Journal of Biogeography (J. Biogeogr.

) (2010) 37, 1407–1413

GUEST Identifying refugia from climate change

EDITORIAL
Michael B. Ashcroft*

Australian Museum, 6 College Street, Sydney, ABSTRACT

NSW 2010, Australia
This article highlights how the loose definition of the term ‘refugia’ has led to
discrepancies in methods used to assess the vulnerability of species to the current
trend of rising global temperatures. The term ‘refugia’ is commonly used without
distinguishing between macrorefugia and microrefugia, ex situ refugia and in situ
refugia, glacial and interglacial refugia or refugia based on habitat stability and
refugia based on climatic stability. It is not always clear which definition is being
used, and this makes it difficult to assess the appropriateness of the methods
employed. For example, it is crucial to develop accurate fine-scale climate grids
when identifying microrefugia, but coarse-scale macroclimate might be adequate
for determining macrorefugia. Similarly, identifying in situ refugia might be more
appropriate for species with poor dispersal ability but this may overestimate the
extinction risk for good dispersers. More care needs to be taken to properly define
the context when referring to refugia from climate change so that the validity of
methods and the conservation significance of refugia can be assessed.

Keywords
*Correspondence: Michael B. Ashcroft,
Bioclimatic envelope models, climatic stability, conservation biogeography,
Australian Museum, 6 College Street, Sydney,
NSW 2010, Australia. cryptic refugia, ecological niche models, extinction risk, interglacial refugia,
E-mail: mick.ashcroft@austmus.gov.au macrorefugia, microclimate, microrefugia.

prefer cooler climates are generally restricted to refugia during

INTRODUCTION
interglacial periods (Stewart et al., 2010). Both glacial and
The importance of refugia is increasingly being recognized interglacial refugia should be conserved to ensure long-term
(Noss, 2001; Petit et al., 2003; Bennett & Provan, 2008). While persistence of species (Skov & Svenning, 2004); however, it is
the term was originally introduced to refer to locations where the species that prefer cooler conditions that are of most
species survived the last glacial period (Bennett & Provan, immediate concern as they are currently restricted to intergla-
2008), it is now increasingly used to refer to areas that should cial refugia and face increased threat with further rises in global
be conserved to limit the impacts of rising global temperatures temperatures. Present-day average global temperatures are
in the 21st century (Barnosky, 2008; Trivedi et al., 2008; c. 2 C cooler than the previous interglacial (Jouzel et al.,
Williams et al., 2008; Rull, 2009). However, the broadening 1987), but there are spatial and seasonal differences in this
usage of the term has introduced apparent contradictions in relationship and some locations are already warmer than the
methodology and potentially decreased its usefulness (Bennett last interglacial during some seasons (Kubatzki et al., 2000;
& Provan, 2008). This article provides an overview of different Montoya et al., 2000; Kaspar et al., 2005). In addition,
interpretations of climate change refugia and highlights some temperatures are expected to rise by a further 1.1–6.4 C
of the methodological discrepancies and potential problems during the 21st century (IPCC, 2007), and this will place
that can result (Table 1). Authors need to explicitly address additional stress on species that prefer cooler temperatures and
these inconsistencies or the ecological significance of refugia are currently restricted to interglacial refugia.
will be ambiguous, thus confounding their conservation value. Refugia from 21st century climate change will differ from
current interglacial refugia in that temperatures will be warmer
and species will have to cope with landscapes that have been
REFUGIA FROM CLIMATE CHANGE
fragmented by humans (Vos et al., 2008). If refugia are
Taxa that prefer warmer climates generally contract their restricted to locations that remain suitable for a species (in situ
distributions to refugia during glacial periods, while taxa that refugia; Attorre et al., 2007; VanDerWal et al., 2009), then

