakeholders is essential for a multi-
functional landscape (Tscharntke et al. 2011). The success in using multifunctional
planted forests to build a sustainable agricultural landscape is strongly based on
achieving social and economic benefits. Therefore, the demand policies must con-
sider a landscape scale to promote multifunctionality (Holt et al. 2016).

10.6 Final Comments

Forests may provide ecosystem services (ES) at different levels, but the implementa-
tion of a sustainable and multifunctional landscape requires focus on a range of issues
and principles, as adaptive management, stakeholder involvement, and multiple objec-
tives (O’Farrell and Anderson 2010; Sayer et al. 2013). Some constraints that must be
overcome include institutional and governance concerns, transparent negotiation, and
share of rights (O’Farrell and Anderson 2010; Sayer et al. 2013). Learning actions to
bring together the multiple stakeholders in the construction of multifunctional land-
scapes and ways to foster synergy between ecosystem functioning and social dynam-
ics are needed (O’Farrell and Anderson 2010; Lescourret et al. 2015).
Under local and regional scale the mosaic of exotic planted forests and native
forests in the rural landscape matrix has brought immeasurable benefits to sustain-
ability. The mixed-planted forests (with low or high diversity) emerge as an alterna-
tive to traditional cropping and allow a right balance between production (wood)
and ecological benefits. Multifunctional landscapes are expected to reduce biodiver-
sity loss and maintain a stable supply of ecosystem services, while under commer-
cial level increased rotation length, multiple uses, alternative spacing and species or
clone arrangements (as mixed with N2-fixing trees), as well as conservative soil
practices are necessary to mitigate the loss of natural capital.

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Chapter 11
The Risk of Invasions When Using Acacia
spp. in Forestry

Ciro José Ribeiro de Moura, Nina Attias, and Helena de Godoy Bergallo

11.1 Aliens Welcome

Exotic tree species such as Pinus and Eucalyptus have a great impact on the Brazilian
economy, accounting for 6.1% of the Brazilian GDP in 2018 (Industria Brasileira de
Árvores, 2019). Nowadays Brazil is the third largest exporter of pulp, accounting
for 13.2% of the world market. According to IBGE (2019), planted forests currently
occupy ten million hectares, which corresponds to 1% of the country’s agricul-
tural lands.
“The climate, the soil and the technology we have in Brazil have allowed us to achieve the
highest average annual productivity in the world,” explains agronomist João Salomão, gen-
eral coordinator of Forestry and Livestock Affairs at the Ministry of Agriculture, Livestock
and Supply (MAPA).

In 2016, Brazil led the global ranking of forest productivity, with an average of
35.7 m3 ha−1 year−1 in eucalypt plantation and 30.5 m3 ha year−1 in planting pine
trees, according to data from the Brazilian tree industry (Industria Brasileira de
Árvores 2019).

C. J. R. de Moura (*)
Federal University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
N. Attias
Department of Animal Biology, Federal University of Mato Grosso do Sul,
Campo Grande, MS, Brazil
H. de Godoy Bergallo
Department of Ecology, Institute of Biology Roberto Alcântara Gomes, Rio de Janeiro State
University, Rio de Janeiro, RJ, Brazil

© Springer Nature Switzerland AG 2020 221

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_11
222 C. J. R. de Moura et al.

However, some of these genera such as Acacia and Pinus present invasive behav-
ior in some ecosystems, and it is necessary to account for and internalize these
impacts economically.
In Brazil, the impacts of all invasive species generate an annual loss of approxi-
mately US$ 50 billion per year (Pimentel et al. 2001). However, this estimation is
outdated, resulting in an underestimate of the invasion problems caused by several
species and its negative environmental and socioeconomic impacts (Rouget et al.
2016). Despite the abundant evidence and warnings of the possible impacts and
damages caused by the introduction of exotic species, they continue being intro-
duced to new locations for various purposes (Vitousek et al. 2017).
We estimate that 21% of known plant species in Brazil are exotic (Pimentel et al.
2001), including the main crops such as soybean, coffee, sugarcane, rice, corn,
oranges, bananas, coconut, and many others. To control the action of invasive exotic
species, management and eradication techniques have to be implemented (van
Wilgen et al. 2011) and are surrounded by a high degree of uncertainty, besides
elevated costs. Hence, considering the risk of invasion and the costs associated with
the control of alien species, the Convention on Biological Diversity (1992) states
that, according to the precautionary principle, the prevention of future invasions
should be the most efficient form of management.
The perception of the impact of the biological invasion is supplanted by the per-
ception of utility and generation of economic revenues from the use of these spe-
cies, which is seen as a commodity to feed the people. As a rule, the costs of the
invasion impact caused by the invasive alien species are externalized to the whole
society. Furthermore, the decision to prioritize caution and control by the society as
a whole depends on the perception and type of impact caused by the biological inva-
sion and the willingness to pay for the high control costs.
When an exotic species has been settled for multiple human generations, it
becomes part of the landscape memory and can be mistakenly recognized as native
species (Diamond 2005). One example of this is the jackfruit Artocarpus hetero-
phyllus, originally from Asia and introduced in Brazil in the sixteenth century
(Ferrão 1993). The species has been classified as Artocarpus heterophyllus by Lam.,
as published in Encyclopédie Méthodique Botanique in 1789 but, 23 years later, in
1812, the same species was misclassified as Artocarpus brasiliensis by Ortega, in
Memórias de Mathematica e Phisica da Academia Real das Sciencias de Lisboa 3:
84, portraying how the species had been incorporated into the local landscape.

11.2 Acacia Silviculture

The economic value of eucalypt was recognized from the earliest days of European
settlement in Australia, and this stimulated the transfer of seeds of many taxa around
the world. However, systematic collection and evaluation of Australian Acacias spp.
only began in the 1970s. The major agency involved was the Australian Tree Seed
Centre that dispatched samples of 322 taxa (1/3 of them Acacia spp. native to
11 The Risk of Invasions When Using Acacia spp. in Forestry 223

Australia) between 1980 and 2010 to 149 countries. Plantations in SE Asia and
South Africa supplying the pulp and paper industry also provide logs for solid wood
products (Griffin et al. 2011).
This commercially versatile genus can be used in a small scale as a resource of
firewood in rural properties or in large scale industrially (Midgley and Turnbull
2003). At local scale, it is used for landscape purposes, such as firebreaks and wind-
breaks; in the forestation of urban and rural areas; and, in consortium with other
legumes, for the reclamation of degraded soils (Carvalho et al. 1998, Faria et al.
1998, Souza et al. 2004, Balieiro et al. 2007).
Acacias as N2-fixing trees have been used in mixed plantations with eucalypt
increasing biomass productivity while maintaining the fertility, because of the more
efficient use of soils, both physically and chemically (Kleinpaul et al. 2010), high-
lighting the importance of soil enriched with symbiotically fixed N in substitution
of high doses of synthetic N fertilizer (see Chap. 6).
Acacia mangium has become a widely used species in reforestation programs in
the humid tropical plains of Asia. It also is one of the most common leguminous tree
species in plantations in the tropical and subtropical regions of southeastern China
(Midgley and Turnbull 2003, Xiong et al. 2008).
In Brazil, Acacia mangium is planted with multifunctional characteristics in a
consortium with agricultural crops and lends itself to uses in integrated forest and
livestock cultures. The first commercial plantation in Brazil was set up in 1930,
when 30 kg of seeds were imported from South Africa (Higa et al. 2009).
Around the word, this species is implemented in plantations destined to the pro-
duction of firewood (calorific value of ~4900 kcal/kg) (Sahri et al. 1998), wood pulp
(Weber et al. 2007), wood for construction, and adhesives (Hoong et al. 2009).
It began to be used in reforestation programs as a carbon sequestration plant
(Heriansyah et al. 2007, Tonini et al. 2010). In Brazil, the most common use is in
reforestation programs of land reclamation, and this use was incorporated and popu-
larized by Embrapa (the Brazilian Agricultural Research Corporation) in Brazil,
especially in the Amazon and in Rio de Janeiro states.
Finally, this tree, in addition to the various possible uses of its wood, is approved
due to its melliferous flowers; that is, its floral nectar is used by exotic bees of the
genus Apis for the production of honey (Barbosa 2002). Acacia produces a high
amount of wood with low accumulation of nutrients, being a silvicultural option in
areas with low soil fertility (Franco and De Faria 1997, Balieiro et al. 2004).
In 2006 black Acacia (Acacia mearnsii De Wild.) was the third most planted for-
est species in Brazil, surpassed only by Eucalyptus spp. and Pinus spp. (SBS, 2006).
Brazil has 9.85 million hectares of planted forests, 75.2% of which in eucalypt and
20.6% in Pinus, according to the survey Plant Production and Forestry 2017 (PEVS
in Portuguese) (IBGE, 2017).
The use of Acacia mearnsii as a raw material for tannin, cellulose, and charcoal
also presents great social importance, mostly in small properties. One strategy of
cultivation is at the beginning of the crop and, at 3 years of age, the area is trans-
formed into cattle pasture under the canopies (Mora, 2002).
224 C. J. R. de Moura et al.

From 2010 to 2016 the area planted with black Acacia species had been stabi-
lized around 149.000 (±11.85 ha) according to Ibá and Pöyry (2016).

11.3 Success for the Successful

There are approximately 1350 species of the genus Acacia (Fabaceae) distributed
worldwide (Maslin et al. 2003). We estimate that the area planted with trees of the
genus Acacia in the world in the year 2000 was close to eight million hectares (FAO
2006). Nevertheless, several factors can influence the successful establishment of an
exotic species. In most cases, only a small portion of species introduced are able to
thrive in natural environments and indeed become invasive and maintain long-term
viable populations and disperse from the area of introduction (Lockwood et al. 2001).
Australian acacias have great adaptability and rapid growth, which favors their
popularity for introduction in several countries and climatic regimes, with some
species introduced in more than 70 countries (Midgley and Turnbull 2003). However,
acacias have a consistent history of introduction followed by invasion, which, since
1900, has been recorded throughout Southeast Asia (Richardson et al. 2015), South
Africa, Hawaii (Richardson et al. 2011a), and Portugal (Fernandes et al. 2013).
Acacias possess a set of ecological characteristics that can be related to their
establishment success such as short generation time and high seed production
(Richardson et al. 2015). However, it is important to keep in mind that, as for other
exotic species, in the journey of success of the acacias, the intentional introduction
has aided the species to overcome biological filters (Groom et al. 2006), such as
biogeographic isolation and biotic conditions, through human intervention. The
probability of a successful establishment can be further increased by the fact that
foresters actively select areas where environmental conditions are similar to those in
the native ranges of the species (Richardson et al. 2015).
The genus Acacia was introduced in Brazil about a 100 years ago (Schneider
et al. 1991). Within the genus Acacia, the species A. mangium Willd. and A. mearn-
sii De Wild. are those that occupy the largest area in Brazil being used in activities
such as forestry, land reclamation, and urban and rural afforestation (Attias et al.
2014). In Brazil A. mangium has shown a cycle of 8–15 years, and although it has
not been invasive in areas already vegetated, either under forest or planted pasture
(Franco 2018) under native environments such as the savannas of the state of
Roraima, and oligotrophic soils, this species has shown an invasive character
(Aguiar Jr et al. 2014).
Other species were also brought to Brazil, as Acacia auriculiformis A. Cunn. ex
Benth. and Acacia holosericea A. Cunn. ex G. Don., and were very successful in
their establishment as well.
Coincidently, or not, those are the acacia species most frequently recorded in the
regional lists of invasive alien species in Brazil (Attias et al. 2014). The Horus
Institute, a Brazilian NGO dedicated to the invasive species study and control, eval-
11 The Risk of Invasions When Using Acacia spp. in Forestry 225

uated A. holosericea as of high risk of invasiveness in a calculation of the risk of

introduction.
According to Balieiro and Tonini (2018), the first experimental mixed planta-
tions with A. mangium were carried out in 1979 by the Brazilian Agricultural
Research Corporation (Embrapa) in Colombo (Paraná) and, in 1985, plantings were
­established in Minas Gerais. Around 1993, the Embrapa center at Seropédica (Rio
de Janeiro) established the first experimental plantations with the species, which
culminated later in the pioneering of that research center in the restoration of
degraded areas in Brazil.
In the southeastern states in Brazil, Acacia spp. were planted for several purposes
as afforestation of roads or highway, landscaping, soil conservation, and land recla-
mation. Since that time, technicians and specialists noticed the behavior of the spe-
cies in invading open environments in a very aggressive way, beyond its planting
areas (Balieiro, personal communication).
In Brazil, these species have been recorded in areas adjacent to their introduction
sites (Mochiutti et al. 2007, Aguiar Jr et al. 2014). Plantations consist of a continu-
ous source of dispersing individuals, increasing the chance of invasion by the spe-
cies in adjacent areas. Furthermore, the anthropogenic disturbance generated by
plantation management activities can modify the environmental conditions and
facilitated the invasion process in these areas. However, the organized introduction
of acacias in Brazil, by itself, does not explain all the success in the establishment
in the new environment.
Some other ecological characteristics can be ascribed to them as their ability to
define much of the structure of a new community as a foundation species (Ellison
et al. 2005), keystone species (Mills et al. 1993), and ecosystem engineer (Ellison
et al. 2005) and probably it is most consistently determined by their propagule pres-
sure (Lockwood et al. 2005, Cassey et al. 2018).
Nowadays the evaluation of the risk of invasion of these species is already done
by the NGO Horus Institute (2018) providing support for prevention strategies to be
adopted before these species cause significant damage in new areas in Brazil, as
they already do in other countries (Richardson and van Wilgen 2004).
Moreover, according to the National Database of Invasive Alien Species I3N in
Brazil, the genus Acacia is spread across 11 states. The database indicates invasions
at different levels by Acacia auriculiformis, Acacia farnesiana, Acacia holosericea,
Acacia longifolia, Acacia mangium, Acacia mearnsii, and Acacia podalyriifolia.
It is important to consider that in their native environment in Australia, the spe-
cies of the genus Acacia occupy a wide variety of environments, but are particularly
prevalent in arid, semiarid, and subtropical dry regions. The seeds are produced in
large quantities and have the capacity to remain viable for long periods (ABRS
2001). Acacia mangium, however, has very small and not very competitive seeds
when competing with already established vegetation.
Acacia species as other plants known for their histories of introductions to new
habitats by humans are in the selected group of species that easily become domi-
nant. This can be attributed to their escape from specialist consumers and release
from enemies, which is also thought by some researchers to lead to the evolution of
226 C. J. R. de Moura et al.

increased competitive ability, driven by a decrease in the plant’s resource allocation

to consumer defense and an increase in allocation to size or fecundity (Callaway
and Ridenour 2004).
In Brazil, the deliberate introduction of acacia species for multiple purposes pos-
sibly influenced the success of the species. In this sense, the propagule pressure is a
determinant for the establishment and success of alien species. The number of indi-
viduals introduced to find a new population may have surpassed any obstacle or
competitor in favor of the establishment of the acacias (Cassey et al. 2018).
A well-documented case of introduction occurred in 1998, when A. mangium
was introduced in Roraima as an experimental planting of a thousand seedlings.
Due to the apparent success of this planting, Walter Vogel founded Ouro Verde
Agrosilvopastoril Ltda. (OVA) and started to invest in commercial acacia forestry in
the Boa Vista, RR region, from 1999 (Forest Management Plan—Ouro Verde
Project 2007).
During the process of establishing the company, Walter Vogel donated 100 seed-
lings of A. mangium to each public school in Boa Vista. Parts of these seedlings were
planted within the school grounds and another part distributed to parents and school
employees. Thus, because it provided efficient shading, the species was quickly
accepted by the residents and disseminated through the city (Isabela Coutinho, resi-
dent of Boa Vista, personal communication), facilitating the invasion process.
In 2007, 80,866 ha of savannah land was occupied by the activities of the OVA
company, of which 26,757 ha were planted with acacias, and the production capac-
ity of A. mangium sawmills was estimated at 10,000 m3/year (Forest Management
Plan—Ouro Verde Project 2007).
As part of the preparation process of the A. mangium planting area, Cajanus
cajan (L.) Millsp.), another exotic and invasive species in other regions, was planted
with a function of wind breaking for the seedlings, facilitating the vertical growth of
acacia seedlings.
According to the OVA Management Plan, in recognition of the invasive potential
of A. mangium, a task force was created to once a year clean up all watercourses of
the farms of the company of invasive vegetation of this species (Management Plan
Forestry—Ouro Verde Project 2007). However, these measures have not been shown
to be totally effective, with A. mangium occurring spontaneously outside the planta-
tion area (Aguiar Jr et al. 2014).

