Ecophysiological forecasting: predicting adaptation and limits to adaptation

Edited by Ary A. Hoffmann and Steven L. Chown
August 2013

Ecophysiological forecasting: predicting adaptation and limits to adaptationIn 2004, Craig Venter and Daniel Cowen argued that ‘…the 21st century will be the century of biology’, defined by the new biology of genome research. From the biological perspective this appears to true – genomics and the landscape of other approaches stemming from it have fundamentally changed and continue to change the discipline. However, the century of biology seems to be defined more as a century of ‘loss’ than of ‘fundamental advance’. Despite some optimism (Ellis et al. 2013), the rates of loss of biodiversity seem higher than ever, through ongoing modification of landscapes for human needs, the extents and impacts of biological invasions, and the growing impacts of climate change (Williams et al. 2008; Butchart et al. 2010; Dawson et al. 2011; Chown et al. 2012).

In consequence, one of biology’s greatest challenges is providing options for mitigating these impacts and facilitating organismal adaptation to a rapidly changing set of global circumstances. From one perspective, this means providing further information for sound global environmental policy decisions (e.g., Griggs et al. 2013), although much of what should be done is clear and has been for decades – both growing populations and growing resource and energy demands need to be replaced by a more sustainable strategy. From another perspective, addressing this challenge means understanding how change will play out at local and regional levels, and what can be done to assist biodiversity to survive in a form that substantially decreases its rate of loss – after all this is a globally agreed target (Pereira et al. 2013).

Many approaches exist for achieving these aims, and cover a wide range of human enquiry, as is reflected in many mainstream scientific publications. In Functional Ecology, there has also been growth in both the number and scope of papers addressing environmental change questions from a functional perspective, with the realization that this perspective provides a valuable tool for predicting adaptive responses. In 2012, a virtual issue was dedicated to plant function in a rapidly changing world.

In this virtual issue on ecophysiological forecasting, composed of a suite of recent papers from the pages of Functional Ecology, four themes are highlighted that are providing new insights and tactics to help addresses this great challenge facing biology. All of them adopt what can be considered an ecophysiological perspective which, in turn, forms the basis of an innovative approach for providing more accurate taxon- and location-based forecasts of the impacts and outcomes of change. This approach is set out in the initial paper (Chown & Hoffmann 2013). The virtual issue then focuses on each of the four major themes.

The first theme concerns the interplay between environments, behaviour and change. It is addressed from the microclimate scale (Pincebourde & Woods 2012), to variation in habitat use and activity time (Huang & Pike 2011; Huang et al. 2013), and to impairment of risk assessment associated with ocean acidification (Ferrari et al. 2012). The next theme is a traits-based one. The first paper describes a novel, thermodynamic niche framework for understanding the impacts of environmental change (Kearney et al. 2013). Then, the implications of heat dissipation limit theory for the evolution of functional traits in birds, and their responses to changing environmental circumstances, is reviewed (Grémillet et al. 2012). Body size follows as a focal trait (Ohlberger 2013), with an explicit exploration of the physiological mechanisms underlying body size change and an important call to consider emergent properties at the community level. Finally, a model of the way C3 plants should respond to rising CO2 concentrations is tested using experimental data, demonstrating that responsiveness is greater in slow-growing species (Ali et al. 2013).

Demographic outcomes of change are then considered. The first work addressing this theme draws attention to contrasting effects of changing flight time availability and egg viability on butterfly demographics (Buckley & Kingsolver 2012). The next two works underscore the need to understand among-population variation in physiological traits when assessing environmental change impacts (Glanville et al. 2012; Gunderson & Leal 2012). The final study makes innovative use of species that have been introduced outside their natural range to demonstrate that flowering responses to warming are consistent among populations on two different continents (Hulme 2011).

For the final theme, the virtual issue focuses on the potential for evolutionary responses to counter the effects of environmental changes. The first treatment argues that the potential disadvantage of lower genetic variance in tropical thermal specialists can be offset by the potential advantage of a greater maximal development rate, despite the sensitivity of extinction risk estimates to generation time and genetic variance (Walters et al. 2012). It contributes to an ongoing debate about the relative risks posed by climate change to temperate and tropical species. Following that, an assessment of upper and lower thermal limits in ectotherms concludes that there may be substantial boundaries to upper thermal limits that might not be readily overcome by evolutionary change (Hoffmann et al. 2013). The study calls for greater focus on understanding the evolution of upper thermal tolerance traits, while the following work makes a similar plea for understanding local adaptation to pH conditions in the context of the impacts of ocean acidification (Kelly & Hofmann 2013). This section and the virtual issue, conclude with a comprehensive treatment of the difficulties of testing theoretical considerations of the interactions between plasticity, genetic evolution and demography in the field, and highlight a range of questions that require urgent attention (Chevin et al. 2013).

While in some senses this virtual issue raises more questions than it answers, in keeping with Loren Eiseley’s view of the nature of science itself, it highlights the rapid progress in understanding and the suite of tools that are becoming available to address the challenge of minimizing biodiversity loss during a time of rapid change.