ª Australian Museum 2010 www.blackwellpublishing.com/jbi 1407

doi:10.1111/j.1365-2699.2010.02300.x
M. B. Ashcroft

Table 1 A list of potential issues that could arise when identifying inter-annual protection from drought conditions (Manning
refugia from climate change. et al., 2007). These definitions of refugia could also be
extended to include climate change impacts, for example by
Potential methodological issues
management actions that create thermally buffered environ-
Limiting studies to in situ refugia might exaggerate extinction risk for ments such as nest boxes (Williams et al., 2008). While
good dispersers, while including ex situ refugia might underestimate attempts have been made to distinguish between refugia and
extinction risk for poor dispersers or where there are barriers to refuges (e.g. Rull, 2009), corresponding rules are not always
dispersal followed. This highlights the need to replace the term ‘refugia’
The minimum viable size of refugia depends on body size and area with a more descriptive term and to clarify the context in
required to support the population, and therefore the relevant scale of which refugia is used (Bennett & Provan, 2008).
macrorefugia and microrefugia will be taxon specific
Throughout this article the term ‘refugia’ is used for areas
Macrorefugia can be identified using commonly used climate grids
that are at least large enough to support a small population of
based on elevation-sensitive interpolations (e.g. BioClim and
WorldClim), but microrefugia require fine-scale climate surfaces that
some species (e.g. c. 100–10,000 m2 or more), while individual
consider a broader range of climate-forcing factors shelters such as rocks and nest boxes are regarded as ‘refuges’
Refugia based only on climate stability are limited to in situ refugia, and are not considered further. However, this arbitrary
and may be misleading if species in more climatically stable areas are classification is biased towards plants and vertebrates, and
more sensitive to change smaller species, such as invertebrates, may be able to maintain
Refugia based on habitat stability may be biased towards cooler viable populations in climate change refugia at finer scales.
locations if climate stability is ignored (uniform warming), and these Once again, the taxon specific variations in the scale of refugia
will be biased towards high elevations if climate surfaces neglect other highlight the need to clarify the definition and interpretation
climate-forcing factors of refugia.
Refugia based on climate stability or community composition may
include non-refugial species unless they demonstrate a contraction in
distribution for individual species MICROREFUGIA AND MACROREFUGIA
Species distribution models (SDMs) need to predict where, and for how
long, species can persist in areas where habitat has become Although refugia can be examined at a continuum of scales,
unfavourable if they are to comprehensively predict species persistence they have been broadly classified as either macrorefugia
(classical refugia) or microrefugia (cryptic refugia; Bennett &
Provan, 2008; Holderegger & Thiel-Egenter, 2009; Rull, 2009).
For example, during the last glacial period large areas with
refugia from 21st century climate change will occupy a subset favourable regional climate in southern Europe acted as
of the locations where interglacial refugia currently occur macrorefugia for temperate taxa, while small areas with
(areas that are cooler than the surrounding region are expected unusual microclimate in northern Europe acted as microref-
to shrink as the climate warms; Ohlemüller et al., 2008). ugia. The climate grids needed to identify microrefugia differ
However, some species can survive periods of unfavourable from those needed to identify macrorefugia, yet the term
climate in locations that they did not occupy previously ‘refugia’ is sometimes used without distinguishing between the
(ex situ refugia; Loarie et al., 2008; Holderegger & Thiel- two. This is an unfortunate oversight, as it makes it difficult to
Egenter, 2009). Identifying in situ refugia from climate change assess the appropriateness of the climate grids used.
might be more appropriate for species with poor dispersal or The responses of species to climate change are often
where human land-use changes have created barriers, but this identified using coarse-scale species distribution models
might exaggerate the extinction risk for good dispersers. (SDMs; Pearson & Dawson, 2003; Thomas et al., 2004), yet
Potential ex situ refugia that were previously unreachable may these may overestimate extinction risk because the climate
become available if humans assist colonizations or create new grids used by these models are too coarse to predict the
corridors (Hunter, 2007; Vos et al., 2008). The choice between location of microrefugia (Thuiller et al., 2005; Araújo &
in situ and ex situ climate change refugia is therefore an Rahbek, 2006; Pearson, 2006). For example, commonly used
important aspect that should be justified in terms of species climate grids, such as BioClim (Houlder et al., 2003) and
dispersal capabilities. This choice is analogous to the assump- WorldClim (Hijmans et al., 2005), are developed using
tion in species distribution models that species either have no elevation-sensitive interpolations from weather stations. While
dispersal (in situ refugia only) or universal dispersal (both in these methods are suitable at coarse resolutions, the climate
situ and ex situ refugia; Thomas et al., 2004; Pearson, 2006). surfaces cannot simply be downscaled to finer resolutions as
The differences between in situ and ex situ refugia illustrate they neglect climate-forcing factors that operate over small
the confusion that arises when the term ‘refugia’ is used distances (< 10 km; Daly, 2006). Local climates are also
without clarifying definitions and context. For example, the affected by cold air drainage, streams, oceans, lakes and
terms ‘refugia’ and ‘refuge’ are used at a variety of spatial and topographic exposure to winds and radiation (Lookingbill &
temporal scales, including intra-day shelters from predators Urban, 2003; Daly, 2006; Ashcroft et al., 2008; Fridley, 2009;
(Monasterio et al., 2009), small patches of forest left undis- Bennie et al., 2010), all of which are neglected when temper-
turbed during forest harvesting (Perhans et al., 2009) and atures are interpolated or downscaled based only on elevation