11.4 But Why?

Popularly known in Brazil as Australian Acacia, A. mangium, or even only Acacia,

it has a dense crown and white flowers and can reach up to 30 m in height (Lorenzi
et al. 2003, Midgley and Turnbull 2003).
In plantations, flower and seed production starts at 2 years of age and mature
pods can be observed 7 months after flowering. Flower pollination occurs by insects,
mainly by bees (Midgley and Turnbull 2003). The fruits are spiral-shaped pods,
11 The Risk of Invasions When Using Acacia spp. in Forestry 227

which contain small black seeds that remain in the mature pods fixed by an orange
aryl and which are dispersed naturally by wind and birds (Kull and Rangan 2008).
In natural habitat, A. mangium individuals are concentrated in lowland coastal
areas at altitudes of up to 300 m. They grow on the banks of closed forests, in open
forests, woods, and especially areas disturbed by fire (Midgley and Turnbull 2003).
The initial growth rate is directly proportional to the light incidence, reaching its
maximum in open areas. Many physiological characteristics define A. mangium as
a pioneer species that is fast growing and with ease of establishment in a wide vari-
ety of environmental conditions, especially in humid tropical areas (Tong and
Ng 2008).
Other characteristics of this species favor its dominant establishment in many
places as, for example, the ability to shade competitors quickly, the reduced amount
of potential pathogens, and the ability to capture large amounts of rainwater associ-
ated with essential nutrients in the runoffs of the trunk. High tolerance to soils that
are compacted and very acidic (pH 4.2–6.5) and have low nutrient concentration
also contributes to this facility (Lorenzi et al. 2003, Midgley and Turnbull 2003,
Balieiro and Tonini 2018).
These characteristics guarantee to this species a great competitive potential in
environments under water stress and conditions of low soil fertility (Faria et al. 1998,
Balieiro et al. 2007). It is important to note that these same characteristics (e.g., large
seed production, rapid initial growth, and shading capacity of competing species) are
common features of invasive alien species (Rejmánek and Richardson 1996, Castro-
Diez et al. 2011). However, as commented before, its small seeds are not very suc-
cessful in establishing at seedlings stage competing in areas densely vegetated.
Despite all characteristics mentioned above, a special one that gives to Acacia
species a great competitive advantage is the ability to grow on low-nitrogen soils
due to the biological property of forming symbiosis with rhizobial bacteria
(Duponnois and Plenchette 2003).
This is especially important in extremely adverse situations found in heavily
degraded soils that have lost their upper horizons, where the physical and chemical
factors are too restrictive for plant growth. Acacia symbioses with nodulating N2-­
fixing bacteria and arbuscular mycorrhizal fungi constitute an efficient strategy to
accelerate soil reclamation and initiate natural succession (Chaer et al. 2011, see
also Chaps. 6 and 7).

11.5 Acacia and Its Interactions

Complex interactions can be generated as a result of the introduction of exotic

plants into a new community. These interactions can cause disturbances in several
environmental variables, affecting species, communities, and ecosystems
(Richardson et al. 2011a, b, Vilà et al. 2011). In this context, the form and intensity
with which an exotic species affects the physical, chemical, and biological environ-
ment are described as disturbance (Richardson et al. 2011a, b).
228 C. J. R. de Moura et al.

A. mangium plantations are often responsible for changes in various edaphic

attributes. Studies conducted in Thailand have indicated that soil moisture within an
acacia planting is lower than adjacent open areas, indicating a high rate of water
consumption and competition among individuals for this resource (Sakai and
Thaingam 1998 cited in Kamo et al. 2009). The concentration of nutrients in these
environments can also be altered. Peak plant growth is capable of rapidly absorbing
large amounts of nutrients, which can deplete the soil and limit the growth of indi-
viduals at advanced ages (Tong and Ng 2008, Nykvist and Sim 2009).
Soil acidification is common under cropping systems depending on N2 fixation
as a source of nitrogen if parts of crop removed contain large quantities of bases. For
Nambiar et al. (2014) the effect of Acacia spp. in acidifying soils is questionable
because of the confounding problems in the design of the studies. The pH fluctua-
tion in time (or the moment of soil sampling) and the use of a pasture, abandoned
land, or forests as reference treatments are some of those factors. In the case of
A. mangium, if harvest residues and litter are maintained, the only removal of poles
should not affect too much the soil pH (Franco, A. A., personal communication).
The amount of litter accumulated in the soil is influenced mainly by the amount
of organic matter produced by the plants associated with the litter decomposition
rate (Garay et al. 2003). A. mangium adult individuals do not have leaves but rather
flat stems, called phyllody, with leaflike appearance. When they fall, these phyl-
lodes decay very slowly, accumulating in the litter (Balieiro et al. 2004, Kull and
Rangan 2008). The reduction of litter decomposition rate is a common disturbance
in invasion processes (Vilà et al. 2011), but very desirable as a soil conditioner in
tropical soils for sustainability of the system.
When compared decomposition rates were slower for acacia residues than for
Eucalypt residues despite initial higher N and P concentrations in the Acacia resi-
dues. The decomposition rates depended on the carbon quality of the litter, primar-
ily in terms of water-soluble compounds and lignin, and on the P availability
(Bachega et al. 2016).
In mixed plantations of eucalyptus and Acacia the niche separation of the fine
root system’s architecture and distribution in the soil horizons, associated with the
capacity of biological symbioses with nodulating N2-fixing bacteria and the differ-
ent dynamics of phosphorus, can be beneficial for both species (Balieiro, personal
communication).
Parrotta and Knowles (1999), in a study of the Brazilian Amazon region, found
that a higher litter accumulation and slower humus-layer formation in the natural
regeneration and mixed native species plots are due to the relatively slow decompo-
sition of the dominant species in these stands, when compared to other treatments,
as Cecropia spp., or Eucalyptus spp. mixed with Acacia mangium in the mixed
commercial species treatment. These trends may reflect treatment differences in the
development and activity of litter invertebrate communities and other litter decom-
posers, a topic meriting further research.
The accumulation of litter under individuals of A. mangium benefits the recovery
of degraded areas by protecting soil from erosion, soil temperature fluctuation, and
increasing nutrient reserve (Balieiro et al. 2004). However, this accumulation may
11 The Risk of Invasions When Using Acacia spp. in Forestry 229

also be responsible for increased propensity for burning and inhibition of native
seed germination (Parrotta and Knowles 1999, Balieiro et al. 2004, Kull and
Rangan 2008).
The modifications observed in the soil can have influence not only on the local
vegetation, but also on the edaphic fauna (see Chap. 8). Tsukamoto and Sabang
(2005) reported the simplification of the structure of the macroinvertebrate soil
community in a 14-year plantation in Malaysia. Compared to the adjacent native
forest area, the acacia plantation had a total biomass four times higher, but with a
different taxonomic composition and lower diversity. It is interesting to note that
one of the dominant species of this community is a species of exotic earthworm that
probably was also introduced during planting (Tsukamoto and Sabang 2005).
Another important aspect on soils and soil-fauna is the allelopathic effects attrib-
uted to the Acacia species (Lorenzo et al. 2008, Lorenzo et al. 2010). Callaway and
Ridenour (2004) proposed that invaders with allelochemical substances have com-
petitive advantages in their new habitats, which they named as “allelopathic advan-
tage against resident species” hypothesis or “AARS.”
The same experience as reported in Brazil is also reported in the rest of the
world, accordingly with the International Union for Conservation of Nature (IUCN),
about several environmental disturbances caused by the introduction of acacia and
eucalyptus in Bangladesh since the 1980s. These include competition with native
flora, high water consumption, reduction of soil fertility due to the deposition of
slowly degradable leaves, inadequacy of their fruits and nectar for the consumption
of native fauna, and production of pollen with a potential negative effect on the
human respiratory tract (Barua et al. 2001).
Back to Brazil, in Roraima, 3- and 4-year plantations were responsible for the
disappearance of native herbaceous vegetation through shading. In this same region,
a large increase in the density of exotic bees of the genus Apis sp. (Barbosa 2002)
was observed. This high density of bees harms the hunting and extraction activities
of the indigenous populations that occupy lands near the plantations, generating
complaints from them (C. Castilho, personal communication). On the other hand,
an experiment of reclamation of mining residue, conducted in Porto Trombetas,
Pará state, in a forest predominating matrix, has shown that, after 10 years of plant-
ing, several introductions of A. mangium have died out completely and have been
replaced by a diverse and much superior biomass production than the plots planted
with Eucalyptus spp. and that no seedling or plant of A. mangium was observed in
the forest nearby (Campello 1999, Franco 2018).
In savanna areas adjacent to plantations in the state of Roraima, the spontaneous
occurrence of adult reproductive A. mangium individuals was observed. In this loca-
tion, the species density was inversely proportional to the distance of the source
area, with 900 m being the maximum distance of dispersion observed (Aguiar Jr
et al. 2014). According to Richardson et al. (2000), a species may be considered
invasive if it is able to generate new reproductive individuals at a distance of more
than 100 m from the source individuals in a period of less than 50 years. Thus, the
study conducted by Aguiar Jr et al. (2014) shows that this species has invasive
behavior in the Cerrado region of Roraima. After only 9 years of planting, A. man-
230 C. J. R. de Moura et al.

gium was able to disperse over long distances and reach the reproductive stage
(Aguiar Jr et al. 2014). The same study found the presence of Acacia mangium
individuals up to 900 m from the plantation edge 8–9 years after its introduction,
independent of life stage or establishment pattern, indicating that this species can
naturally disperse over long distances in open areas as natural Amazonian savanna.

11.6 We Are Not Alone: The Pity Comes by Horseback

The black acacia (A. mearnsii) is included in the list of the 100 “worst” invasive
species in the world according to IUCN (Lowe et al. 2000); the invasion of natural
environments by black acacia has not been extensively tested in Brazil, as in other
parts of the world, even though it has been planted and used in the South for
many years.
In Brazil, this species is found frequently in disturbed environments adjacent to
crops, along roadsides and even in protected areas as parks and reserves. In Rio
Grande do Sul, it was recorded as invasive in rural environments near cultivated
areas. However, because it is a pioneer plant with high light demand, it is not able
to establish itself in shady environments, areas of forest, or savannas (capoeiras in
Portuguese) (Mochiutti et al. 2007). In this same Brazilian state, Nardelli (2004)
recorded occurrences of black acacia in the natural ecosystems adjacent to planta-
tions. The environment of black acacia plantations in Rio Grande do Sul is com-
posed of areas of natural pasture, plains, areas of agricultural cultivation, field areas,
regrown natural vegetation, called “capoeiras,” and open environments with light
availability, suitable for the establishment of the species.
In Paraná state, also located in the south of Brazil with a subtropical climate,
A. mearnsii was recorded as an invasive species within the Vila Velha State Park
(PEVV). At this site, black acacia is found in abundance in areas reforested with
Eucalyptus spp. and in areas of intensive use (Carpanezzi 2011).
Given the increase in the number of individuals of Acacia and other exotic inva-
sive tree species, as Pinus elliottii and Pinus taeda in the PEVV (Carpanezzi 2011),
the Environmental Institute of Paraná, in partnership with other organizations, man-
aged to promote the withdrawal of 50,000 trees from invasive alien species in 2007
(www.institutohorus.org.br/pr_vilavelha accessed 12/01/2019).
The invasion process of A. mearnsii has been responsible for several disturbances
in the water balance and edaphic conditions of the invaded sites, affecting local
biodiversity and economy (Moyo and Fatunbi 2010). This species has very high
levels of water consumption, even when compared to other species of Acacia. This
is due to its high rate of evapotranspiration and great capacity to capture rainwater
and soil nutrients (Jobbágy and Jackson 2003). In South Africa, researchers esti-
mate that the damage caused by this high water consumption is $ 2.8 million per
year (Moyo and Fatunbi 2010). Also in South Africa, Richardson and van Wilgen
11 The Risk of Invasions When Using Acacia spp. in Forestry 231

(2004) observed that, in riparian environments, commonly colonized by this spe-

cies, this has a direct consequence in the reduction of the flow of streams.
The canopies of the black acacia, besides shading smaller species, like light-­
dependent grasses, produce large numbers of leaves. These are deposited in large
quantities on the litter and, after their decomposition, can modify the composition
of nutrients and minerals of the soil. It was observed that soils in areas dominated
by black acacia are drier and more acidic (pH 4.4) when compared to natural areas
of grasses (pH 5.3) (Moyo and Fatunbi 2010). The association of these factors, such
as the change in chemical composition of the soil, the shading of open areas, and the
large layer of litter formed by this species, tends to make it difficult to establish
seedlings of native species and, consequently, process of natural succession.
The biological characteristics of A. mearnsii, such as the large production of
small seeds and the short juvenile phase, allow it to disperse and colonize open
areas rapidly. This combination of strategies, among others, makes it an aggressive
invader (Rejmánek and Richardson 1996). This species has been recorded as an
invasive species in several countries, with the most alarming cases being recorded
in South Africa and Hawaii, USA (Daehler and Carino 2000, Richardson and van
Wilgen 2004, Henderson 2007, Moyo and Fatunbi 2010).
Currently, A. mearnsii can be found in the following 42 countries: Afghanistan,
Albania, Angola, Bangladesh, Bosnia and Herzegovina, Botswana, Brazil, Bulgaria,
China, Colombia, Croatia, Eritrea, Ethiopia, Indonesia, Iran, Italy, Japan, Kenya,
Lesotho, Malawi, Malaysia, Mexico, Mozambique, Myanmar, Namibia, New
Zealand, Nicaragua, Pakistan, Panama, Papua New Guinea, Portugal, Romania,
South Africa, Sri Lanka, Swaziland, Tanzania, Thailand, Uganda, the United States,
Vietnam, Zambia, and Zimbabwe (www.worldagroforestry.org accessed on
07/03/2019).
Black acacia has been officially declared an invasive species in South Africa
since 1984. In this country, it is estimated that more than 2.5 million hectares have
already been invaded by the species, which is called “green cancer” (Galatowitsch
and Richardson 2005).
In African biomes, the species mainly invades areas where there are fires, which
stimulate the germination of seeds accumulated in the seed bank (Midgley and
Turnbull 2003, Mochiutti et al. 2007, Moyo and Fatunbi 2010). In Hawaii, black
acacia has invasive behavior and propagates easily in regions between 600 and
1200 m altitude, with rainfall between 1000 and 1200 mm.
It was only in the late 1930s that 65,000 individuals of this species were intro-
duced into conservation areas in Hawaii. These individuals should be the progeni-
tors of the invading individuals currently found, not only within conservation units
but also in other natural environments (Little Jr. and Skolmen 1989, Stone et al.
1992, Frohlich and Lau 2008).
But things can be worse if acacia is planted associated with Leucaena leuco-
cephala (Santos et al. 2009), another legume tree species on the list of 100 worst
invasive species (Lowe et al. 2000) or other aggressive species.
This chapter presented several case studies in countries that recognized and stud-
ied the invasive potential of acacia genera, well documented in scientific literature
232 C. J. R. de Moura et al.

accumulated over the decades. It is important to consider that we have in Brazil

similar environmental conditions to those areas spread across the globe, especially
in the tropics and even in Europe. Similarities in the history of invasion by acacia
species when the weather and local conditions are favorable for their occurrence
may produce the same patterns of invasion, which can happen here in Brazil or, may
be, is already happening.

