Update

Trends in Ecology and Evolution November 2011, Vol. 26, No. 11

References

4 Joppa, L.N. et al. (2011) How many species of flowering plants are there?
Proc. R. Soc. B 278, 554559
5 Pimm, S.L. et al. (2010) How many endangered species remain to be
discovered in Brazil? Natureza Conservacao 8, 7177
6 Hopkins, G.W. and Freckleton, R.P. (2006) Declines in the numbers of
amateur and professional taxonomists: implications for conservation.
Anim. Conserv. 5, 245249

1 Rockel, D. et al. (1995) In Manual of the Living Conidae (Vol. 1),

Springer-Verlag
2 Godfray, H.C.J. (2002) Challenges for taxonomy. Nature 417, 1719
3 Gaston, K.J. and May, R.M. (1992) Taxonomy of taxonomists. Nature
356, 281282

0169-5347/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tree.2011.07.010 Trends in Ecology and Evolution, November 2011,
Vol. 26, No. 11

Appendix A. Supplementary data

Supplementary data associated with this article can be
found, in the online version, at doi:10.1016/j.tree.
2011.07.010.

Letters

Climate change responses: forgetting frogs, ferns

and flies?
David P. Bickford, Jennifer A. Sheridan and Sam D. Howard
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore

We were pleased to see Gardner et al.s recent paper in

TREE on a third universal response to climate warming [1].
Indeed, we have noticed the same trend, and have presented
similar comments on the topic (Sheridan, J.A. and Bickford,
D, unpublished data). We agree with Gardner et al. [1] that
there is strong evidence of a third pervasive response to
climate change; size reduction has been found in too many
organisms experiencing climate change to be a simple coincidence. Gardner et al. present an excellent suite of potential
studies that can examine this trend and help identify proximate causes of the observed declines. However, we suggest
that although birds provide an excellent endothermic study
system, ectotherms offer a richer group from which to draw
conclusions and offer research hypotheses aimed at understanding the mechanisms behind shrinking organisms. We
feel that studies of size declines in ectotherms should receive
equal attention for several reasons.
First, ectotherms represent the vast majority of both
species diversity and biomass across ecosystems and they
are integral parts of trophic networks in all ecosystems.
How they respond to warming, both on ecological and
evolutionary scales, will have widespread and important
impacts. If they are being affected in large-scale ways by
the same or similar mechanisms, one might be able to
predict and mitigate against those effects.
Second, there are two explicit thermodynamic and metabolic rules of ecology that are well known in ectotherms:
the temperature metabolic rate rule [2] and the temperature-size rule [3]. The former states that ectotherms burn
more metabolic energy when it is warmer and need more
energy to achieve and maintain adult body size at higher
temperatures [2]. Large-scale implications of this are that
ectothermic organisms will have to consume more metabolic energy to maintain their body size as temperatures
increase. It is unlikely that increased consumption is
sustainable, so it is reasonable to expect that ectotherms
Corresponding author: Bickford, D.P. (rokrok@nus.edu.sg).

will decrease in size with continued climate warming, as

has been shown for toads [4] and tortoises [5]. The temperature-size rule relates larval development and temperature; animals mature earlier and at smaller sizes when
they experience warmer temperatures [3,6]. Continued
increases in global temperatures are likely to result in
faster development times and smaller sizes of ectotherms.
This theoretical framework provides ample experimental
and model-based approaches to test hypotheses about the
ultimate mechanisms of body size reductions.
Third, although body size changes in endotherms are
real and have been observed in many taxa [79], many of
the endothermic size reductions are secondary effects of
climate change (altered diet or nutrition, to cite the main
example from [1]). Size declines of ectothermic animals and
plants, by contrast, are more likely to be direct results of
changes in temperature and precipitation associated with
climate change. Precipitation is predicted to become increasingly variable across the globe, and to decrease in
some areas [10]. This reduction in predictable rainfall is
likely to reduce plant size, as has been shown for North
American species [11], and is also likely to affect food
availability for both faunal and human populations.
Studies on the mechanisms directly affecting size changes
in ectotherms and primary producers might, therefore,
have broader impact than studies on secondary changes
in endotherms.
As noted by Gardner et al., there is much work yet to be
done on understanding the mechanisms of this trend, how
it plays out across the tree of life, and what it will mean for
ecosystem functioning and human livelihood. A broad
perspective and theoretical framework are necessary to
understand fully observed trends in organism size change,
and to develop effective mitigation strategies.
References
1 Gardner, J.L. et al. (2011) Declining body size: a third universal
response to warming? Trends Ecol. Evol. 26, 285291
553