1408 Journal of Biogeography 37, 1407–1413

ª Australian Museum 2010
 Identifying refugia from climate change

or other simplistic methods (e.g. Saxon et al., 2005; Trivedi VanDerWal et al., 2009). Although locations that are stable in
et al., 2008; Vos et al., 2008; VanDerWal et al., 2009). climate are likely to be stable in habitat for many species, the
Studies that use simplified climate grids based only on methodological issues that arise from the two different
elevation need to be clear that they can only capture definitions deserve closer attention and are discussed in detail
macrorefugia, regardless of spatial resolution, because they in the remainder of this section.
do not consider the climate-forcing factors that create unusual Locations that are stable in climate are defined without
local variations from the regional climate. Studies that attempt reference to any particular species, yet they are topographically
to identify microrefugia need to provide specific details on and geographically biased in their locations and will only
how the fine-scale climate surfaces were derived, as the climate capture a subset of species in a region (Ashcroft et al., 2009;
surfaces are crucial for assessing the appropriateness of the Fridley, 2009). In some landscapes, localities with low summer
methods. Fine-scale climate grids need to be developed using maximum temperatures have received less warming than
large networks of temperature sensors across a broad range of warmer localities, and therefore microrefugia are expected to
environments. It is not possible to simply interpolate obser- help protect the species that are most at risk in a warming
vations from a sparse network of weather stations that are climate (Ashcroft et al., 2009). In these cases, as warmer
biased towards environments such as flat, low-elevation or localities experience larger increases in temperature than cooler
unvegetated areas (Lookingbill & Urban, 2003; Ashcroft et al., localities, it also raises the possibility that climate change will
2008; Fridley, 2009; Bennie et al., 2010). increase the length of landscape-scale temperature gradients
Another alternative is to use coarse-scale climate surfaces (Fridley, 2009). This could create higher environmental
and the within-cell elevational range to predict whether there diversity (Faith & Walker, 1996; Faith, 2003), and therefore
are microrefugia somewhere within grid cells (Luoto & lead to higher landscape-scale biological diversity if new
Heikkinen, 2008; Vetaas & Ferrer-Castán, 2008; Randin et al., species that prefer warmer conditions are able to disperse to
2009). Ironically, this coarse-scale method may be more the area.
successful at identifying the approximate location of micro- This trend of cooler locations warming less than warmer
refugia than fine-scale models that use climate surfaces only locations is not universally applicable, however. At the global
based on elevation (Trivedi et al., 2008; VanDerWal et al., scale the colder polar regions are warming more than the
2009). This is because topography creates complex mosaics of global average and overall global diversity is predicted to
exposure to wind and radiation, and sheltered locations may decrease (Hughes, 2000; Thomas et al., 2004). At the landscape
be buffered from regional climate change (Hampe & Petit, scale, winter minimum temperatures decrease further from the
2005; Williams et al., 2008; Ashcroft et al., 2009). Deep gorges, coast and more warming is expected to occur in these cooler
such as those that provide microrefugia for the Wollemi pine locations (Ashcroft et al., 2008, 2009). Winter minima are
(Wollemia nobilis) in Australia (Offord et al., 1999), are generally increasing more than summer maximum tempera-
predicted to be warmer than the surrounding area if climate tures (Hughes, 2000; Ashcroft et al., 2009), and therefore
surfaces are based only on elevation, but are actually cooler refugia from rising winter minimum temperatures may have
when topographic shelter is considered (Ashcroft et al., 2008). greater conservation significance.
Both microrefugia and macrorefugia are of conservation In the context of the current warming trend, less warming is
interest. Larger refugia are expected to provide a more secure generally expected to occur in locations that are nearer to
buffer against extinction, and will be needed for large-bodied streams or coastlines, or where there is cold air drainage,
animals or species with large home ranges (Stewart et al., higher soil moisture, higher canopy cover, higher elevation or
2010). However, as temperatures increase, microrefugia can less exposure to hot winds and radiation (Kennedy, 1997;
persist even once the regional climate is unsuitable and no Noss, 2001; Bennett & Provan, 2008; Ashcroft et al., 2009;
macrorefugia remain. This means that microrefugia have the Fridley, 2009). However, the relative effect of these factors will
potential to withstand a greater amount of warming than vary between seasons and locations. For example, the trend of
macrorefugia. Microrefugia may also be the only conservation decreased warming with elevation is stronger in tropical zones,
option for rare or threatened species that exist in small with the trend outside the tropics obscured by snow–ice
fragmented populations (Maschinski et al., 2006). feedback and greater warming near the 0 C isotherm (Pepin &
Lundquist, 2008).
One problem with defining refugia with respect to climatic
ARE REFUGIA STABLE IN CLIMATE OR
stability is that species that are adapted to climatically stable
HABITAT?
locations may be more susceptible to changes than are other
There is confusion as to whether refugia should be defined species (Williams et al., 2008). Even if a cool gorge experiences
with respect to stability in climate or habitat. Some have half the warming of more exposed ridges, the biological
suggested that microrefugia are locations where the climate is impacts may be equivalent. Another problem is that climatic
more stable (or has less warming) than the surrounding areas stability could be defined with respect to a number of factors,
(Saxon et al., 2005; Ashcroft et al., 2009; Fridley, 2009; Rull, including winter minimum temperatures, summer maximum
2009). However, SDMs are typically used to predict stability in temperatures or humidity (Barnosky, 2008). The location of
habitat rather than stability in climate (Attorre et al., 2007; refugia from climate change would vary according to which