11.7 Conclusions: In Doubt Do Not Overtake

Australian acacias have several characteristic attributes of invasive species. These

attributes are considered advantageous in the establishment, dispersal, and popula-
tion growth phases (Rejmánek 1996, Rejmánek and Richardson 1996, Pysek and
Richardson 2007). In addition, these species occupy an extensive geographical area
in their native distribution in Oceania, being adapted to a wide range of climatic
conditions.
This characteristic favors the establishment of these species in the introduction
regions, especially in the tropics and subtropics possibly because these species have
a higher capacity to overcome abiotic filters (Castro-Díez et al. 2011). Besides
these, several other physiological and biological characteristics of both species are
favorable to establishment and invasion.
The invasion process can be influenced equally by factors extrinsic to the spe-
cies, such as the time elapsed since introduction and the number of forms of use
(Pysek and Richardson 2007, Castro-Díez et al. 2011). The most serious problems
related to invasion are caused commonly by species widely cultivated for long peri-
ods of time (Richardson 1998). The information compiled in this study demon-
strates that A. mangium was introduced in the Brazilian territory more than 30 years
ago (1979) and A. mearnsii approximately 100 years ago (1918), both being used
for several purposes, and reports of them being invasive under our conditions until
now are not very generalized.
Castro-Díez and his collaborators (2011) observed that the number of forms of
human use is the most predictive feature of the distribution and abundance of
Australian acacias in South Africa, where exotic acacias with the greatest number of
uses were proven to be the most abundant and widely distributed. In addition, exotic
species introduced through cultivation exert constant pressure of propagules due to
the periodic introduction of new individuals. This fact increases the chances of the
introduced species to find environments suitable for colonization, besides reducing
the influence of environmental heterogeneity as a filter for the establishment of spe-
cies (Wilson et al. 2009).
In this context, the set of characteristics of the studied species shows its potential
invasion in Brazil and in the world. According to Nardelli (2004), Mochiutti et al.
(2007), and Aguiar Jr et al. (2014), there are invasion records of Acacia spp. in sev-
eral Brazilian regions as Amazonian savanna (3° north latitude), Brazilian lowland
11 The Risk of Invasions When Using Acacia spp. in Forestry 233

Atlantic Forest in southeast in Espírito Santo state (19° south latitude), and grass-
lands (30° south latitude) in the Rio Grande do Sul state.
These are similar to invasion histories of these species in other regions of the
world (Daehler and Carino 2000, Barua et al. 2001, Richardson and van Wilgen
2004, Henderson 2007, Moyo and Fatunbi 2010), where they have been used for a
longer time, which may serve as an alert. In regions already extensively invaded by
these species, such as South Africa, major economic and ecological damages have
been reported. The Working for Water program, developed in South Africa, has
invested more than US$ 125 million in the mechanical removal of Australian acacia
trees in an area of 135,000 ha between 2000 and 2010. However, this program did
not obtain success in the eradication or population reduction of the target species in
all regions of the action (van Wilgen et al. 2011).
In order to prevent Brazil from having similar losses, preventive and control
measures should be adopted, especially in the vicinity of the introduction areas
(Richardson and Thuiller 2007). One trend observed in the study of the invasion
process is that disturbed environments tend to be more susceptible to invasion
(Pysek and Richardson 2007). Areas adjacent to commercial plantations are often
deprived of their original vegetation and suffer from various disturbances associated
with the management of plantations, such as the movement of machines.
Similarly, areas where species are introduced for the reclamation of degraded
soils also tend to be altered environments, especially due to low species diversity. In
this sense, these areas would be adequate for the beginning of the process of disper-
sion and establishment of the exotic species.
The most controversial management issues involve species that have invading
behavior, causing serious damage and at the same time providing economic and
ecological benefits in specific situations and areas. Australian acacias fit this profile
and are managed in different ways in different countries. In South Africa, the plant-
ing of Australian acacia for commercial purposes is permitted in demarcated areas.
However, all owners are responsible for controlling the dispersal of the species
around their lands (van Wilgen et al. 2011).
A strategy to avoid dispersal of species from their places of introduction would
be the “encircling” of commercial plantations by native species to the region in
question, of fast growth and with great capacity of shadowing. Since both species
have high affinity and similar dependence on light, especially in the initial stages of
growth, the shading of the perimeter of the plantation could inhibit the germination
of the seeds dispersed in the adjacent areas. The maximum dispersion distance of
the species should be used as a parameter to define the width of this planting of
native species.
In cases where the invasion process has already begun, measures to control inva-
sive populations need to be adopted. In South Africa, young invading individuals are
pulled out manually while adult individuals are mechanically cut and treated with
herbicides (Garlon 4 or Timbrel) (Dahl et al. 2001). Adult individuals located in
areas with steep slopes are ringed to reduce the risk of erosion due to the removal of
trees (Department of Water Resources Republic of South Africa—http: //www.
dwaf.gov.za/wfw/Control/). Due to the large number of seeds accumulated on the
234 C. J. R. de Moura et al.

soil and the permanence of plant structures, such as stumps and roots, the removal
of individual trees is followed by controlled burning of the region. This process, in
addition to inhibiting regrowth, breaks seed dormancy and stimulates their germina-
tion. In this way, the seed bank is reduced and the new seedlings can be removed
manually. Considering that invasion of riparian environments by these species is
common, the use of herbicides should be cautious, since some of its components
may persist in the environment for prolonged periods and contaminate water
(Dahl et al. 2001).
Correia and Martins (2015) found the presence of Acacia mangium in the soil
seed bank of a previously native forest area, which followed a reforestation project
that contemplates the eradication after the period of planting and after a final clear-­
cut. This corroborates the proposal that the use of alien species in forestry processes
may be, in part of the cases, the risk of contamination for the remaining ecosystems,
proving that they can invade native forests.
The good notice that emerges from Correia and Martins (2015) is the low seed
density of Acacia mangium that germinated under the canopy of this forest with a
restoration project. It is plausible and may be inferred that the species is leaving the
system for not finding sufficient light levels for germination and establishment.
However, the presence of a few seeds on the native forest seed bank illustrates well
the problem of the use in forest restoration projects with certain alien invasive spe-
cies that may contaminate nearby preserved ecosystems.
In this sense, another ecological characteristic of Acacia mangium arises, that is,
the short life cycle. A personal and empirical observation of a restoration project
was conducted in the Piraí municipality, located in SE Brazil over the last two
decades, close to the margins of a power plant water reservoir, where the area
planted in the 1990s is nowadays almost gone after the trees’ dieback. However, the
clearings opened by the acacias’ death after approximately 25 years after planting
are not being colonized by native species, even in the presence of a source of propa-
gules of native species in the forest patches on surroundings.
Considering that planting acacias is a consolidated activity in Brazil, the devel-
opment of national invasion prevention strategies becomes indispensable. The cre-
ation of public policies to reduce the use of these species and regulate their
management is essential. Its use for landscaping and the recovery of degraded areas
proved to be inefficient and inadequate due to its invading status and should be
replaced by native fast-growing species.
Its cultivation for commercial purposes must be regulated, with new policies to
delimit the areas of planting and to control the invasion in the surrounding areas,
following the example of South Africa. Within this regulation the responsibility of
the entrepreneur for the containment and periodic control of the invasion (polluter
pays principle) should be highlighted. In addition, detailed records and studies of
control of these species in Brazil are required. This type of material is still scarce
and not detailed. However, considering that invasion control is much more expen-
sive in comparison to prevention (Thuiller et al. 2005, Richardson and Thuiller
2007, Broennimann and Guisan 2008) and that the invasion process in Brazil is
11 The Risk of Invasions When Using Acacia spp. in Forestry 235

Table 11.1 Examples of Brazilian native species, which can be used as alternatives to Acacia
species for multiple purposes
Acacias Brazilian native species
Use or resource Species equivalent References
Firewood Piptadenia gonoacantha Hansted et al. (2016)
Reforestation programs Anadenanthera peregrina Suganuma et al. (2014);
Bombacopsis glabra Rodrigues et al. (2009)
Centrolobium tomentosum
Citharexylum myrianthum
Dalbergia nigra
Peltophorum dubium
Trema micrantha
Xylopia brasiliensis
Carbon sequestration plant Multiple species Brancalion et al. (2018)
Melliferous Mabea fistulifera, Croton sp. Oliveira et al. (2004)

already under way (Aguiar Jr et al. 2014), it is necessary that these control measures
be systematized with urgency, based on the information available in Brazil and
the world.
Although control is of importance, it is highly important to consider the socio-­
environmental interactions among local people and invader species. Regardless of
local people considering the presence and the utility of those species as being
­positive because of their use as firewood, charcoal, wood, or even a crop, a scientific
control will be necessary.
In this sense, Shackleton et al. (2019) recommend that policymakers and manag-
ers need to be more reflexive about the ways in which environmental problems are
framed and to put those frames more in conversation with local people’s experi-
ences in order to productively resolve invasive species management dilemmas.
We propose that it is necessary to investigate the use of equivalent native species
as a resource for the substitution of exotic trees, as shown in Table 11.1.
Therefore, the discussion about the use or not of exotic species that can be inva-
sive still is in vogue. In this sense, an important question remains: Why use exotic
species in a mega diverse country? The book “Ecological Imperialism by Crosby
(2004) discusses the biological invasion of the new lands by what they call the “por-
table biota”: the set of animals, plants, and diseases that have shipped with the
Europeans in the caravels and risk and their analysis in the context of fifteenth cen-
tury. Hence, after all consequences and all science produced should we still be
doing the same thing in the twenty-first century?
In short: Acacias present a great invasive potential, especially in environments
with water stress, and where soils are shallow or of low fertility. For being helio-
philic, needing high light incidence, they are also competitive with native species in
open areas, dominated by ground vegetation. This occurred with Acacia mangium
in sites of Cerrado (Brazilian savannah) in Roraima and Amapá. The same is true for
other acacias and different exotic species, as Elaeis guineensis, Casuarina equiseti-
folia, and Pinus elliottii among others.
236 C. J. R. de Moura et al.

Thus, acacias have a high invasive potential in open areas, as the Brazilian
Cerrado, and should not be recommended in this biome. Nevertheless, they show a
low invasive potential in forested areas and pastures, where they cannot compete
with established vegetation.
Lastly this chapter is not a monolith engraved with biological xenophobia argu-
ments. We are not proposing to ban or leave out introduced species as coffee, wheat,
orange, sugar cane, corn, bananas, eucalyptus, pinus, acacias, most pasture grasses,
and many other diverse sources of food but its mandatory to all technicians keep in
mind, the intrinsic responsibility on the risks involved in the management of an exotic
species, especially those with a large repertoire of invasions across the globe, in order
to conserve and preserve local environments as mentioned throughout this chapter.

Acknowledgments CJRM thanks the Coordination of Superior Level Staff Improvement for the
doctorate scholarship, NA thanks the National Council for Scientific and Technological
Development for the master’s scholarship and H.G.B. thanks Carlos Chagas Filho Foundation for
Research Support of the State of Rio de Janeiro, National Council for Scientific and Technological
Development, and Prociência/UERJ for research grants.

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Chapter 12
Multifunctional Mixed-Forest Plantations:
The Use of Brazilian Native Leguminous
Tree Species for Sustainable Rural
Development

Antonio Carlos Gama-Rodrigues

12.1 Introduction

As a result of global climate change, declining biodiversity, increasing soil degrada-

tion, and diminishing water resources, there has been a growing recognition of the
relevance of mixed-species plantations for sustainable rural development, integrat-
ing actions to ensure water security, energy, and food, in such a way that this forest
system can be considered an adequate technique of climate-smart forestry. In this
context, there is evidence that mixed-species plantations have high potential to
achieving higher productivity than monocultures (Binkley 1992; Wormald 1992;
Petit and Montagnini 2006; Kelty 2006; Gama-Rodrigues et al. 2007; Piotto 2008;
Piotto et al. 2010; Pretzsch et al. 2017). However, there are limited examples of suc-
cessful mixed-species plantations, especially mixtures with indigenous tropical tree
species (Liu et al. 2018). In Brazil, successful mixed-species plantations have been
with fast-growing, exotic, and low-density wood species such as Eucalyptus and
Acacia (Bouillet et al. 2013; Chap. 2), while studies on mixtures of N2-fixing and
non-N2-fixing native tree species are still quite scarce, despite the high diversity of
tree species in all forest types that make up the various Brazilian biomes.
Thus, this chapter focuses on the Brazilian experience, complemented with other
experiences in tropical and subtropical countries, on the potential of mixed-species
plantations with native tree species and N2-fixing leguminous species for timber and
non-timber products, for the reclamation of degraded lands and for environmental
services.

A. C. Gama-Rodrigues (*)
Darcy Ribeiro State University of Norte Fluminense, Campos dos Goytacazes, RJ, Brazil
e-mail: tonygama@uenf.br

© Springer Nature Switzerland AG 2020 241

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_12
242 A. C. Gama-Rodrigues

12.2 Planted Forests

The forest plantations in several regions of Brazil are basically with Eucalyptus and
Pinus, but in recent years native and other exotic tree species have been widely
used. Currently, the area of forest planted with other species occupies 521.1 thou-
sand ha, corresponding to 7.3% of the total area of existing forest plantations. The
species Acacia mangium (acácia), A. mearnsii (acácia negra), Hevea brasiliensis
(seringueira), Tectona grandis (teca), and Schizolobium parahyba var. amazonicum
(paricá) are established in greater planted area, accounting for 83.4%. Of this total,
only Schizolobium parahyba occupies a planted area of 87,901 ha, accounting for
16.9% of the total area of plantations with other tree species in Brazil (ABRAF
2013; Cordeiro et al. 2015). Schizolobium parahyba has been planted commercially,
around 20,000 ha, in the states of Acre, Mato Grosso, Pará, Rondônia, Maranhão,
and Tocantins. However, these monospecific plantations with a non-N2-fixing
legume species are usually very heterogeneous and irregular and apparently the
results obtained are not satisfactory (Carvalho 2007). As a result, this tree species is
used in mixed-species plantations, particularly by association of Cordia goeldiana
(freijó) and Swietenia macrophylla (mogno) (Cordeiro et al. 2015), and also as a
shade tree in coffee or cacao plantations in Rondônia and Pará. The planted area of
Acacia mangium and A. mearnsii, both N2-fixing legume species, is 148.3 thousand
ha, concentrated in the states of Amapá, Mato Grosso, Paraná, Roraima, Rio Grande
do Sul, and Amazonas (ABRAF 2013). A. mearnsii is planted commercially in
mixed stands with Eucalyptus sp. in Rio Grande do Sul, while A. mangium is also
used mostly in mixed stands with eucalypt or in ecological restoration areas.

