Climate change responses: forgetting frogs, ferns and flies?

Climate change responses: forgetting frogs, ferns and flies?

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 a...

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


4 Joppa, L.N. et al. (2011) How many species of flowering plants are there? Proc. R. Soc. B 278, 554–559 5 Pimm, S.L. et al. (2010) How many endangered species remain to be discovered in Brazil? Natureza Conservac¸a˜o 8, 71–77 6 Hopkins, G.W. and Freckleton, R.P. (2006) Declines in the numbers of amateur and professional taxonomists: implications for conservation. Anim. Conserv. 5, 245–249

1 Ro¨ckel, 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, 17–19 3 Gaston, K.J. and May, R.M. (1992) Taxonomy of taxonomists. Nature 356, 281–282

0169-5347/$ – see front matter ß 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.


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we have noticed the same trend, and have presented similar comments on the topic (Sheridan, J.A. and Bickford, D, unpublished data).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. ([email protected]).

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 [7–9], 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, 285–291 553

Update 2 Gillooly, J.F. et al. (2001) Effects of size and temperature on metabolic rate. Science 293, 2248–2251 3 Atkinson, D. (1994) Temperature and organism size: a biological law for ectotherms? Adv. Ecol. Res. 25, 1–58 4 Reading, C.J. (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151, 125–131 5 Loehr, V.J.T. et al. (2007) Growing and shrinking in the smallest tortoise, Homopus signatus signatus: the importance of rain. Oecologia 153, 479–488 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, 329–340 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, 140–148

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, 464–467 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, 3845–3852 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, 1321–1334 0169-5347/$ – see front matter ß 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


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. ([email protected]).


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).