Journal of Biogeography 37, 1407–1413 1409

ª Australian Museum 2010
M. B. Ashcroft

parameters were chosen, and this would also affect which which is at least risk under a warming climate, is at most risk
species were protected. Although climatic stability may play a under a cooling climate if climatic stability is ignored (Fig. 1a).
large role in determining the location of in situ refugia, SDMs However, the same site can have higher habitat stability under
are still needed to determine which species may be able to both warming and cooling climates when climatic stability is
persist in ex situ refugia, and to determine the species-specific considered (Fig. 1b).
risks of extinction based on changes in multiple environmental The implications are even more dramatic when considering
factors. that commonly used climate surfaces such as BioClim
Habitat stability is species specific, and therefore the (Houlder et al., 2003) and WorldClim (Hijmans et al., 2005)
location of refugia will differ among species. While habitat are based on elevation-sensitive interpolations. The assump-
stability is undoubtedly influenced by climatic stability, SDMs tion of uniform warming will potentially over-emphasize the
sometimes assume there is uniform warming or downscale importance of the coldest locations in the landscape (Fig. 1),
global climate models in a manner that would result in nearly and the assumption that temperatures are correlated with
uniform warming at fine scales (see references in Beaumont elevation will result in these being at higher elevations. There is
et al., 2007; Trivedi et al., 2008; and VanDerWal et al., 2009). thus the danger that SDMs will identify refugia from climate
Under these circumstances, cooler locations will almost change at higher elevations simply based on the assumptions
inevitably be less susceptible to warming than warmer that were made during the modelling process rather than based
locations as they can withstand a larger increase in regional on the ecology or distribution of the species. Microrefugia are
climate before the habitat becomes unsuitable (Fig. 1a). known to occur in sheltered locations at lower elevations, and
However, it is possible that a warmer site could have higher the methods employed to locate them should be capable of
habitat stability if it had higher climatic stability (Fig. 1b). The capturing the unique climates in these topographic positions.
differences are more apparent when considering refugia from a Therefore, it is important to consider variations in climatic
cooling climate. Under these circumstances, the cooler site, stability, even when using a definition of refugia based on
habitat stability.
Studies therefore need to include both climatic stability and
(a)
habitat stability in studies of refugia. While this may not be a
problem at coarse scales, where SDMs are widely employed
and spatial variations in climate change are well studied,
further work is needed to adequately address both these factors
when locating microrefugia.