12.3 Mixed Plantations Including Native Species

Brazil has many leguminous tree species which are suitable to produce timber and
other products. Knowledge of the functional ecological traits of this tree species
group is important to ensure the sustainability of the mixed-species plantations. One
of the most important specific attributes is the ability of some species to associate
with diazotrophic N2-fixing bacteria (see Chap. 6). In this case, the Atlantic Forest
has 469 species of leguminous trees identified, but only 174 species have positive
nodulation registration by N2-fixing bacteria (Canosa et al. 2012).
The species that compose the Atlantic Forest fragments showed different abili-
ties to absorb nutrients (Leão and Silva 1991; Cunha et al. 2009). When these native
tree species were implanted in monocultures, they caused changes in soil physical,
chemical, and microbiological properties, differentiating them markedly from the
soils under natural forest (Silva 1988; Gama-Rodrigues et al. 1999; Gama-Rodrigues
and Barros 2002; Gama-Rodrigues et al. 2008; Gama-Rodrigues et al. 2011a). In
these forest plantations, litterfall is season dependent and its decomposition rates
are variable (Vinha and Pereira 1983; Vinha et al. 1985; Gama-Rodrigues et al.
2003). Further, the trees grow very slowly in height and diameter for the first
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 243

15 years after planting (Vinha and Lobão 1989). An alternative, therefore, to native-­
species monocultures in tropical regions, both for the reclamation of degraded soils
and timber production, is mixed-species plantation systems, which can promote
ecophysiological conditions favorable to higher tree growth in addition to providing
improvements in soil structure and increasing organic matter content and nutrient
availability (Gama-Rodrigues et al. 2007). This type of forest system aims to maxi-
mize the ecophysiological attributes of native tree species when in their natural
environment.
Based on this, the general hypothesis is that native tree species, when removed
from the natural forest and placed in pure plantations, would not present an ade-
quate form (accentuated cymose branching) to commercialize and would always
grow below the expectation. There are several reasons for a better development of
the native tree species in mixed plantations, as a relatively constant litterfall rate
throughout the year, the more varied kinds of litter and of nutrient transfer through
litterfall, and the diverse quality of the litter components, leading to a more uniform
decomposition rate, besides the complementary role of the different tree species in
nutrient uptake, resulting in improved soil fertility (Gama-Rodrigues et al. 2007). A
mixed-species plantation reproduces the complex interactions of a natural forest. In
such an ecosystem, collective and emergent properties are manifested simultane-
ously (Salt 1979; Odum 1983). The continuous litterfall rate in the mixed-species
plantation is a collective property of the tree species on the site. The litter decompo-
sition rate represents an emergent property, due to the interaction of decomposition
processes of its components and not only of the total sum of the individual rates of
the tree species (Gama-Rodrigues et al. 2003). Thus, the complementary interac-
tions overlap with those of competition, providing greater stability to the forest
ecosystem. Therefore, priority for the establishment of a mixed planting is the com-
bination of species with complementary ecophysiological attributes, such as species
with high nutrient cycling rates together with species of high nutrient-use efficiency
(Gama-Rodrigues et al. 2007). In this sense, some N2-fixing leguminous tree spe-
cies in the stands may be planted solely to improve growing conditions for the target
timber tree species. In turn, in monocultures, nutrient cycling is restricted to the
litter of the planted tree species. The eventual slow litter decomposition of one par-
ticular tree species would diminish the rate of nutrient cycling, which would affect
tree growth, independently of any improvement in soil fertility.

12.4 Case Studies

A mixed-species plantation for timber production can be managed in two ways:

(1) it may be designed to harvest crop trees all at the same time or (2) the planta-
tion may allow for different species maturation rates, with harvests occurring
years to decades apart (Hall and Asthon 2016). In this sense, Gama-Rodrigues
et al. (2007) evaluated the biomass and nutrient cycling in 22-year-old pure and
mixed stands of six native hardwood species of the Atlantic Forest in southeastern
244 A. C. Gama-Rodrigues

Table 12.1 Diameter at breast height (DBH), total height (TH), and tree stem volume (VOL) of
native forest species, in pure (P) and mixed stands (M) in southeastern Bahia, Brazil
DBH TH VOL
Species P (cm) M (cm) P (m) M (m) P (m3 tree−1) M (m3 tree−1)
P. angustiflora 16.7 13.1 12.5 15.0 0.114 0.088
C. robustum 14.6 14.6 15.5 19.8 0.125 0.179
A. psilophylla 13.7 14.6 12.7 15.3 0.099 0.155
S. chrysophyllum 18.1 17.5 12.3 18.2 0.127 0.254
C. trichotoma 14.8 16.9 15.5 19.9 0.142 0.222
M. latifolium 16.9 18.0 11.5 16.5 0.166 0.204
Mean 15.8a 15.8b 13.3 17.5 0.129 0.184
a
Mean of the pure stands
b
Mean of the species in the mixed stand (from Gama-Rodrigues et al. 2007)

Table 12.2 Biomass of components of native forest species, in pure (P) and mixed (M) stands
Species Leaf Branch Bark Bolewood Total
P M P M P M P M P M
−1
kg tree
P. angustiflora 5.0 7.3 34.0 38.9 8.1 5.7 93 69 140 121
C. robustum 3.0 2.9 11.3 11.5 14.0 16.9 60 81 88 112
A. psilophylla 7.3 20.1 23.0 55.2 6.3 11.1 60 105 95 191
S. chrysophyllum 9.8 9.6 20.9 22.4 8.8 11.8 76 84 116 128
C. trichotoma 1.6 4.2 10.4 15.6 10.0 15.6 69 111 91 147
M. latifolium 6.8 8.8 20.1 22.1 15.0 12.0 84 109 121 152
Mean 5.6a 8.8b 20.0 27.6 10.4 12.0 74 93 110 142
a
Mean of the pure stands
b
Mean of the species in the mixed stand (from Gama-Rodrigues et al. 2007)

Bahia. The following species were studied: Peltogyne angustiflora (pau-roxo),

Centrolobium robustum (putumuju), Arapatiella psilophylla (arapati),
Sclerolobium chrysophyllum(arapaçu), Macrolobium latifolium (óleo-comumbá),
Cordia trichotoma (claraíba). The first five species are leguminous trees. The
mixed species outmatched pure stands in height, stem volume, and total biomass
(Tables 12.1 and 12.2). Thus, growth and yield in mixed-species stands were
higher than in pure stands owing to the combination of species with complemen-
tary ecophysiological attributes, consequently improving the efficiency in nutrient
use and cycling. In contrast, Silva and Vinha (1991) did not find any differences in
tree height of the native species Arapatiella psilophylla, Bombax macrophyllum
(imbiruçu), Bowdichia virgilioides (sucupira-preto), and the exotic Gmelina arbo-
rea (gmelina) between pure and mixed stands under the same environmental con-
ditions. In southern Bahia, Vinha (1992) also reported that in plantations with
Bombax macrophyllum shaded with Leucaena leucocephala (leucena) the survival
rate was approximately 90%, whereas in pure plantings it was little more than
10%. Thus, empirical evaluations showed that, in general, the satisfactory further
development of native hardwood species in southern Bahia occurred in mixed
stands and not in pure stands.
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 245

Mixed stands of six hardwood species at the age of 9 years (farinha seca—Pel-
tophorum dubium, ipê rosa—Handroanthus heptaphylla, ipê amarelo—Handroan-
thus chrysotrichus, mogno africano Khaya sp., paineira—Ceiba speciosa, and
sobrasil—Colubrina glandulosa) with 75% density of fast-growing N2-fixing legu-
minous trees (acacia auriculada—Acacia auriculiformis, acacia—Acacia mangium,
guachapele—Pseudosamanea guachapele, jaracandá da Bahia—Dalbergia nigra,
orelha de negro—Enterolobium contortisiliquum, pau-jacaré—Piptadenia gonoac-
antha, and sabiá—Mimosa caesalpiniaefolia) can increase soil P concentrations
through cycling and accumulation of organic and inorganic P compounds, and con-
serving N and organic matter in a red-yellow Latosol, in the state of Rio de Janeiro
(Aleixo et al. 2019, in press). However, growth and yield of all tree species were not
satisfactory (Fig. 12.1).

Fig. 12.1 Mixed stand with six hardwood species and fast-growing N2-fixing leguminous trees for
the reclamation of degraded lands in southern Rio de Janeiro, Brazil (photo: A.C. Gama-Rodrigues)
246 A. C. Gama-Rodrigues

Fig. 12.2 Consortium of Acacia mangium (for energy) and Schizolobium amazonicum (for lami-
nate) in Paragominas, state of Pará, Amazon, 10 months after planting (photo: J.L.M. Gonçalves)

In the Amazon region, several consortium combinations have been tested

between Schizolobium parahyba and other tree species (Fig. 12.2). In southern Pará,
mean annual increments in height, diameter at breast height, and volume of
Schizolobium parahyba were higher in mixed plantations with Cordia goeldiana
and Swietenia macrophylla than in pure plantations (Cordeiro et al. 2015). Souza
et al. (2003) reported several consortia tested in the municipality of Igarapé-Açu,
Pará: (1) Schizolobium parahyba × Swietenia macrophylla × Protium heptaphyllum
(breu sucuruba); (2) Schizolobium parahyba × Tectona grandis × Hymenaea cour-
baril (jatobá); (3) Schizolobium parahyba × Ceiba pentandra (sumaúma) × Ochroma
pyramidale (pau de balsa). The highest growth of the species was in consortium
with Swietenia macrophylla and Protium heptaphyllum. In Amazonas, in a 4-year-­
old the consortium Schizolobium parahyba × Carapa guianensis (andiroba) pre-
sented the highest growth in height and diameter over the consortia Schizolobium
parahyba × Bertholletia excelsa (castanha-do-pará) and Schizolobium parahyba ×
Swietenia macrophylla. Even though S. parahyba is a legume tree it is a non-­
nodulating species and may not contribute with N to the system.
In Costa Rica, 15–16-year-old mixed plantation of Vochysia guatemalensis,
Virola koschnyi, Jacaranda copaia, Terminalia amazonia, and Hieronyma alcho-
rneoides may be the preferred system for reforestation with native species
designed for timber production or carbon sequestration because this system is
more economically viable and productive than pure plantations (Piotto et al.
2010). Hall and Ashton (2016) describe a project of planting design and growth
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 247

through time for a mixed-species timber plantation, with four native species in
Panama: Ormosia macrocalyx (N2-fixing species), Dalbergia retusa (also fixes
N2), Terminalia amazonia, and Hieronyma alchorneoides. According to the model
T. amazonia and H. alchorneoides can be harvested at around 20 years; while
D. retusa can be harvested at around 30 years of age.
The use of leguminous tree species associated with N2-fixing bacteria and arbus-
cular mycorrhizal fungi is a technique that has shown viability to accelerate land
reclamation and initiate natural succession in several regions of Brazil
­(Gama-­Rodrigues et al. 2008; Chaer et al. 2011). However, trees from the genera
Acacia, Mimosa, and Gliricidia, among other N2-fixing species, have been used
mainly in pure stands. The focus on commercial use of these species is secondary to
improving environmental conditions. Among them, high inputs of organic matter
via litterfall (Costa et al. 2014) and increases in the organic C and N contents of the
soil and microbial biomass have been reported (Gama-Rodrigues et al. 2008).
Advances as higher mineralization rates of C and N of the soil (Nunes et al. 2016),
greater contents of soil organic P (Zaia et al. 2008), higher abundance, and richness
of the soil fauna (Manhães et al. 2013; Bianchi et al. 2017) were also detected. Such
improvements further reduce the risks of erosion, given the permanent cover of the
soil by the accumulated litter. In a 7-year-old mixed-species stand with the native
Atlantic Forest species Anadenanthera falcata (angico—N2-fixing species),
Myracrodruon urundeuva (aroeira), Gochnatia polymorpha (cambará), and
Tabebuia impetiginosa (ipê-roxo) uniform litterfall rates enabled a more effective
soil cover, even though pure stands of Gochnatia polymorpha and Anadenanthera
falcata had showed the highest litterfall production (Garrido and Poggiani 1982).
However, regarding the improvement of soil quality using leguminous trees, whether
in pure or mixed systems, the magnitude of edaphic changes is related to the soil
buffer capacity. In soils with high contents of organic matter and clay, it is expected
that these changes are of low magnitude. In this situation, changes of soil properties
will take longer periods of time. Therefore, in addition to soil resilience, the level of
degradation and the type and intensity of land use influence the ability of forest spe-
cies to change the soil attributes, and site productivity.
Rappaport and Montagnini (2014) evaluated the restoration potential of 21 native
tree species of the Atlantic Forest 3 years after planting in the understory of an old
rubber plantation in southern Bahia. Eight leguminous tree species were tested:
Arapatiella psilophylla (arapati), Caesalpinia echinata (pau-brasil), Copaifera
lucens (pau-óleo), Tachigali densiflora (ingá-açu), Andira legalis (angelim),
Swartzia macrostachya (manga-brava), Parkia pendula (faveira), and Inga hetero-
phylla (ingá-caixão). Among these eight tree species, Parkia pendula and Tachigali
densiflora grew faster than the other leguminous tree species.

12.5 Use of N2-Fixing Tree Species in Agroforestry Systems

Multistrata agroforestry systems are considered a good model of mixtures of N2-­

fixing and non-N2-fixing tree species. In this case, agroforestry systems (AFS)
based on cacao (Theobroma cacao) are the best example of sustainability of shaded
248 A. C. Gama-Rodrigues

Fig. 12.3 Cacao-cabruca systems in southeastern Bahia, Brazil (photo: A.C. Gama-Rodrigues)

tree-shrub systems because of their high potential for sequestering carbon, recy-
cling nutrients, and providing other environmental services, in order to ensure
greater diversity of multiple supply of timber and non-timber products. Brazil is one
of the major cacao-producing countries, accounting for 5% of the world’s cacao
production. The main cacao-producing areas are (1) Amazon region (Pará, Rondônia,
Mato Grosso, and Amazonas) in 192,411 ha of planted area and (2) south of Bahia
and northern Espírito Santo in 550,000 ha of planted area. The cacao-cabruca and
cacao shading leguminous tree systems are the matrices that dominate the landscape
in the cocoa-growing region in southern Bahia. In cabruca systems, the cacao is
planted under thinned natural forest shaded by native tree species (Fig. 12.3), where
the cacao stand density is about 600 plants ha−1 and the remaining shade trees range
from 30 to 70 individuals ha−1 with a mixture of N2-fixing and non-N2-fixing tree
species. This plantation system is established in an area of 385,000 ha−1. In these
systems, the leguminous tree Erythrina spp. (erythrina) is the most common among
such introduced shade trees in areas where all native forest has been removed
(Fig. 12.4). In this Atlantic Forest system (AFS) cacao and erythrina are established
at densities of 1111 and 32 plants ha−1, respectively, and the canopy of erythrina is
not pruned. This plantation system grew out of the 1960s, when CEPLAC (Executive
Committee of the Plan of Cacao Farming) initiated a broad program aiming at sig-
nificant increases in cacao production based on the reduction of cacao shading,
eliminating 50–70% of the trees of the Atlantic Forest (Monroe et al. 2016).
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 249

Fig. 12.4 Cacao-erythrina agroforestry systems in southeastern Bahia, Brazil (photo: A.C.
Gama-Rodrigues)

However, in the last two decades, CEPLAC has recommended that erythrina be
replaced by multiple-use tree species such as rubber trees (Hevea brasiliensis) to
increase the farmers’ income. Currently, the planted area of the cocoa-rubber sys-
tem is 12,000 ha. This AFS is established in double rows of rubber alternated with
4–5 cacao rows and a row of Gliricidia sepium (gliricidia), a N2-fixing legume tree,
in the cacao-planting area (Fig. 12.5). These three cacao AFS have high potential for
sequestering carbon in the plant-soil system (Gama-Rodrigues et al. 2011b; Monroe
et al. 2016), high nutrient cycling rates and soil nutrient stocks (Zaia et al. 2012;
Fontes et al. 2014; Aleixo et al. 2017), and high soil biodiversity (Moço et al. 2010;
Oliveira et al. 2018). Thus, these ecological processes are excellent evidence of the
compatibility and complementarity of different species for the sustainability of mul-
tistrata production systems.
There are several models of agroforestry systems based on the shaded cacao with
a mixture of N2-fixing and non-N2-fixing tree species in the Amazon region (Müller
and Gama-Rodrigues 2012). Figure 12.6 shows the combination of cocoa with the
tree species Schizolobium amazonicum (paricá), Cordia alliodora (freijó-louro),
Bagassa guianensis (garrote), Swietenia macrophylla (mogno), Bertholletia excelsa
(castanha-do-pará), and Tabebuia heptaphylla (ipê-roxo), all of them non N2-fixing
species. In Rondônia, this model has been used since 1973 and totals 30,650 hect-
ares. It can be considered as an artificial cabruca system. Another plantation system
design is the combination of cacao with coconut (Cocos nucifera) and gliricidia plus
banana. In this system, the planting densities are cocoa 740 plants ha−1, coconut 123
250 A. C. Gama-Rodrigues