References
Butchart S.H.M., Walpole M., Collen B., van Strien A., Scharlemann J.P.W., Almond R.E.A., Baillie J.E.M., Bomhard B., Brown C., Bruno J., Carpenter K.E., Carr G.M., Chanson J., Chenery A.M., Csirke J., Davidson N.C., Dentener F., Foster M., Galli A., Galloway J.N., Genovesi P., Gregory R.D., Hockings M., Kapos V., Lamarque J.-F., Leverington F., Loh J., McGeoch M.A., McRae L., Minasyan A., Morcillo M.H., Oldfield T.E.E., Pauly D., Quader S., Revenga C., Sauer J.R., Skolnik B., Spear D., Stanwell-Smith D., Stuart S.N., Symes A., Tierney M., Tyrrell T.D., Vié J.-C. & Watson R. (2010) Global biodiversity: indicators of recent declines. Science, 328, 1164-1168.

Chown, S.L., Huiskes, A.H.L., Gremmen, N.J.M., Lee, J.E., Terauds, A., Crosbie, K., Frenot, Y., Hughes, K.A., Imura, S., Kiefer, K., Lebouvier, M., Raymond, B., Tsujimoto, M., Ware, C., Van de Vijver, B. & Bergstrom, D.M. 2012. Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proceedings of the National Academy of Sciences of the U.S.A., 109, 4938-4943.

Dawson T.P., Jackson S.T., House J.I., Prentice I.C. & Mace G.M. (2011). Beyond predictions: biodiversity conservation in a changing climate. Science, 332, 53-58.

Ellis, E.C., Kaplan, J.O, Fuller, D.Q., Vavrus, S., Goldewijk, K.K. & Verburg, P.H. 2013. Used planet: a global history. Proceedings of the National Academy of Sciences of the U.S.A., 110, 7978-7985.

Griggs, D., Stafford-Smith, M., Gaffney, O., Rockström, J., Öhman, M.C., Shyamsundar, P., Steffan, W., Glaser, G., Kanie, N. & Noble, I. (2013) Policy: Sustainable development goals for people and planet. Nature, 495, 305-307.

Pereira, H.M., Ferrier, S., Walters, M., Geller, G.N., Jongman, R.H.C., Scholes, R.J., Bruford, M.W., Brummitt, N., Butchart, S.H.M., Cardoso, A.C., Coops, N.C., Dulloo, E., Faith, D.P., Freyhof, J., Gregory, R.D., Heip, C., Höft, R., Hurtt, G., Jetz, W., Karp, D.S., McGeoch, M.A., Obura, D., Onoda, Y., Pettorelli, N., Reyers, B., Sayre, R., Scharlemann, J.P.W., Stuart, S.N., Turak, E., Walpole, M. & Wegmann, M. 2013. Essential biodiversity variables. Science, 339, 277-278.

 Venter, J.C. & Cowen, D. (2004) The century of biology. New Perspectives Quarterly, 21, 73-77

Williams S.E., Shoo L.P., Isaac J.L., Hoffmann A.A. & Langham G. (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biology, 6, 2621-2626.

Introduction
Ecophysiological forecasting for environmental change adaptation
Steven L. Chown and Ary A HoffmannEnvironments, change and behaviour

Environments, change and behaviour
Climate uncertainty on leaf surfaces: the biophysics of leaf microclimates and their consequences for leaf-dwelling organisms (pages 844–853)
Sylvain Pincebourde and H. Arthur Woods

Future advantages in energetics, activity time, and habitats predicted in a high-altitude pit viper with climate warming (pages 446–458)
Shu-Ping Huang, Chyi-Rong Chiou, Te-En Lin, Ming-Chung Tu, Chia-Chen Lin and Warren P. Porter

Climate change impacts on fitness depend on nesting habitat in lizards (pages 1125–1136)
Wen-San Huang and David A. Pike

Effects of ocean acidification on visual risk assessment in coral reef fishes (pages 553–558)
Maud C. O. Ferrari, Mark I. McCormick, Philip L. Munday, Mark G. Meekan, Danielle L. Dixson, Oona Lönnstedt and Douglas P. Chivers

The traits-based perspective
Balancing heat, water and nutrients under environmental change: a thermodynamic niche framework
Michael R. Kearney, Stephen J. Simpson, David Raubenheimer and Sebastiaan A. L. M. Kooijman

Heat dissipation limit theory and the evolution of avian functional traits in a warming world (pages 1001–1006)
David Grémillet, Laurence Meslin and Amélie Lescroël

Climate warming and ectotherm body size – from individual physiology to community ecology
Jan Ohlberger

A trait-based ecosystem model suggests that long-term responsiveness to rising atmospheric CO2 concentration is greater in slow-growing than fast-growing plants
Ashehad A. Ali, Belinda E. Medlyn, Kristine Y. Crous and Peter B. Reich

Demographic outcomes
The demographic impacts of shifts in climate means and extremes on alpine butterflies (pages 969–977)
Lauren B. Buckley and Joel G. Kingsolver

Thermal adaptation in endotherms: climate and phylogeny interact to determine population-level responses in a wild rat
Elsa J. Glanville, Shauna A. Murray and Frank Seebacher

Geographic variation in vulnerability to climate warming in a tropical Caribbean lizard (pages 783–793)
Alex R. Gunderson and Manuel Leal

Consistent flowering response to global warming by European plants introduced into North America
Philip E. Hulme

Evolutionary outlooks
Forecasting extinction risk of ectotherms under climate warming: an evolutionary perspective (pages 1324–1338)
Richard J. Walters, Wolf U. Blanckenhorn and David Berger

Upper thermal limits in terrestrial ectotherms: how constrained are they?
Ary A. Hoffmann, Steven L. Chown and Susana Clusella-Trullas

Adaptation and the physiology of ocean acidification
Morgan W. Kelly and Gretchen E. Hofmann

Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field
Luis-Miguel Chevin, Sinéad Collins and François Lefèvre

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