REDUCTION IN DISTRIBUTION
A key attribute of refugia is a reduction in species
distributions. This usually involves a reduction in overall
range size, but it is also possible that a species’ overall range
may be more or less maintained while it contracts its
(b) distribution to a number of microrefugia within that range
(Bennett & Provan, 2008). While the term ‘refugia’ is
generally used with respect to contractions and expansions
that have occurred over glacial and interglacial periods in
the Quaternary (e.g. Stewart et al., 2010), there are also
contractions and expansions that have been occurring over
longer time periods. For example, Bennett & Provan (2008)
highlight examples of species that have been expanding their
range sizes in a stepwise manner during the glacial and
interglacial periods of the Quaternary. Conversely, the
gradual shift of Australia and South America towards the
equator has caused some species to contract their ranges in a
stepwise manner (Kershaw, 1986; Ledru et al., 2007). Climate
Figure 1 The bell curves illustrate the relationship between
change could further reduce the distribution of these species,
habitat suitability and temperature for a hypothetical species. Two
demonstrating that climate change refugia need not be
locations, A and B, are subjected to global warming which raises
their temperature to A¢ and B¢ respectively. Site A is less suscep- limited to species that expand and contract their ranges in
tible to global warming under the assumption of uniform warming the glacial and interglacial periods. Similarly, even species
(a) because it is a cooler location. However, if site B was more that prefer warmer conditions and have initially expanded
climatically stable (b), then it could be less susceptible to warming during the current interglacial period may eventually reach a
than site A even if it was originally warmer. limit and begin to contract.

1410 Journal of Biogeography 37, 1407–1413

ª Australian Museum 2010
 Identifying refugia from climate change

Species distribution models typically predict that many necessary to know how long the climate will be warmer than
species will contract their distributions under climate change ‘normal’ interglacial conditions so that the probability of
(e.g. Thomas et al., 2004; Thuiller et al., 2005; Svenning & Skov, persistence in refugia can be estimated.
2006; Coetzee et al., 2009). Therefore, restricting the term
‘refugia’ to species that have contracted in range size is unlikely
CONCLUDING REMARKS
to hinder studies predicting refugia from 21st century climate
change. Indeed, any study that uses coarse-scale SDMs to predict Refugia need to be identified and protected across multiple
future distributions is effectively identifying macrorefugia from spatial and temporal scales (Noss, 2001). While the trend of
climate change if a range contraction occurs. Nevertheless, if a rising global temperatures poses immediate threats, long-term
contraction in distribution is a requirement for the use of the survival of species depends on protecting both glacial and
term ‘refugia’, then this needs to be demonstrated. A species interglacial refugia (Skov & Svenning, 2004) as well as refugia
that has continued to exist in a small area is unlikely to be from climate change, and these may not coincide. The variety
regarded as a refugial population if there is no expansion and of species responses to climate change (Bennett & Provan,
contraction (Bennett & Provan, 2008). 2008) and the methodological discrepancies highlighted in this
Range contractions are also problematic for methods that article illustrate the need to improve the terminology and
identify refugia based on climatic stability (see the previous clarify the context to which the term ‘refugia’ is applied. This
section), the compositional irreplaceability of locations (Coet- article has highlighted a number of potential methodological
zee et al., 2009) or other methods based on the expected issues that could arise when identifying refugia from climate
response of multiple species. Unless these methods estimate change (Table 1), and clarifying the context of refugia in each
the range change for individual species, they may be based to study would help avoid these pitfalls. It would be beneficial to
some degree on rare or restricted species where no contraction replace the general term ‘refugia’ with more distinct terms such
in distribution occurs. Indeed, as species respond individual- as ‘interglacial microrefugia’ (Rull, 2009) or ‘microclimatic
istically to climate change, it makes sense to limit the definition refugia’ (Trivedi et al., 2008); however, even these leave some
of refugia to individual species (as per Stewart et al., 2010). ambiguities with regard to in situ versus ex situ refugia and
This does not prevent other terms, such as ‘ecosystem climatic stability versus habitat stability. If studies are based on
hotspots’ (Vos et al., 2008), being used to refer to locations a clearer definition of refugia (e.g. Stewart et al., 2010), it will
where refugia for multiple species coincide, and this might be help others to assess the appropriateness of the methods
beneficial from a conservation perspective. employed and place their results in the appropriate ecological
context.