Fig. 12.5 Cacao-rubber agroforestry systems with gliricidia in southeastern Bahia, Brazil (photo:
A.C. Gama-Rodrigues)

plants ha−1, banana 740 plants ha−1, and gliricidia 247 plants ha−1 (Fig. 12.7).
Currently, there are about 500 ha of this mixed system. On the other hand, Almeida
et al. (2009) evaluated the richness of tree species and timber potential, present in
some cacao plantations established in Ouro Preto do Oeste, Rondônia, since the
1980s. The number of tree species found during the survey is described in Table 12.3.
The leguminous tree species accounted for 22% of all tree species surveyed. The
largest number of leguminous tree species was Caesalpinioideae (six species), fol-
lowed by Mimosoideae (five species) and Papilionoideae (three species). Most
shade tree species came from natural regeneration and only 2–20% from seedling
planting, with Schizolobium amazonicum being the most common tree species, with
45% of individuals inventoried and timber average volume of 51 m3 ha−1.
Additionally, these cacao AFS with this profile of floristic diversity could be consid-
ered in the Amazon as areas of forest restoration in the properties with demand of
environmental liabilities.
Forest-based fallow systems enriched with fast-growing N2-fixing leguminous
tree species appear to be a viable option for managing N despite the large amount of
N removed from the system as timber and fuelwood (Gama-Rodrigues 2011). This
technique has been used as an alternative to the use of fire and reduction of a fallow
period in slash-and-burn systems adopted by family farming in northeast Pará (Kato
et al. 2006). The selected leguminous tree species to accelerate the accumulation of
biomass and nutrients are Acacia angustissima, A. auriculiformis, Acacia mangium,
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 251

+ 3,0 m + + + + + + + + + + + + + + +
3,0 m

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +
15,0 m

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +
15,0 m

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + +

Fig. 12.6 Schematic diagram showing the spatial arrangement of cacao-based (+) association
with native tree species ( ): Schizolobium amazonicum, Cordia alliodora, Bagassa guianensis,
Swietenia macrophylla, Bertholletia excelsa, and Tabebuia heptaphylla (from Müller and Gama-­
Rodrigues 2012)

+ + + + + + + + + +
3,0 m 3,0 m 3,0 m 9,0 m
3,0 m

+ + + + + + + + + +
9,0 m

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

+ + + + + + + + + +

Fig. 12.7 Schematic diagram showing the spatial arrangement of cacao-based (+) association
with coconut (●) and gliricidia (∗) (from Müller and Gama-Rodrigues 2012)
252 A. C. Gama-Rodrigues

Table 12.3 Shading species present in four cocoa plantations in Ouro Preto do Oeste, Rondônia,
Brazil
Common name
(Portuguese) Family Genus or species
Abacateiro Lauraceae Persea americana Mill.
Algodoeiro ou Bombacaceae Eriotheca sp.
Imbiruçu
Amoreira Moraceae Maclura tinctoria (L.) D. Don ex Steud
Angelim-saia Fabaceae-­Mimosoideae Parkia pendula (Willd.) Benth. ex Walp.
Angico-branco Fabaceae-­Mimosoideae Piptadenia foliolosa Benth
Angico-rosa Fabaceae-­Mimosoideae Parapiptadenia rigida (Benth.) Brenan
Babaçu Arecaceae Attalea speciosa Mart. ex Spreng
Babão ou Coco Babão Arecaceae Syagrus comosa (Mart.) Mart.
Bacurizeiro Arecaceae Attalea phalerata Mart. ex Spreng
Bajinha Fabaceae-­ Pterogyne sp.
Caesalpinioideae
Bandarra ou Paricá Fabaceae-­ Schizolobium parahyba var. amazonicum
Caesalpinioideae (Huber ex Ducke) Barneby
Bolão Sapotaceae Pouteria pachycarpa Pires
Cajazinho ou Anacardiaceae Spondias mombin L.
Taperebá
Canela Lauraceae Nectandra sp.
Castanheira-do-brasil Lecythidaceae Bertholletia excelsa Humb. & Bonpl.
Cebolão Unknown Unknown
Cedro-rosa Meliaceae Cedrela odorata L.
Cerejeira Fabaceae-­Papilionoideae Amburana acreana Ducke (A.C.Sm.)
Coração-de-negro Fabaceae-­Papilionoideae Swartzia panacoco Cowan
Camaruzeiro Fabaceae-­Papilionoideae Dipteryx sp.
Embireira Timeleaceae Daphnopsis sp.
Farinha-seca Chrysobalanaceae Parinari coriaceum Benth
Feijão-cru Fabaceae-­Mimosoideae Pithecellobium saman var. acutifolium
Benth
Figueira Moraceae Ficus sp.
Freijó-cinza Boraginaceae Cordia goeldiana Huber
Garapa Fabaceae-­ Apuleia leiocarpa (Vogel) J.F.Macbr
Caesalpinioideae
Garrote Moraceae Bagassa guianensis Aubl.
Gmelina ou Melina Verbenaceae Gmelina arborea Roxb.
Goiabeira Myrtaceae Psidium guajyava L.
Imbaúba Cecropiaceae Cecropia sp.
Ingazeira Fabaceae-­Mimosoideae Inga sp.
Ipê-amarelo Bignoniaceae Tabebuia incana A. Gentry
Ipê-champagne Bignoniaceae Tabebuia sp.
Ipê-roxo Bignoniaceae Tabebuia sp.
Ipê-tabaco Bignoniaceae Tabebuia serratifolia (Vahi) Nichols.
(continued)
12 Multifunctional Mixed-Forest Plantations: The Use of Brazilian Native… 253

Table 12.3 (continued)

Jangada Rubiaceae Guettarda viburnoides Cham. &Schltdl.
Jaqueira Moraceae Artocarpus integra L.
Jatobá Fabaceae-­Papilionoideae Hymenaea oblongifolia Huber
Jenipapeiro Rubiaceae Genipacaruto H.B.K.
Laranjeira Rutaceae Citrus sinensis (L.) Osbeck
Leiteira Moraceae Brosimum sp.
Limeira Rutaceae Citrus bergamia Risso
Limoeiro Rutaceae Citrus limon (L) Burm
Louro Lauraceae Ocotea sp.
Mamica-de-porca Tutaceae Zanthoxylum acreanum (Krause) J.F. Macbr.
Mangueira Anacardiaceae Mangifera indica L.
Maparaíba Unknown Unknown
Mogno Meliaceae Swietenia macrophylla KING
Mutamba Sterculiaceae Guazuma sp.
Paineira Bombacaceae Chorisia sp.
Pau d’alho Phytolaccaceae Gallesia integrifolia (Spreng.) Harms
Pau-sangue Guttiferae Vismia brasiliensis Choisy
Pintadinho Fabaceae-­ Poeppigia procera Presl
Caesalpinioideae
Ponkan Rutaceae Citrus reticulata Blanco
Pupunheira Arecaceae Bactris gasipaes H.B.K.
Seringueira Euphorbiaceae Hevea brasiliensis (Willd. ex. Adr. De Juss.)
Muell. Arg.
Sete Camadas Unknown Unknown
Sumaumeira Bombacaceae Ceiba pentandra (L) Gaertn.
Tarumã Berbenaceae Vitex sp.
Tauari Lecytidaceae Couratari sp.
Tucumazeiro Arecaceae Astrocaryum sp.
Unha-de-vaca Fabaceae-­ Bauhinia sp.
Caesalpinioideae
Urtigão Unknown Unknown
From Almeida et al. 2009

Clitoria racemosa, Inga edulis, and Sclerolobium paniculatum. The fallow vegeta-
tion enriched with A. mangium is the one that presented the greatest potential for
sequestering carbon 2 years after fallow.

12.6 Outlook and Conclusions

Mixed-forest plantations have high potential to be an alternative to conventional

monoculture systems to address environmental, social, and economic issues in
Brazil. But their integration in agricultural landscapes requires a qualitative SWOT
254 A. C. Gama-Rodrigues

(strengths-weaknesses-opportunities-threats) analysis of local stakeholders’ per-

ceptions. A priori, lack of systematic research and technology inputs to improve the
system would be the major weaknesses, while sustainability, multi-functionality,
and high sociocultural values would be common strengths. Potential government
support, climate-smart forestry, and climate-change mitigation would constitute
good opportunities, but lack of knowledge on economic viability and strong pres-
sure towards high productivity would be threat factors. Thus, SWOT analyses
should take from climate-smart forest to climate-smart landscapes. To achieve
climate-­smart landscapes, future research needs should prioritize forest breeding
and biotechnology for multifunctional mixed-forest plantations integrated into the
biological management of soil fertility and modeling of plant-soil interactions.
Therefore, the technology produced based on ecological processes can support
farmers as managers of complex social-ecological systems better than those based
on technological packages. Thus, integrated management of natural resources can
increase rural prosperity through better communication of results between different
stakeholders.

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Chapter 13
The Brazilian Legal Framework
on Mixed-­Planted Forests

Luiz Fernando Duarte de Moraes, Renata Evangelista de Oliveira,

Maria Jose Brito Zakia, and Helena Carrascosa Von Glehn

13.1 Introduction

Forests have been playing a very important role in the establishment of land-use
policies worldwide. Forest cover changes directly affect biodiversity, global carbon
budget, and ecosystem functions. In many countries in Latin America, historically
there has been a contrasting dynamics between rates of deforestation and reforesta-
tion. From 2001 to 2010, Brazil lost hundreds of thousands of hectares of forests,
and simultaneously the country witnessed the greatest expansion of woody vegeta-
tion gain (Aide et al. 2013). A significant part of this gain was likely due to planting
forests with exotic and native species all over the country.
Planting forests in Brazil has two main motivations throughout history: as an
economic activity, supplying raw materials for construction and furniture making,
and as actions for the fulfillment of legal obligations. Landowners plant forests as
an option to restore permanent preservation areas and legal reserves and so meet the
legal requirements placed by the current legal framework on land use (Oakleaf et al.
2017). Recently, planted forests have also become relevant to mitigate the effects of
climate change.
Natural and planted forests have multiple benefits, contributing to production,
protection and conservation, and environmental and social services (SFB 2013;

L. F. D. de Moraes (*)
EMBRAPA Agrobiology, Brazilian Agricultural Research Corporation, Seropédica, RJ, Brazil
e-mail: luiz.moraes@embrapa.br
R. E. de Oliveira
Department of Rural Development, Federal University of São Carlos, Araras, SP, Brazil
M. J. B. Zakia
Department of Forest Sciences, São Paulo State University, Botucatu, SP, Brazil
H. C. Von Glehn
São Paulo Environmental System, São Paulo, SP, Brazil

© Springer Nature Switzerland AG 2020 257

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3_13
258 L. F. D. de Moraes et al.

Yao et al. 2016). Additionally, different forms of reforestation may be used for
many objectives (Baral et al. 2016), for instance, depending on the purpose (indus-
trial use, environmental, agroforestry, and farm forestry) or species composition
(monoculture or mixed species, hardwood or softwood, native or exotic species).
Forest plantations can be used to restore biodiversity and to provide goods and
services, but different goals require different strategies, planting, and management
models as well, including the use of more or less species. In Brazil, most planted
forests are tree monospecific plantations of exotic species, mainly Pinus and
Eucalyptus.
According to Lamb et al. (2005), if we intend to supply goods and ecological
services, tree plantation monocultures are efficient for timber or food production,
but in most circumstances they are less successful in supplying services.1 Mixed-­
species plantations with native species can potentially supply a wider range of
goods and services than monocultures, since biodiversity gains are expected to be
greater.
Whether for economic reasons or for requirement of legal compliance, there is a
high demand and the enormous challenge of identifying opportunities offered by
laws and public policies for the planting of mixed forests.
In this chapter, we discuss the legal framework of planted forests, focusing on
federal Brazilian rules for use and management of forest plantations, with either
exotic or native species. We intend to clarify when, where, and how those forests
can be established according to legal rules, to a more effective provision of timber
and non-timber products, and services as well.
We focus on the legal framework of the so-called multifunctional mixed-planted
forests; neither native forest remnants nor monocultures will be the object of
discussion.

13.2 Concepts

New definitions on “forest” have been necessary to have policies promoting effec-
tive forest conservation; minor changes in traditional definitions may distinguish
native forests from plantations, ensuring that planted forests will protect biodiver-
sity and contribute to sustainable development (Sasaki and Putz 2009).
For the Brazilian legal framework, the concept of forest has not been estab-
lished yet. According to FAO, forest is as a “land spanning more than 0.5 hectares
with trees higher than 5 meters and a canopy cover of more than 10 %, or trees able
to reach these thresholds in situ. It does not include land that is predominantly
under agricultural or urban land use”; planted forests are defined as being predomi-
nantly composed of trees established through planting and/or deliberate seeding
(FAO, 2012).

1
Services supplying means conserving ecological and hydrological processes.
13 The Brazilian Legal Framework on Mixed-Planted Forests 259

Since FAO’s definition is not suggested to meet the minimum requirements to

attend public policies, a new definition was adopted under the Kyoto Protocol:
“Forest is a minimum area of land of 0.05–1.0 hectares, with tree crown cover (or
equivalent stocking level) of more than 10–30%, with trees with the potential to
reach a minimum height of 2–5 m at maturity in situ.” A forest may consist of either
closed forest formations where trees of various storeys and undergrowth cover a high
proportion of the ground or open forest. Young natural stands and all plantations
which have yet to reach either a crown density of 10–30% or tree height of 2–5 m are
included under forest. Those are considered areas normally forming part of the forest
area which are temporarily unstocked, as a result of human intervention such as har-
vesting or natural causes but which are expected to revert to forest (Kant 2006).
During the World Congress of Forests in 1990, new concepts and management
practices were proposed to distinguish the so-called forest plantations (simple trees
cultivation/silviculture) from “planted forests” (which brings the comprehension of
these forests as ecosystems):
The success of the forest plantations depends on the species fitness, its origin, and on their
objectives. Further than the dogmatic controversial issues concerned to the introduction of
exotic species, management priorities should aim the maintenance of soil productivity
potential, as well of some biodiversity and sustainable income. The management of forest
plantations must aim changing plantations into forests.

In fact, this simple change of words brings distinct concepts: while “forest plan-
tations” focus on timber production, “planted forests” are planned and managed for
both forest production and ecosystem services, like water regulation and soil and
biodiversity conservation.
FAO’s recommendation in the 1990s may be seen as a way of integrating forestry
production (through plantations) to the maintenance of ecological and hydrological
processes, i.e., to social and environmental values (ensured by planted forests, in
this case). As we can see, there is not a clear relationship between “forest planta-
tions” (single-tree cultivation) and “planted forests,” since the concept of planted
forests is suggested to aggregate social and environmental issues into planning,
decision-making, and forest management (Lima and Zakia 2006).
Anyway, a new concept has been proposed: multifunctional forests are suggested
to embrace issues further than structure, concerning species composition and eco-
logical functioning of forests, closely related to the provision of ecosystem services,
as described in Fig. 13.1. As suggested in Fig. 13.1, a mixed plantation consisting of
Eucalyptus and Acacia (only two species and both exotic) is not expected to provide
multiple functions (or services) to the environment.
The Brazilian legal framework (Federal Decree 8375/2014) defines planted for-
ests as those “consisting predominantly of trees, established by planting or seedling,
cultivated with economic purposes and for trades, out of permanent preservation,
restrict use and legal reserve areas.”
Planted forests in Brazil are placed by legislation according to two aspects: the
portion of either the landscape or the rural property they are located on, and the
260 L. F. D. de Moraes et al.