Update
2 Gillooly, J.F. et al. (2001) Effects of size and temperature on metabolic
rate. Science 293, 22482251
3 Atkinson, D. (1994) Temperature and organism size: a biological law for
ectotherms? Adv. Ecol. Res. 25, 158
4 Reading, C.J. (2007) Linking global warming to amphibian declines
through its effects on female body condition and survivorship.
Oecologia 151, 125131
5 Loehr, V.J.T. et al. (2007) Growing and shrinking in the smallest
tortoise, Homopus signatus signatus: the importance of rain.
Oecologia 153, 479488
6 van der Have, T.M. and de Jong, G. (1996) Adult size in ectotherms:
temperature effects on growth and differentiation. J. Theor. Biol. 183,
329340
7 Smith, F.A. et al. (1998) The influence of climate change on the body
mass of woodrats Neotoma in an arid region of New Mexico, USA.
Ecography 21, 140148

Trends in Ecology and Evolution November 2011, Vol. 26, No. 11

8 Ozgul, A. et al. (2009) The dynamics of phenotypic change and the
shrinking sheep of St Kilda. Science 325, 464467
9 Gardner, J.L. et al. (2009) Shifting latitudinal clines in avian body size
correlate with global warming in Australian passerines. Proc. R. Soc.
Lond. B 276, 38453852
10 IPCC (2007) Climate Change 2007: The Physical Science Basis.
Contribution of Working Group I to the Fourth Assessment Report of
the Intergovernmental Panel on Climate Change, Cambridge
University Press
11 Franks, S.J. and Weis, A.E. (2008) A change in climate causes rapid
evolution of multiple life-history traits and their interactions in an
annual plant. J. Evol. Biol. 21, 13211334
0169-5347/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tree.2011.06.016 Trends in Ecology and Evolution, November 2011,
Vol. 26, No. 11

Letters

Climate change, body size, and phenotype

dependent dispersal
Shannon J. McCauley1 and Karen E. Mabry2
1
2

Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA 93407-0401, USA
Department of Biology, MSC 3AF, New Mexico State University, Las Cruces, NM 88003-8001, USA

Gardner and colleagues [1] recently reviewed the evidence

for shifts in body size as a third major response to climate
change, in addition to widely recognized shifts in the
ranges and phenology of species [2]. The authors conclude
that, although a pattern of declining body size is commonly
observed (i.e. [3]), increases in body size might also occur
and more detailed studies are needed [1]. Although their
review focuses on the evidence for declining body size as a
third general response to climate change, we would like to
add that the effect of climate on individual body size has
the potential to impact one of the other major responses
to climate change dramatically: species range shifts
(Figure 1).
Although rarely made explicit, much of the literature
makes the implicit assumption that dispersal will facilitate species range shifts into areas with newly suitable
climatic conditions [2,4,5]. However, there is accumulating evidence indicating that dispersal behavior is often
phenotype dependent and that body size is a major factor
shaping the propensity and ability of individuals to disperse [4,6,7]. Body size is also likely to play an important
role in establishment once those individuals that move
beyond the prior range borders arrive in new habitats.
Incorporating the interactive effects of body size and
dispersal will allow a more thorough understanding of
the effects of climate change on range shifts, and will
improve the ability to predict the effects of climate change
on biota.
Although under some conditions the influence of
climate change on body size might facilitate species range
shifts, the emerging consensus that warmer climates will
Corresponding author: McCauley, S.J. (smccaule@calpoly.edu).

554

result in generally smaller body sizes [1,3] suggests that

this effect will often be inhibitory for many species. In
either case, effects of climate on body size and dispersal
should be incorporated into analyses assessing range
shifts and into planning associated with maintaining
the capacity of populations to make such range shifts.
To date, there are relatively few examples of direct connections between climate change and dispersal behavior,
and observed patterns have been mixed (i.e. [8,9] and
references therein). Further studies incorporating explicit linkages between climate, body size and dispersal
might provide insight into examples in which species
either have not shifted their ranges in response to climate
change or have shown unexpected shifts (e.g. examples
in [10]).
Long-distance dispersers (the tail of the dispersal
kernel) are critical in driving range shifts that are rapid

Climate change

Phenology
Range shifts

Body size

Phenotype dependent
dispersal
TRENDS in Ecology & Evolution

Figure 1. Schematic representation of the direct effects of climate change (solid

arrows) and a potential indirect effect of body size on species range shifts,
mediated through phenotype-dependent dispersal (broken arrow).