SPECIES PERSISTENCE
ACKNOWLEDGEMENTS
The conservation value of refugia reflects their ability to allow
species to persist during periods of unfavourable climate. As This manuscript was significantly improved through conver-
the distribution of the species contracts to a smaller area, the sations with John Gollan and comments from Richard Pearson
probability of extinction is increased, and this risk increases the and two anonymous referees.
longer the unfavourable conditions last (Stewart et al., 2010).
However, species persistence is also affected by the quality of
REFERENCES
the habitat in refugia. Species may even be able to persist for a
limited time after their habitat becomes unsuitable. Examples Araújo, M.B. & Rahbek, C. (2006) How does climate change
include seeds stored in the soil bank, or species that can affect biodiversity? Science, 313, 1396–1397.
survive as adults for long periods even when conditions are Ashcroft, M.B., Chisholm, L.A. & French, K.O. (2008) The
not suitable for reproduction. These species are effectively effect of exposure on landscape scale soil surface tempera-
committed to extinction (Thomas et al., 2004), and it may be tures and species distribution models. Landscape Ecology, 23,
more appropriate to refer to these as relict populations than 211–225.
refugial populations (Hampe & Petit, 2005). However, even Ashcroft, M.B., Chisholm, L.A. & French, K.O. (2009) Climate
these relicts could have conservation value if the trend in change at the landscape scale: predicting fine-grained spatial
climate change reversed in future, and they can recover when heterogeneity in warming and potential refugia for vegeta-
conditions become favourable again. tion. Global Change Biology, 15, 656–667.
If the term ‘refugia’ is used to refer purely to species that Attorre, F., Francesconi, F., Taleb, N., Scholte, P., Saed, A.,
have contracted in range, then this definition would also Alfo, M. & Bruno, F. (2007) Will dragonblood survive the
include long-lived species surviving in unsuitable habitat. This next period of climate change? Current and future potential
is problematic for SDMs, as it requires them to identify distribution of Dracaena cinnabari (Socotra, Yemen).
previously suitable habitat, estimate how long the adults or Biological Conservation, 138, 430–439.
seeds could survive under unfavourable conditions, and Barnosky, A.D. (2008) Climatic change, refugia, and bio-
determine whether they could recover in future. Even if these diversity: where do we go from here? An editorial comment.
relicts are excluded from the definition of refugia, it is still Climatic Change, 86, 29–32.