Fig. 13.1 Framework to introduce the concept of multifunctional mixed forests (adapted from
Thiel, 2017). Hans Thiel, Close to Nature Planted Forests (CTNPF). World Bank/FAO Collaborative
Program (CP) Initiative. Report, 2017 (not published)

objectives of planting forests. Forests can be planted on permanent preservation

areas and legal reserve, which are mandatory protected natural areas (Silva and
Ranieri 2014); on areas of restricted use; and on areas available for agriculture and
forestry with no restrictions. Legal definitions of each type of area described below,
as well as their closeness to different kinds of planted forests, are given below:
• Permanent Preservation Area (APP): A protected area, covered or not by native
vegetation, with its environmental functions of preserving water resources, land-
scape, geological stability, and biodiversity; improving the fauna and flora gene
flow; protecting the soil; and ensuring the well-being of human populations.
• Legal Reserve: An area located within a property or a rural possession, under the
terms of article no. 12, with the purpose of ensuring the economic and sustain-
able use of the rural property’s natural resources, keeping and restoring ecologi-
cal processes, and promoting biodiversity conservation, which includes shelters,
and protection of wild fauna and native flora.
• Consolidated Rural Area: A rural property area occupied by human beings,
existing prior to July 22, 2008, with its buildings, improvements, or agricultural
and forestry activities, which may include a fallow system.
• Areas of Restricted Use: Areas with specific characteristics, which are:
–– Pantanal areas and plains, and areas where ecologically sustainable exploitation
is allowed, and where technical recommendations from official research author-
ities must be observed. New removals of native vegetation for alternative use of
the soil will depend on the approval of the state’s environmental authority.
13 The Brazilian Legal Framework on Mixed-Planted Forests 261

–– Slope areas between 25° and 45° where sustainable forest management and
farming, cattle breeding, and forestry activities are allowed, as well as the main-
tenance of the physical infrastructure connected to the development of these
activities, provided that good agricultural practices are observed. The conver-
sion of new areas is forbidden, except when declared of public interest.
• Area for Common Use: Non-protected area, available for agriculture, cattle rais-
ing, and forestry (alternative soil uses).
An overview of the evolution of legal framework on forests may allow under-
standing how the regulatory environment affects the perception on the alternatives
for the use and management of forests in rural properties. To meet the main objec-
tive of this book, it is necessary to state that mixed Eucalyptus and Acacia planted
forests are not allowed to fulfill legal environmental requirements (to recover per-
manent preservation areas or legal reserves, for instance). The legal framework
related to native and planted forests in Brazil, in a historical perspective, is pre-
sented below.

13.3 Brazilian Federal Legal Framework

The historical development of legal system regulating the use and management of
forests in Brazil may be divided into historical periods.
The first regulatory mechanisms on forests in Brazil were based on the Portuguese
legal system. The Colonial period, from 1500 to the beginning of the nineteenth
century, was characterized by an unsustainable exploitation of timber products. A
good example was the intense withdrawal of the valuable “pau-brasil” (Brazil
wood), exclusively traded with the Portuguese Crown that adopted the first legal
acts (as the “Pau-Brasil Act, in 1605) to protect natural resources, basically with
economic purposes (Medeiros 2006; Bacha 2004). By the end of the eighteenth
century, a Royal Charter stated the need to conserve native forests and prohibited
the unauthorized cutting of valuable hardwood tree species (Medeiros 2006). From
that period to the end of the nineteenth century the plantation of forests had basi-
cally ornamental and scientific purposes (Hora 2015).
During the Imperial period (nineteenth century), Brazilian Atlantic Forest faced
an intense deforestation for coffee farming expansion, which led to the creation of
command and control policies. In the first decades of the Brazilian Republic, estab-
lished in the end of the nineteenth century, the government promoted the forest
sector with economic purposes, by introducing Eucalyptus (the potential of native
tree species was poorly known) plantations, which resulted in great deforestation.
Following this period, government initiatives showed some concerns on environ-
mental aspects, and created the Brazilian Forest Service, in the 1920s, and the first
Forest Code, in 1934, which proposed four categories of forests: protective, rem-
nants, model, and production (Thomas and Foleto 2013; Bacha 2004). The 1934
forest code implied the “obligation of large consumers of forest products (such as
262 L. F. D. de Moraes et al.

steel companies and transportation) to keep the cultivation of forests for firewood or
charcoal supply (spare)” (Bacha 2004). Imprisonment, detention, and fines were
some of the penalties imposed by the 1934 forest code to those responsible for
deforestation, burning forests, and invading public lands (Moretto et al. 2010).
Environmental concern increased during the 1960s, when an intensification of
command-and-control regulation to stop deforestation was observed. No tools to
stimulate the conservation of native forests were created though. A second version
of the Brazilian Forest Code was passed in 1965, replacing the 1934 version. Some
modifications of the first version included the requirement of authorization of the
public authorities to explore all native forests, the requirement for forest replace-
ment for all consumers of forest products, and the requirement for management
plans to explore the forests in some regions of the country (Bacha 2004). From the
beginning of the twentieth century to the 1960s, although forests were planted for
economic purposes, planted forest expansion had not promoted the development of
forestry (Hora 2015).
Despite requiring forest replacement in deforested areas, legal framework had
not defined which species could be planted (Moretto et al. 2010), which resulted in
the intense introduction of exotic and invasive species. By that time (1960s), there
was a conflict between the legal framework related to forests and other laws, like the
Land Statute, which stated that the landowner could benefit from deforestation
(Bacha 2004). Consequently, rural landowners were authorized, even when funded,
to replace native forests by homogeneous stands (Moretto et al. 2010; Bacha 2004).
It resulted in the expansion of Eucalyptus and Pinus plantations over native forests
(Moretto et al. 2010).
The area of planted forest faced a great expansion from 1965 to 1986, due to
public financial incentives and strengthening of the legal framework (Hora 2015); in
1970, planted forests covered 1.66 million hectares, reaching up to almost six mil-
lion hectares in 1985 (Bacha 2004). There were no clear concerns on the costs of
planting forests in that period (Hora 2015).
The expansion of forest-planted area in Brazil from 1975 to 2000, however, was
about 5% of the deforested area in Amazonia, in the same period (Bacha 2004). In
summary, forest plantations were used in that period as a tool for economic develop-
ment, putting aside other benefits forests can provide, especially those related to
biodiversity conservation and ecosystem service delivery.
The economic development approach in that period was evidenced by the cre-
ation, in 1967, of the Brazilian Institute of Forest Development (IBDF), to regulate
afforestation and reforestation activities, evaluating projects applied to access pub-
lic funds. Most of the reforestation projects supported by the IBDF had economic
purposes and used mostly exotic species. Only by the end of the 1980s the legal
framework brought the concern on prioritizing native species in reforestation made
by legal compliance (Moretto et al. 2010).
In 1988, the new Brazilian Constitution allowed states to also create specific laws
and legislate on the management and use of forest resources. On the other hand, public
policies for the economic development remained a great threat to forest conservation,
and deforestation indices remained high (Bacha 2004). As the destruction of forest
13 The Brazilian Legal Framework on Mixed-Planted Forests 263

resources could affect the economic development of the country, new policies based
on command and control have been established to reduce deforestation (Bacha 2004).
During the Earth Summit in 1992, in Rio de Janeiro, intergovernmental and interna-
tional agreements were made to use sustainable development to protect forests (Nazo
and Mukai 2001).
The lack of financial incentives, although forestry was considered a profitable
activity, was followed by a reduction in the planted area, to almost five million ha in
2000. As it was difficult to expand planted forests, the sector invested, from 1990 to
2000, in the development of tools and techniques to improve efficiency in forestry
(Hora 2015).
Up to 2006, Brazilian legal frames targeting forest remained excessively protec-
tionist, but the Law 11284/2006, which aimed to protect the Atlantic Forest, pro-
moted sustainable use and conservation in public forests. That law provided the
basis of a forest-based development model, by taking into account several issues,
like ecosystem and biodiversity protection, rights of traditional communities, an
efficient and rational forest use, and conditions to stimulate long-term investment
(Bustamante et al. 2018). Importance of economic goals (e.g., profitability, produc-
tivity, efficiency) became most visible when the responsibility for and coordination
of planted forests were transferred from the Ministry of the Environment to the
Ministry of Agriculture (Bustamante et al. 2018).
There is a clear expansion of planted forests over the last decades in Brazil (Hora
2015), and a concern that forestry expansion may negatively affect biodiversity. The
current Brazilian legal framework provides a system for the protection and forestry
regulation with laws mostly focusing on native vegetation (Brazil holds six biomes3),
water resources, and climate. Four legal tools,2 as below, rule planted forests:
(a) The National Policy on Climate Change (Federal Law 12187/2009), established
to consolidate and expand protected areas, fostering reforestation and revegeta-
tion of degraded areas.
(b) Conflicts between biodiversity conservation and social and economic interests
pushed the establishment of the most recent legal framework in Brazil: the Law
for the Protection of Native Vegetation (12651/2012). This law establishes rules
for the protection, restoration, and compensation of native vegetation, and
defines rules for forest exploitation and controls the origin of forest products. It
regulates extractive activities and management of wood and non-wood products
in native and planted forests, in conformity to a previously approved sustainable
forest management plan (Oliveira and Sais 2017; Zakia and Guedes Pinto 2013;
Kuntschik 2012). Forest plantation in non-protected areas is considered as
agriculture.
(c) Most recently, Brazil has established an Agriculture Policy for Planted Forests
(Decree 8375/2014), and the National Policy for the Recovery of Native
Vegetation (Decree 8972/2017). Both policies offer interesting opportunities
for the development and expansion of planted forests in Brazil.

2
Federal laws can be consulted in http://www4.planalto.gov.br/legislacao/
264 L. F. D. de Moraes et al.

13.4  he National Plan on Climate Change, the Federal Law

T
and the National Policy for the Protection of Native
Vegetation, and National Policy on Planted Forests:
Opportunities and Challenges

The goals placed by legal framework and forest-based Brazilian policies offer sig-
nificant opportunities for the expansion of multifunctional mixed-planted forests,
but some bottlenecks need to be addressed.
One policy that has a great potential in fostering the expansion of mixed-planted
forest is the Brazilian National Climate Change Plan (NCCP), which aims “to make
the economic and social development compatible with the protection of the climate
system and to promote the reduction of greenhouse gas emissions by encouraging the
use of clean energy” (Brasil 2008). One of the goals of the NCCP was to eliminate
the net loss of forest coverage in Brazil by 2015, which meant avoiding deforestation,
and upscaling of forest plantations to 11 million ha in 2020; two million ha have been
expected to be plantations of native species to replace degraded pastures (Brasil 2008).
The most important Brazilian law on forestry (Federal Law 12651/2012) estab-
lishes that no previous authorization is necessary for reforestation, using either exotic
or native species (Brazil 2012). In 2017, the decree 8.972/2017 created the National
Policy for Native Vegetation Recovery (Proveg), to articulate, integrate, and promote
policies, programs, and actions that encourage forest recovery and other native vegeta-
tion forms. In order to implement that policy, the National Plan for Recovery of Native
Vegetation (Planaveg) aims to have at least 12 million ha of forests and other forms of
native vegetation restored in Brazil, up to 2030. Among the guidelines of Planaveg are
the following: to foster society’s awareness of the benefits of recovering native vegeta-
tion, and to improve the regulatory environment and increased legal certainty for the
recovery of native vegetation with economic exploitation (Brazil, 2017).
The principles of the National Plan on Climate Change are to stimulate the pro-
duction of forest goods and services for the social and economic development of the
country, and mitigate the effects of climate change (Brazil, 2014). The Brazilian
Ministry of Agriculture is in charge of creating the “National Plan for the
Development of Planted Forests,” which will establish forest production goals in
Brazil, and the actions to be taken to achieve them.
Principles, objectives, and goals above are assumed as voluntary commitments
from Brazil for the restoration of degraded areas, which may result in the expansion
of planted forests. Multifunctional mixed forests have the conditions to fulfill legal
requirements, provide adequate environmental services, and deliver economic ben-
efits. An overview on the regulation of multifunctional mixed forests in Brazil is
summarized in Table 13.1.
According to the Brazilian legal framework, multifunctional mixed forests consist-
ing exclusively of native tree species can be planted to recover all these sites in rural
properties: permanent preservation areas (within small, medium, and large properties),
legal reserves, restricted-use areas, and areas that do not need any specific regulation
(Table 13.1).
13 The Brazilian Legal Framework on Mixed-Planted Forests 265

Table 13.1 Summary of permissions and possibilities placed by Brazilian legal framework for the
implementation of multifunctional planted forests in rural properties
Recovery of
APP in Non-­
Recovery of medium and protected
APP in small great Recovery of area (suitable
properties (see properties (see Recovery of restricted-use for
Box 13.1) Box 13.1) legal reserve area agriculture)a
Plantations of Not allowed Not allowed Not allowed Not allowed Allowed
exotic trees
only
Plantations Allowed Not allowed Allowed Allowed Allowed
combining
native and
exotic trees
Plantations of Allowed Allowed Allowed Allowed Allowed
native trees
only
Agroforestry Not allowed Not allowed Not allowed Not allowed Allowed
systems with
exotic trees
only
Agroforestry Allowed Allowed Allowed Allowed Allowed
systems with
native trees
only
Agroforestry Allowed Not allowed Allowed Allowed Allowed
with native and
exotic species
Plantations for Allowed Not allowed Allowed Allowed Allowed
economic
purposes
Environmental Preserve Preserve Assist the Assist the Water and
function water water conservation conservation soil
established by resources, resources, and and conservation
legal landscape, landscape, rehabilitation rehabilitation
framework geological geological of ecological of ecological
stability and stability and processes and processes and
biodiversity, biodiversity, promote the promote the
facilitate gene facilitate gene conservation of conservation of
flow of fauna flow of fauna biodiversity, as biodiversity, as
and flora, and flora, well as shelter well as shelter
protect soil protect soil and protection and protection
of wildlife and of wildlife and
native flora native flora
Eligible for the Yes Yes Yes Yes No legal
payment of prediction
ecosystem
services
(continued)
266 L. F. D. de Moraes et al.

Table 13.1 (continued)

Recovery of
APP in Non-­
Recovery of medium and protected
APP in small great Recovery of area (suitable
properties (see properties (see Recovery of restricted-use for
Box 13.1) Box 13.1) legal reserve area agriculture)a
Legal rules Federal Law Federal Law Federal Law Federal Law Federal Law
12.651/2012 12.651/2012 12.651/2012 12.651/2012 12.651/2012;
Federal Federal Federal Decree Federal
Decree Decree 7850/2012 Decree
7850/2012 7850/2012 8.375/2014
Allowed use Needs Not Needs Needs –
and regulation applicable regulation regulation
management
for economic
purposes
APP permanent preservation areas
a
Here is a bill under discussion in the Brazilian Congress (6411 PL/2016) that proposes that silvi-
cultural activities should not require environmental licensing, in case of planting and management
of either native or exotic trees, for logging and forest resource extraction, in consolidated rural
areas, located in APP, or in degraded lands due to human activities, since those lands are not
located on the APP or the legal reserve area

Brazilian rural properties may be classified into small, medium, or large, according
to the corresponding fiscal modules (in units of area—see Box 13.1). Small properties
and familiar-based farmers have some extra benefits related to the use and manage-
ment of their lands in Brazil. There is no legal restriction for native planted forests to
meet ecological requirements, but no exploitation is allowed in recovered permanent
preservation areas (APP) located in medium and large properties. As we can see,
Brazilian current legal framework allows small farmers (Box 13.1, below) to manage
planted forests in their APP.
The use of noninvasive exotic species in planted forests to meet legal require-
ments is allowed for the recovery of APP only in small farms and to recover legal
reserves, always combined with native species. No systems consisting exclusively
of exotic trees—like the so-called Eucalyptus-Acacia system—are allowed to
recover legally protected areas. This indicates a great concern on the potential inva-
siveness of some exotic species, as Acacia species.
Plantations for economic purposes are also allowed for the recovery of restricted-­
use areas and legal reserves, which enhances the potential multifunctionality of the
models designed for those areas (Fig. 13.2). These plantations are allowed in
restricted-use areas only if the use of area is consolidated (according to Federal Law
12651/2012), and under the adoption of water and soil conservation practices that
include the Eucalyptus-Acacia system.
Since it is mandatory, the recovery of legal reserve areas offers the best opportu-
nity for the expansion of multifunctional mixed-planted forests, since environmen-
tal functions and economic benefits can be obtained simultaneously. It is important
to notice that mixed-planted forests in the legal reserve may contain noninvasive
13 The Brazilian Legal Framework on Mixed-Planted Forests 267

Box 13.1 Zakia and Guedes-Pinto (2013)

Rural Module?
A rural module is calculated for each rural property, and its area reflects the
kind of exploitation or utilization prevailing in the rural property.
Fiscal Module
A fiscal module is a land measuring unit in Brazil, established by Law no.
6746 of December 10, 1979. It is expressed in hectares, is variable, and set for
each municipality according to:
• Kind of exploitation prevailing in the municipality
• The income brought in by the main exploitation business
• Other existing exploitation businesses in the municipality which, even if not
prevailing, are significant for the income they bring, or the area they use
• Concept of family property
A fiscal module should not be confused with a rural module.
A fiscal module equals the minimum area required for a rural property to run
a viable exploitation business. Depending on the municipality, a fiscal module
may vary from 5 to 110 ha. In metropolitan regions, a rural module is usually
quite smaller than in rural areas farther away from major urban centers.
A fiscal module also serves as a standard to define beneficiaries at PRONAF
(small family farm producers, owners, sharecroppers, legal holders, partners,
or tenants of up to four (4) fiscal modules).

Fig. 13.2 Opportunities of economic uses in planted forests and potential of providing forest
services and goods according to the legal framework (adapted from Thiel, 2017). Hans Thiel,
Close to Nature Planted Forests (CTNPF). World Bank/FAO Collaborative Program (CP) Initiative.
Report, 2017 (not published)
268 L. F. D. de Moraes et al.

exotic species, which still needs legal regulation, especially for the management and
use of native trees.
The presence of native forest remnants has been costly and sometimes punitive
to rural landowners. Brazilian laws historically have restricted the use and manage-
ment of native forests, resulting in an understanding that “an overprotective approach
may fail in effective protection.” The management practices and uses recently
allowed in legal reserve are a chance to change that paradigm.
In the definition of legal reserve given by the Federal Law 12651/2012, the eco-
nomic purposes are not allowed just to mitigate costs of the reforestation (restora-
tion), but also to offer new incomes for the landowner. In this new approach, the
ecological function of the legal reserve concerns rather to ecosystem services than
the biodiversity conservation or community structure. The model that better fits to
the new objectives (as to restoration purposes) of the legal reserve is that related to
the concept of multifunctional planted forest (see Table 13.1).
The law states that economic-based alternatives to be proposed for the use
and management of legal reserve must target the maintenance of ecological
functions. As other legal tools also require the legal reserve to attend ecological
functions, there is no reason to avoid the sustainable use of forest resources in
the legal reserve. It is a matter of searching a balance between biodiversity, con-
servation, and economic sustainability, and enabling the dual functions of the
legal reserve.
In São Paulo state, this is especially challenging. Most of the rural properties do
not have enough native vegetation and need reforestation actions to fulfill the mini-
mum requirements of a legal reserve. Landowners may either protect, restore, or
offset the legal reserve to meet the legal requirements (Oakleaf et al. 2017). The
restoration of legal reserve to comply with the legal framework may be done by
either assisting natural regeneration or planting forests in the rural properties. The
combination of restoration and offset may offer a great opportunity to allow the
expansion of forest cover in strategic areas for water conservation and to reconnect
isolated forest remnants (implementation of ecological corridors). Lands in São
Paulo state have the greatest opportunity costs of land use in Brazil, both in the
Atlantic Forest and in Cerrado, resulting in high costs of restoration of native forests
as well. A proper regulation may provide economic sustainability to multifunctional
planted forests in the legal reserve, independent of legal obligations.

13.5 Final Comments

Brazilian legal framework places a good range of opportunities for the expansion of
planted forests. However, environmental threats, such as global warming and bio-
logical invasions, recommend extreme care on the use of exotic and invasive tree
species, as is the case of the Eucalyptus-Acacia consortium; their use must be
planned considering rather a multifunctional approach. For the establishment of
public policies, however, mixed-planted forests should be multifunctional and pri-
13 The Brazilian Legal Framework on Mixed-Planted Forests 269

oritize the use of multiple native species in mixed combinations (diversity is always
welcome!). This is an opportunity for the development of the silviculture of native
species.
Planting mixed forests for the recovery of permanent preservation areas in small
properties and legal reserves needs regulation to enable the delivery of economic
benefits to landowners, as well as environmental services to the landscape.
Governance is also a key issue. The opportunities discussed in this chapter, con-
sidering all the possible uses and services from multifunctional forests, will only be
achieved if governments maintain and support the legal framework and public poli-
cies listed here.
Government actions must support the consolidation of the legal environment,
and new policies should avoid conflicts with formerly published policies. Conflicts
can affect the effectiveness of regulation, hindering the achievement of policy-­
related goals. Further, since most of Brazilian forest-related policies are associated
to international agreements concerning global issues, governance should contribute
to a collective international effort, and try not to favor specific sectors.
It should be noted that government actions must always strengthen sustainable
development policies and strategies and that all care must be taken to avoid changes
in government and/or political directions negatively affecting them (unfortunately,
recent decisions of the Brazilian Government apparently have pointed in another
direction). It is also a duty of Brazilian civil society to watch out for any misconduct
in this regard.
Finally, it is important to remember that the forest cover, hopefully fulfilled with
the so-called multifunctional forests, is located in multiple and heterogeneous rural
landscapes, where the socioeconomic and cultural aspects are essential for the per-
manence (or not) of these forests, and their participation in the effectiveness of rural
development in Brazil.

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Index

A genetic improvement, 6
Abiotic factor, 59 green cancer, 231
Above net primary production (ANPP), 60 histories, 225
Aboveground biomass intercropped system, 3
A. mangium, 29–32 intraspecific competition, 36
canopy stratification, 29, 33 invasive alien species, 224
E. urophylla x grandis, 33 invasive vegetation, 226
eucalypt, 33 keystone species, 225
growth pattern, 33 Leucaena leucocephala, 231
LAI, 33 litter, 228
PAR, 33 local vegetation, 229
replacements and additive series, 33 mixed plantations, 8, 107, 228
stemwood biomass production, 33, 34 mixed-species plantations, 126
Acacia spp., 97 monoculture, 27
allelopathic effects, 229 N contribution, 22
A. mangium, 6, 48, 57, 60, 61, 68, 94, 160, N-deficient soils, 9
162, 168, 195, 223–228, 230, 232, N fertilization, 16
234, 235 N2-fixing bacteria, 227
A. mearnsii, 57, 223–225, 230–232 N2-fixing trees, 29
arbuscular mycorrhizal fungi, 227 plantation management, 225
biogeographic isolation, 224 plantations, 226
biomass, 229 seedlings stage, 227
biotic conditions, 224 silvicultural management, 20
BNF products, 112 silvicultural programs, 126
Brazilian native species, 235 silviculture, 222–224
breeding characteristics, 16 soil acidification, 228
canopies, 231 soil moisture, 228
capoeiras, 230 Acetylene reduction analysis (ARA), 112
decomposition rates, 228 Acidobacteria, 93
ecological characteristics, 224 Actinobacteria, 93
economic value, 6 Agriculture Policy for Planted Forests (Decree
ecosystem engineer, 225 8375/2014), 263
exotic and invasive species, 226 Agrisilviculture, 205
fast-growing exotic species, 5, 6 Agrosilvopastoral system, 205
foundation species, 225 Anadenanthera, 123

© Springer Nature Switzerland AG 2020 271

E. J. Bran Nogueira Cardoso et al. (eds.), Mixed Plantations of Eucalyptus
and Leguminous Trees, https://doi.org/10.1007/978-3-030-32365-3
272 Index

Angicos, 123 Biodiverse forest plantations, 3

Arbuscular mycorrhizal fungi (AMF), 161, Biodiversity, 193–195
176, 184, 209 Biodiversity and ecosystem functioning (BEF)
arbuscules and hyphal coils, 139 theory, 210
Arum type, 139 Bioindicators, 163, 186
characteristic components, 139 Biological fixation, 15
colonization, 145 Biological invasion, 222
extraradical fungal spores, 139 Biological nitrogen fixation (BNF), 18, 26,
features, 140 183, 186, 210
formation, 139 abiotic and biotic factors, 111
growth-promoting effect, 139 Acacia, 113
host plants, 139 Brazilian native species, 118
mycorrhizal endophytes colonize, 139 ecological facilitation strategy, 105
obligate biotrophic behavior, 138 effectiveness, nodulation, 106
Paris type, 139 eucalypt monocultures, 118
P-depleted tropical soils, 139 fast-growing N2-fixing species, 105
spores, 145 fast-growing non-fixing species, 104
Area for common use, 261 induction of nodules, 106
Areas of permanent preservation (APPs), 201 leguminous species, 118
Areas of restricted use, 260 mycorrhization, 110, 111
Arum-type morphology, 139 N accumulation, 116–118
Aspergillus, 93 N requirement, 113
Atlantic Forest system (AFS), 248 NA/E techniques, 113
nodulation, 107
nodule-fixing bacteria, 106
B non-fixing species, 111
Bacillus, 93 planting, 113
Bacillus subtilis, 97 primary N intake form, 104
Bacteria community prokaryotes, 104
ecological interactions, 91 restoration, degraded areas, 104
environmental conditions, 91 silvicultural management, 118
microorganism, 92 sustainable agriculture, 104
mixed plantations, 92 symbiosis establishment, 106
plant coverage, 92 tree species, 113
rhizosphere zone, 92 woody perennial species, 111–113
rich and diverse biodiversity, 91 Biotic factor, 59
soil and plant characteristics, 92 Bowdichia, 123
Bacteria populations, 91 Brazilian forestry production and conservation
Bacterial association, 104 program, 4
Bacterial diversity, 93 Brazilian Institute of Forest Development
Belowground biomass (IBDF), 262
acacia growth, 34 Brazilian legal framework
competition, 35 Atlantic Forest protection, 263
diversified soil exploitation, 35, 36 command-and-control regulation, 262
E. grandis root system distribution, 35 constitution and public policies, 262
fine root density, 36, 37 definition, 260
forest environments, 34 deforestation, 261
inter- and intraspecific competition, root economic development approach, 262
development, 34 ecosystem services, 259
plant community root system, 34 Eucalyptus and Acacia, 261
soil resources, 34 FAO, 258, 259
tree stock density, eucalypt, 36 forest-based Brazilian policies (see
Biodiverse agroforestry systems, 210 Forest-based Brazilian policies)
Biodiverse agroforests, 211 government initiatives, 261
Index 273

legal tools, 263 nitrogen cycling, 148

management practices, 259 nitrogen transfers, 148
permissions and possibilities, 264–266 physical factor, 149
planted forests, 259 rhizobia, 149
regulatory mechanisms, 261 soil, low fertility, 148
Brazilian native legume tree species Community structure, 163
A. colubrina, 123 Complementarity index, 27, 29
B. nitida, 123 Consolidated rural area, 260
C. paraense, 123 Controversial management issues, 233
C. robustum, 123 Crop-livestock integration (CLI), 166
C. tomentosum, 123 Cylindrocladium candelabrum, 97
Dalbergia nigra, 124
Eucalyptus spp., 121
fertilizer, 121–123 D
Hymenolobium, 125 Dalbergia nigra, 124
introduced-potential species, 126–128 Deep soil layers, 146, 147
Plathymenia foliolosa, 125 Diameter at breast height (DBH), 19, 244
T. vulgaris, 125 Diazotrophic bacteria, 103, 105, 108, 111, 195
Tachigali vulgaris, 125 Dissolved organic carbon (DOC), 94
Brazilian Rhizobia selection program
Embrapa Agrobiologia, 108
Legumes tree genera, 109 E
MAPA, 109 Ecological equilibrium, 165
nodulation, 108 Economic-based alternatives, 268
roots, individual plants, 108 Ecosystem engineers, 155, 225
trials, Embrapa, 108 Ecosystem function, 194, 210, 212
Brazilian rural properties, 266 Ecosystem services (ES), 3–5, 10, 173–175,
177–179, 181
A. mangium, 208
C agriculture intensification, 210
Cacao-cabruca systems, 248 AMF effects, 209
Cacao-erythrina agroforestry systems, approach, 195, 196
248, 249 atmospheric C, 207
Cacao plantations, 250, 252–253 biodiverse agroforestry systems, 210
Cacao-producing areas, 248 biodiverse agroforests, 211
Cacao shading leguminous tree systems, 248 biodiverse and threatened ecosystems, 194
Capoeiras, 230 biodiversity, 194
Carbon accumulation, 59 classification, 197
Carbon sequestration, 201 concept, 195
Catabolic diversity, 94 conservation of biodiversity, 210
Cation exchange capacity (CEC), 58 cultural services, 200
Climate change, 202 diazotrophic bacteria, 195
Close to Nature Planted Forests (CTNPF), E. grandis, 208
260, 267 energy/industrial purposes, 206
Collaborative Program (CP), 260, 267 environmental economy, 196
Colonization, 143, 146 Eucalyptus-Acacia mixing model, 210
Common International Classification of evaluation and benefits, 196
Ecosystem Services (CICES), 197 fungus types, 209
Common mycorrhizal networks (CMN) global mixture effect, 206
biological factor, 149 incentive mechanisms, 211
chemical factor, 149 intercropping tree species, 208
definition, 147 land sparing, 211
Fabaceae, 149 landscape approach, 211, 212
incipient growth, 148 management of planted forests, 194
274 Index

Ecosystem services (ES) (cont.) soil bacterial community, 96

mixed-planted forests, 205 soil microbiology, 94
monoculture (see Planted forests) Eucalyptus spp.
multifunctional planted forests, 210, 211 Brazilian soil, 17
N fertilizer, 207 breeding programs, 2
N2O emissions, 207 climatic conditions, 17
native forest ecosystems, 194 fast-growing exotic species, 5
non-N2-fixing trees, 207 intercropped system, 3
PCR-DGGE technique, 208 mixed forest plantation, 8
preservation and sustainable, 196 monoculture, 1, 6, 27
provision (supply) services, 199 nitrogen, 2
reforests, 209 produce wood, 20
regulations, 198–199 superior genotypes, 17
socioeconomic and ecological benefits, 211 wood production, 6
soil nitrogen (N) balance, 206 Eucalyptus stands (EST), 165, 166
support services, 197–198 Eucalyptus urophylla, 60
TEEB, 196 Europe Ecosystem Research Network
Ecosystem Services Partnership (ESP), 196 (Alter-Net), 196
Ectomycorrhizal (ECM), 120, 209 Evapotranspiration, 202
Ectomycorrhizal Acacia roots, 147 Executive Committee of the Plan of Cacao
Ectomycorrhizal fungi (ECMF), 140, 141 Farming (CEPLAC), 248
EMBRAPA (Brazilian Agricultural Research
Company), 6, 7, 9, 108
Enchytraeids F
Cognettia sphagnetorum, 166 Firebreaks, 223
cosmopolitan or peregrine, 167 Flood mitigation, 208
densities, 167 Fluorescein diacetate (FDA), 95
organic and conventional horticulture, 167 Forest-based Brazilian policies
pest, 166 Brazilian law on forestry, 264
roles, 166 Brazilian Ministry of Agriculture, 264
Encircling, 233 economic purposes, 266, 267
Enterolobium, 121 economic-based alternatives, 268
Environmental economy, 196 Eucalyptus-Acacia system, 266
Erosion control, 208 landowners, 268
Erythrina, 121 legal reserve areas, 266, 268
Eucalypt breeding, 15 NCCP, 264
Eucalyptus-Acacia consortium, 268 rural properties, 266
Eucalyptus-Acacia system, 266 voluntary commitments, 264
Eucalyptus cultivation, 156 Forest-based fallow systems, 250
Eucalyptus grandis, 60, 160, 162, 168 Forest cover management
Eucalyptus plantations systems, 204
acacia monoculture and mixed Forest management systems, 157
plantations, 95 Forest plantations, 258
bacterial biomass/activity, 94 Forestry ecosystems, 92
bacterial community, 95 Forest sustainability, 128, 208
bacterial diversity, 93 Foundation species, 225
development, 94 Fungi community, 91, 92
direct measurements, 95
indirect measurements, 94
mechanisms, 94 G
multivariate analysis, 94 Geochemical cycling, 182
nutrient cycling, 95 Global mixture effect, 206
proteobacteria phylum, 93 Green cancer, 231
seedlings and adult plantation, 93 Gross domestic product (GDP), 1
Index 275