Journal of Biogeography 37, 1407–1413 1411

ª Australian Museum 2010
M. B. Ashcroft

Beaumont, L.J., Pitman, A.J., Poulsen, M. & Hughes, L. (2007) Change. Available at: http://www.ipcc.ch (accessed 18
Where will species go? Incorporating new advances in December 2009).
climate modelling into projections of species distributions. Jouzel, J., Lorius, C., Petit, J.R., Genthon, C., Barkov, N.I.,
Global Change Biology, 13, 1368–1385. Kotlyakov, V.M. & Petrov, V.M. (1987) Vostok ice core: a
Bennett, K.D. & Provan, J. (2008) What do we mean by continuous isotope temperature record over the last climatic
‘refugia’? Quaternary Science Reviews, 27, 2449–2455. cycle (160,000 years). Nature, 329, 403–408.
Bennie, J.J., Wiltshire, A.J., Joyce, A.N., Clark, D., Lloyd, A.R., Kaspar, F., Kühl, N., Cubasch, U. & Litt, T. (2005) A model-
Adamson, J., Parr, T., Baxter, R. & Huntley, B. (2010) data comparison of European temperatures in the Eemian
Characterising inter-annual variation in the spatial pattern of interglacial. Geophysical Research Letters, 32, L11703.
thermal microclimate in a UK upland using a combined Kennedy, A.D. (1997) Bridging the gap between general cir-
empirical–physical model. Agricultural and Forest Meteorology, culation model (GCM) output and biological microenvi-
150, 12–19. ronments. International Journal of Biometeorology, 40,
Coetzee, B.W.T., Robertson, M.P., Erasmus, B.F.N., van 119–122.
Rensburg, B.J. & Thuiller, W. (2009) Ensemble models Kershaw, A.P. (1986) Climatic change and Aboriginal burning
predict Important Bird Areas in southern Africa will in north-east Australia during the last two glacial/interglacial
become less effective for conserving endemic birds under cycles. Nature, 322, 47–49.
climate change. Global Ecology and Biogeography, 18, Kubatzki, C., Montoya, M., Rahmstorf, S., Ganopolski, A. &
701–710. Claussen, M. (2000) Comparison of the last interglacial
Daly, C. (2006) Guidelines for assessing the suitability of climate simulated by a coupled global model of intermediate
spatial climate data sets. International Journal of Climatology, complexity and an AOGCM. Climate Dynamics, 16,
26, 707–721. 799–814.
Faith, D.P. (2003) Environmental diversity (ED) as surrogate Ledru, M.P., Salatino, M.L.F., Ceccantini, G., Salatino, A.,
information for species-level biodiversity. Ecography, 26, Pinheiro, F. & Pintaud, J.C. (2007) Regional assessment of
374–379. the impact of climatic change on the distribution of a
Faith, D.P. & Walker, P.A. (1996) How do indicator groups tropical conifer in the lowlands of South America. Diversity
provide information about the relative biodiversity of and Distributions, 13, 761–771.
different sets of areas?: on hotspots, complementarity and Loarie, S.R., Carter, B.E., Hayhoe, K., McMahon, S., Moe, R.,
pattern-based approaches. Biodiversity Letters, 3, 18–25. Knight, C.A. & Ackerly, D.D. (2008) Climate change and
Fridley, J.D. (2009) Downscaling climate over complex terrain: the future of California’s endemic flora. PLoS ONE, 3,
high finescale (<1000 m) spatial variation of near-ground e2502.
temperatures in a montane forested landscape (Great Smoky Lookingbill, T.R. & Urban, D.L. (2003) Spatial estimation of
Mountains). Journal of Applied Meteorology and Climatology, air temperature differences for landscape-scale studies in
48, 1033–1049. montane environments. Agricultural and Forest Meteorology,
Hampe, A. & Petit, R.J. (2005) Conserving biodiversity under 114, 141–151.
climate change: the rear edge matters. Ecology Letters, 8, Luoto, M. & Heikkinen, R.K. (2008) Disregarding topo-
461–467. graphical heterogeneity biases species turnover assessments
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, based on bioclimatic models. Global Change Biology, 14,
A. (2005) Very high resolution interpolated climate surfaces 483–494.
for global land areas. International Journal of Climatology, Manning, A.D., Lindenmayer, D.B., Barry, S.C. & Nix, H.A.
25, 1965–1978. (2007) Large-scale spatial and temporal dynamics of the
Holderegger, R. & Thiel-Egenter, C. (2009) A discussion of vulnerable and highly mobile superb parrot. Journal of
different types of glacial refugia used in mountain bio- Biogeography, 34, 289–304.
geography and phylogeography. Journal of Biogeography, 36, Maschinski, J., Baggs, J.E., Quintana-Ascencio, P.F. & Menges,
476–480. E.S. (2006) Using population viability analysis to predict the
Houlder, D., Hutchinson, M., Nix, H. & McMahon, J. (2003) effects of climate change on the extinction risk of an
ANUCLIM 5.1 user’s guide. Australian National University, endangered limestone endemic shrub, Arizona cliffrose.
Canberra, ACT. Conservation Biology, 20, 218–228.
Hughes, L. (2000) Biological consequences of global warming: Monasterio, C., Salvador, A., Iraeta, P. & Dı́az, J.A. (2009) The
is the signal already apparent? Trends in Ecology and effects of thermal biology and refuge availability on the
Evolution, 15, 56–61. restricted distribution of an alpine lizard. Journal of Bioge-
Hunter, M.L., Jr (2007) Climate change and moving species: ography, 36, 1673–1684.
furthering the debate on assisted colonization. Conservation Montoya, M., von Storch, H. & Crowley, T.J. (2000) Climate
Biology, 21, 1356–1358. simulation for 125 kyr BP with a coupled ocean–atmosphere
IPCC (2007) Climate change 2007: the physical science basis, general circulation model. Journal of Climate, 13,
AR4 synthesis report. Intergovernmental Panel on Climate 1057–1072.

1412 Journal of Biogeography 37, 1407–1413

ª Australian Museum 2010
 Identifying refugia from climate change

Noss, R.F. (2001) Beyond Kyoto: forest management in a time Svenning, J.-C. & Skov, F. (2006) Potential impact of climate
of rapid climate change. Conservation Biology, 15, 578–590. change on northern nemoral forest herb flora of Europe.
Offord, C.A., Porter, C.L., Meagher, P.F. & Errington, G. Biodiversity and Conservation, 15, 3341–3356.
(1999) Sexual reproduction and early plant growth of the Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M.,
Wollemi pine (Wollemia nobilis), a rare and threatened Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de
Australian conifer. Annals of Botany, 84, 1–9. Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L.,
Ohlemüller, R., Anderson, B.J., Araújo, M.B., Butchart, Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L.,
S.H.M., Kudrna, O., Ridgley, R.S. & Thomas, C.D. (2008) Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L. &
The coincidence of climatic and species rarity: high risk to Williams, S.E. (2004) Extinction risk from climate change.
small-range species from climate change. Biology Letters, 4, Nature, 427, 145–148.
568–572. Thuiller, W., Lavorel, S., Araújo, M.B., Sykes, M.T. & Prentice,
Pearson, R.G. (2006) Climate change and the migration capacity I.C. (2005) Climate change threats to plant diversity in
of species. Trends in Ecology and Evolution, 21, 111–113. Europe. Proceedings of the National Academy of Sciences
Pearson, R.G. & Dawson, T.P. (2003) Predicting the impacts of USA, 102, 8245–8250.
climate change on the distribution of species: are bioclimatic Trivedi, M.R., Berry, P.M., Morecroft, M.D. & Dawson, T.P.
envelope models useful? Global Ecology and Biogeography, (2008) Spatial scale affects bioclimatic model projections of
12, 361–371. climate change impacts on mountain plants. Global Change
Pepin, N.C. & Lundquist, J.D. (2008) Temperature trends at Biology, 14, 1089–1103.
high elevations: patterns across the globe. Geophysical VanDerWal, J., Shoo, L.P. & Williams, S.E. (2009) New
Research Letters, 35, L14701. approaches to understanding late Quaternary climate fluc-
Perhans, K., Appelgren, L., Jonsson, F., Nordin, U., Söder- tuations and refugial dynamics in Australian wet tropical
ström, B. & Gustafsson, L. (2009) Retention patches as rain forests. Journal of Biogeography, 36, 291–301.
potential refugia for bryophytes and lichens in managed Vetaas, O.R. & Ferrer-Castán, D. (2008) Patterns of woody
forest landscapes. Biological Conservation, 142, 1125–1133. plant species richness in the Iberian Peninsula: environ-
Petit, R.J., Aguinagalde, I., de Beaulieu, J.-L., Bittkau, C., mental range and spatial scale. Journal of Biogeography, 35,
Brewer, S., Cheddadi, R., Ennos, R., Fineschi, S., Grivet, D., 1863–1878.
Lascoux, M., Mohanty, A., Müller-Starck, G., Demesure- Vos, C.C., Berry, P., Opdam, P., Baveco, H., Nijhof, B.,
Musch, B., Palmé, A., Martin, J.P., Rendell, S. & Vendramin, O’Hanley, J., Bell, C. & Kuipers, H. (2008) Adapting
G.G. (2003) Glacial refugia: hotspots but not melting pots of landscapes to climate change: examples of climate-proof
genetic diversity. Science, 300, 1563–1565. ecosystem networks and priority adaption zones. Journal of
Randin, C.F., Engler, R., Normand, S., Zappa, M., Zimmer- Applied Ecology, 45, 1722–1731.
mann, N.E., Pearman, P.B., Vittoz, P., Thuiller, W. & Gui- Williams, S.E., Shoo, L.P., Isaac, J.L., Hoffmann, A.A. &
san, A. (2009) Climate change and plant distribution: local Langham, G. (2008) Towards an integrated framework
models predict high-elevation persistence. Global Change for assessing the vulnerability of species to climate change.
Biology, 15, 1557–1569. PLoS Biology, 6, 2621–2626.
Rull, V. (2009) Microrefugia. Journal of Biogeography, 36,
481–484.
Saxon, E., Baker, B., Hargrove, W., Hoffman, F. & Zganjar, C.
(2005) Mapping environments at risk under different global BIOSKETCH
climate change scenarios. Ecology Letters, 8, 53–60.
Skov, F. & Svenning, J.-C. (2004) Potential impact of climate Michael B. Ashcroft is a spatial analyst at the Australian
change on the distribution of forest herbs in Europe. Ecog- Museum. His research interests include the spatial and
raphy, 27, 366–380. temporal distribution of plants, invertebrates and associated
Stewart, J.R., Lister, A.M., Barnes, I. & Dalén, L. (2010) Refugia environmental factors.
revisited: individualistic responses of species in space and
time. Proceedings of the Royal Society B: Biological Sciences,
277, 661–671. Editor: Richard Pearson

Journal of Biogeography 37, 1407–1413 1413

ª Australian Museum 2010