H decomposer starvation, 69
Hartig net, 140 diazotrophic bacteria, 70
High-diversity-based planted forests, 212 forest plantation, 59, 60
Home field advantage (HFA), 70 forest products, 57
forest residues, 68
high-temperature environments, 72
I internal and external market, 57
Incentive mechanisms, 211 land-use history, 70
Incubation, 71 leaf litter quality, 72
Indole acetic acid (IAA) production, 97 leguminous species, 72
Infrared spectroscopy, 70 microbial community, 70
Inga, 121 N2-fixing species, 58
Intercropped system, 3, 9 non-N2-fixing and N2-fixing species, 68
Intercropping tree species, 208 P supply, 72
Intergovernmental Platform on Biodiversity soil organic, 71
and Ecosystem Services sustainability, 57–58
(IPBES), 196 Litterfall rate, 243
International Union for Conservation of Litter-soil system, 174
Nature (IUCN), 229 Low-molecular-weight nitrogen
Invasive alien species compounds, 118
Acacia silviculture, 222–224
Artocarpus heterophyllus, 222
biological invasion, 222 M
exotic species, 222 Macrofauna
Fabaceae (see Acacia) Chrysomelidae, 158
forest productivity, 221 Curculionidae, 158
Pinus and Eucalyptus, 221 eucalyptus plantations, 158
Isotopic dilution (ID), 112 forest and agricultural land use, 159
forest management, 157
land-use systems, 157, 158
J soil macroinvertebrates, 157
Jacarandá-da-Bahia, 124 soil monolith method, 158
Mesofauna
Enchytraeidae and Isopoda, 160
K forest plantations, 161
Keystone species, 225 microorganisms, 160
Knowledge and Learning Mechanism on mixed plantations, 160
Biodiversity and Ecosystem nematodes and AMF, 161
Services (EKLIPSE), 196 rhizosphere, 162
soil and litter, 159
Microbial biomass, 94, 174, 184
L Microbial community, 70, 92
Labile tissues, 59 Microfauna, 155, 156
Landscape approach, 211, 212 Microorganisms, 93
Land sparing, 211 Millennium Ecosystem Assessment
Land-use systems, 159, 163, 165 (MEA), 197
Leaf area, 203 Mimosa, 123
Leaf area index (LAI), 29, 33 Mineralization, 68, 72
Legal reserve, 260 Minirhizotron method, 147
Litter, 184, 228 Ministry of Agriculture, Livestock and Food
Litter decomposition, 176 Supply (MAPA), 108
aluminum and iron oxides, 70 Mixed forest plantation
carbon assimilation and partitioning, 59, 60 Acacia mangium, 8, 9
climate change and temperature, 72 Acacia spp. (see Acacia spp.)
276 Index

Mixed forest plantation (cont.) soil P concentrations, 245

Aspidosperma polyneuron, 8 sustainable rural development, 241
biodiverse forest plantations, 3 Swietenia macrophylla, 242
breeding programs, 2 timber production, 243
effects, climate change, 2 tropical tree species, 241
EMBRAPA, 9 Molecular technology, 138
Eucalyptus spp. (see Eucalyptus spp.) Morphotypes, 165
fast-growing species, 8 bioindicators, 163
functional characteristics, species, 4 community structure, 163
history, 6, 7 ecological equilibrium, 165
leguminous trees, 8 edaphic properties, 165
Meliaceae family, 7 EST, 165
meta-analysis, 4 functional and structural biodiversity, 163
N2-fixing legume, 3 Hexapoda, 163
N2-fixing legumes, 9 land-use systems, 165
N2-fixing trees, 9 morphotypes, 165
nitrogen, 2 morphotyping, 163
nitrogen fertilizer, 2 soil use and management, 163
non-N2-fixing species, 3 springtail communities, 164
nutrient-poor soils, 9 Multifunctional planted forests, 210, 211
potential species, timber, 8 Multistrata agroforestry systems, 247
restoration, ecosystems, 9 Multistrata production systems, 249
scocioeconomic benefits Mycorrhiza
Brazilian forestry production and AMF, 138–140
conservation program, 4 classification, 138
diversity, products and ecosystem conventional techniques, 138
services, 5 deep soil layers, 146, 147
ecosystem functions, 4 ECMF, 138, 140, 141
ecosystems, 6 mycorrhizal colonization, 138
high-technology equipment, 5 mycorrhizal hyphal system, 137
income, 5 plant roots, 137
nongovernmental organizations, 4 soil fungi, 137
pre-established criteria, 4 vascular plants, 138
small- and medium-sized producers, 5 Mycorrhizal colonization, 138
sites, 4 Mycorrhizal endophytes colonize, 139
soils, 2 Mycorrhizal fungi, 110
species, 2 Mycorrhizal hyphal system, 137
stand growth (see Stand growth) Mycorrhization
water availability, 2 A. mangium, 110
Mixed-planted forests, 205, 210, 212 biomass production, 110
Mixed plantation, 48, 50, 52 complex interactions, 110
Mixed-species plantations field-level, 111
Amazon region, 246 N and P, 110
Atlantic Forest species, 247 nursery conditions, 111
C. goeldiana, 242 Piptadenia gonoacantha, 111
Costa Rica, 246 rhizosphere, 110
empirical evaluations, 244 tree legumes, 111
leguminous tree species, 247
N2-fixing/non-N2-fixing tree
species, 247–253 N
native hardwood species, 243, 245 N fertilizer, 207
native tree, 242–243 N2-fixing and non-N2-fixing plantations
Panama, 247 Albizia monocultures, 75
planted forests, 242 C content, 79
Index 277

climate and soil characteristics, 75 Nitrogen-fixing trees (NFT), 15

feedback effect, 79 Nitrogen-fixing tree species, 126
growth and microbial activity, 76 Nitrogen transfer
isotopic techniques, 75 decomposition, vegetative tissues, 118
linear relationship, 76 ecological relationship, 121
mineralogy and texture, 76 ectomycorrhizae, 120
monocultures, 75, 76 fine roots and nodules, 119
poor structure and aggregation, 79 living tissue, 120
soil morphological and molecular N2-fixing tree, 118–120
levels, 75 non-N-fixing tree, 119
storage of C, 79 plants, 120
N2-fixing/non-N2-fixing tree species root exudation and mycorrhizal, 120
AFS, 247, 249 routes, 120
Amazon region, 249 Nodulating bacteria, 106
artificial cabruca system, 249 Nodulation, 107
cabruca system, 248 Non-N2-fixing trees, 207
cacao-producing areas, 248 No-tillage (NT), 166
CEPLAC, 248 Novel approach, 174
forest-based fallow systems, 250 Nutrient cycling, 22
leguminous, 250 AMF, 184
multistrata agroforestry systems, 247 atmospheric deposition, 46
S. amazonicum, 250 biomass, 49
N2-fixing species decomposition of forest litter, 52
fast-growing eucalypt plantations, 15 dependency, 45
mixed-species plantations, 19 ecological and economic benefits, 183
non-N2-fixing species, 21, 26 ectomycorrhizae, 184
N2-fixing tree, 120 eucalypt plantations, 49
National Climate Change Plan (NCCP), 264 forest trees, 45
National invasion prevention strategies, 234 geochemical cycling, 182
National Policy for Native Vegetation litter, 184
Recovery, 264 litterfall rate, 51, 52
National Policy for the Recovery of Native microbial biomass, 184
Vegetation (Decree 8972/2017), 263 mycorrhizae and BNF, 186
National Policy on Climate Change, 263 N and P concentrations, 186
Native and planted forest, 179, 180 natural ecosystems, 46
Native forest (NF), 166 nitrogen-fixing bacteria, 183
Native forest ecosystems, 194 organic and inorganic forms, 45
Native hardwood species, 243 outputs, 48, 49
Native tree and P cycling, 183
development, 243 plants to soil, 50
ecophysiological conditions, 243 rainfall, 47
ecosystem, 243 redistribution/biochemical, 50
leguminous, 242 rock weathering, 47
litterfall rate, 243 soil organic matter, 185
monocultures, 242, 243 stages, 46
Native Vegetation Protection Law, 4 sustainability, 182, 184, 186
Natural Capital Project, 196 uptake and accumulation, 47, 48
Natural/seminatural ecosystems, 199 wood production, 45
Nematodes, 161 Nutrient deposition
Net primary production (NPP), 59 Brazilian sandy soils, 62
N-fixing trees, 156 C accumulation pattern and partitioning, 61
Nitrogen fertilizer, 2 forest soils, 61
Nitrogen-fixing bacteria (NFB), 143, 176, litterfall mass, 62–67
181, 183 mixed plantations, 62
278 Index

Nutrient deposition (cont.) geographical origin, 201

N2-fixing trees, 61 leaf area, 203
P and N deposition data, 62 legal framework, 258
scatterplot, 61, 62 management strategies, 202
water deficit, 61 micro-basins, 202
monospecific plantations, 258
scenic/cultural services, 204
O silvipastoral system, 205
Organic matter (OM) cycling, 175 soil and climate behavior, 205
types of ES, 201
water consumption, 202
P Planting arrangements, 23
Paris-type mycorrhizae, 144 Planting forests in Brazil
Payments for ecosystem services (PES), 211 aspects, 259
PCR-DGGE technique, 208 legal framework, 262, 268
Perennial pasture (PA), 166 motivations, 257
Permanent Preservation Area (APP) Plathymenia foliolosa, 125
definition, 260 Polluter pays principle, 234
environmental requirements, 261 Principal component analysis, 159
legal reserves needs regulation, 269 Protection of Native Vegetation law, 263
rural properties, 264–266 Pseudosamanea guachapele, 75
Phospholipid fatty acid (PFLA), 94 Public policies, 2
Phosphorus solubilization, 97
Photosynthetically active radiation (PAR), 33
Phytohormone production, 93 R
Pinus taeda, 60 Redundancy analysis (RDA), 162
Plant growth-promoting endophytic bacteria Reforests, 209
bacterial community, 96 Rhizobia, 105
bacterial nutrition, 96 Rhizobium, 105
benefits, 96 Rhizoctonia solani, 97
biodiversity, 97 Root colonization, 144
culture-dependent and -independent
techniques, 96
diazotrophic bacteria, 96, 97 S
growth, 97 Silvicultural management
inoculum, 97 Acacia spp., 20
microbial community, 96 additive series, 23
microorganisms, 98 adequate nutrient supplies and balance, 22
molecular typing technique, 96 A. mangium, 22
vertical transmission, 96 conservation, natural resources, 20
Plantation monocultures, 258 density and design, plantations, 23, 25
Planted forests Eucalptus spp., 20
agrisilviculture, 205 fertilizers, 22
agrosilvopastoral system, 205 forest plantations, 23
anatomical characteristics, 201 K and N doses, 22
benefits, 257 large infiltration, 21
biodiversity, 204 limiting factor, plant productivity, 20
carbon sequestration, 201 maintenance, forest residues, 21
climate change, 202 mechanical and chemical methods, 20
definition, 258 mixed-specie plantations, 23
ecosystem services, 259 mixtures, 21
environmental benefits, 201 N2-fixing species, 21
environmental regularization, 203 nutrient cycling, 22
forest plantations, 259 nutrient-use efficiency, 21
Index 279

planting arrangements, 23 Soil quality

post- and preemergence herbicides, 20 AMF, 176
pre-closure phase, 23 assessment, 173
published mixed-species, 23 biological properties, 178
rotation length, 21 challenges, 177–178
soil compaction, 21 ES, 173, 179
soil preparation, 20, 21 litter decomposition, 176
tree species, 21 litter-soil system, 174, 175
water availability, 20 microbiological and chemical soil
weather conditions, 22 attributes, 176
weed control, 20 mixed/consortiated forest system, 181
Silvicultural programs, 126 native and planted forest
Silvipastoral system, 205 environments, 179–180
Socio-environmental interactions, 235 nutrient cycling, 176, 179
Soil acidification, 228 OM cycling, 175
Soil bacterial community soil biota, 174
Eucalyptus plantations (see also soil functions, 174
Eucalyptus plantations) soil microorganism processes (see Nutrient
functioning, 92 cycling)
Soil C stocks soil-, water-, and nutrient-use
biogeochemical cycles, 81 efficiency, 174
biological resources, 80 SOM, 174
crop fertilization, 81 sustainability, 174, 175
Eucalyptus, 69, 74 Soil resources, 34
foresters, 80 Stand growth
legumes, 81 intra- and inter-specific interactions
mechanisms, 72 benefits and processes, 25
microbial formation pathway, competition, 16, 25, 26
73, 81 complementarity, 26
mixed plantations, 73 contrasting morphological and
natural and planted forests, 73 physiological traits, 26
N-fixing trees, 77, 78 ecological interactions, 26–29
nutrient management, 81 indirect facilitation, 26
plants and microorganisms, 81 mixed-species plantations, 25
priming effects, 73 monocultures, 25
soil bacteria and fungi, 72 N2-fixing species, 26
tropical climatic zone, 80 N2-fixing trees, 26
Soil ecology, 177 soil nitrogen balance, 25
Soil fauna soil and climatic conditions
abundance and diversity, 156 acacia, 16
ecosystem engineers, 155 biomass production, 19
ecosystem processes and services, 156 Brazilian sites, 17
enchytraeids (see Enchytraeids) climatic characteristics, 16, 17
macrofauna (see Macrofauna) eucalypt monoculture, 17
mesofauna (see Mesofauna) N2-fixing species, 19
microfauna, 155, 156 soil, 18
microorganisms, 156 Southeastern Brazilian coast, 18
N-fixing trees, 156 stem wood biomass, 19
Soil microbial community, 95 stem wood production, E50A50, 19
Soil microbiology, 94 tropical and subtropical sites, 17
Soil monolith method, 158 weather, 19
Soil nitrogen (N) balance, 206 wood productivity, 19
Soil organic matter (SOM), 58, 174 Stress-gradient hypothesis (SGh), 27
Soil preparation, 20 Sucupira, 123
280 Index

Sustainability, 92, 94, 96, 182, 184, 186 The Economics of Ecosystems and
AFS, 247 Biodiversity (TEEB), 196
mixed-species plantations, 242 Total belowground C fluxes (TBCF), 60
multistrata production systems, 249 Tropical Soil Biology and Fertility (TSBF),
systematic research, 254 157, 167
Symbiosis in Eucalyptus sp. and Tropical soils, 104
Acacia sp.
AMF fungi, 142
colonization rate, 142, 143 V
ECM fungus, 146 Vila Velha State Park (PEVV), 230
ECMF colonization rate, 142 Vinhático trees, 125
high-throughput sequencing, 145
host preferences and selectivity, 145
mycorrhizal fungi, 141 W
NFB, 143 Water availability, 20
Paris-type mycorrhizae, 144 Water bodies, 200
root colonization, 143 Water funds, 196
roots, 141 Water supply, 60
spores and colonization, 144 Weed control, 20
structure, mycorrhiza, 141 Windbreaks, 223
symbiotic fungal communities, 142 Wood, 123
Symbiotic nitrogen-fixing bacteria, 92 Woody perennial species, 112
Synergistic response, 110 ARA, 112
B-value, 112
greenhouse (pots)/field conditions, 112
T ID, 112
Tachigali vulgaris, 125 N balance and accretion method, 112
Taxonomy, 105 15
N enrichment, 112