Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?

Thermal performance curves (TPCs), which quantify how an ectotherm's body temperature (Tb ) affects its performance or fitness, are often used in an attempt to predict organismal responses to climate change. Here, we examine the key - but often biologically unreasonable - assumptions underlying this approach; for example, that physiology and thermal regimes are invariant over ontogeny, space and time, and also that TPCs are independent of previously experienced Tb. We show how a critical consideration of these assumptions can lead to biologically useful hypotheses and experimental designs. For example, rather than assuming that TPCs are fixed during ontogeny, one can measure TPCs for each major life stage and incorporate these into stage-specific ecological models to reveal the life stage most likely to be vulnerable to climate change. Our overall goal is to explicitly examine the assumptions underlying the integration of TPCs with Tb , to develop a framework within which empiricists can place their work within these limitations, and to facilitate the application of thermal physiology to understanding the biological implications of climate change.

[1]  Mauro Santos,et al.  Tolerance landscapes in thermal ecology , 2014 .

[2]  Brett R. Scheffers,et al.  Assessing species' vulnerability to climate change , 2015 .

[3]  B. Sinclair,et al.  Variation in Thermal Performance among Insect Populations* , 2012, Physiological and Biochemical Zoology.

[4]  B. Helmuth,et al.  Spatial variability in habitat temperature may drive patterns of selection between an invasive and native mussel species. , 2007 .

[5]  K. A. S. Mislan,et al.  Organismal climatology: analyzing environmental variability at scales relevant to physiological stress , 2010, Journal of Experimental Biology.

[6]  Michael J Angilletta,et al.  The world is not flat: defining relevant thermal landscapes in the context of climate change. , 2011, Integrative and comparative biology.

[7]  J. Rosenheim,et al.  PREDATORS REDUCE PREY POPULATION GROWTH BY INDUCING CHANGES IN PREY BEHAVIOR , 2004 .

[8]  J. R. Brett Energetic Responses of Salmon to Temperature. A Study of Some Thermal Relations in the Physiology and Freshwater Ecology of Sockeye Salmon (Oncorhynchus nerkd) , 1971 .

[9]  C. Harley,et al.  On the prediction of extreme ecological events , 2009 .

[10]  H. U. Riisgård On measurement of filtration rates in bivalves — the stony road to reliable data: review and interpretation , 2001 .

[11]  Ray Berkelmans,et al.  The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change , 2006, Proceedings of the Royal Society B: Biological Sciences.

[12]  D. Janzen Why Mountain Passes are Higher in the Tropics , 1967, The American Naturalist.

[13]  R. Huey,et al.  Global metabolic impacts of recent climate warming , 2010, Nature.

[14]  H. Pörtner,et al.  Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems , 2010, Journal of Experimental Biology.

[15]  W. Dowd,et al.  Thermal variation, thermal extremes and the physiological performance of individuals , 2015, The Journal of Experimental Biology.

[16]  P. Camus,et al.  Thermoregulatory behavior, heat gain and thermal tolerance in the periwinkle Echinolittorina peruviana in central Chile. , 2005, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[17]  A. Köhler,et al.  Staying warm or moist? Operative temperature and thermal preferences of common frogs (Rana temporaria), and effects on locomotion , 2011 .

[18]  Jonathon H Stillman,et al.  Acclimation Capacity Underlies Susceptibility to Climate Change , 2003, Science.

[19]  A. Hoffmann,et al.  Climate change and evolutionary adaptation , 2011, Nature.

[20]  H. Verhoef,et al.  Modelling the time-temperature relationship in cold injury and effect of high temperature interruptions on survival in a chill-sensitive collembolan. , 1998 .

[21]  L. Peck,et al.  Poor acclimation capacities in Antarctic marine ectotherms , 2010 .

[22]  D. Wall,et al.  The future of soil invertebrate communities in polar regions: different climate change responses in the Arctic and Antarctic? , 2013, Ecology letters.

[23]  D. Wethey,et al.  Loss of thermal refugia near equatorial range limits , 2016, Global change biology.

[24]  Alistair Rogers,et al.  The use and misuse of Vc,max in Earth System Models , 2014, Photosynthesis Research.

[25]  S. Chown,et al.  Testing the Beneficial Acclimation Hypothesis and Its Alternatives for Locomotor Performance , 2006, The American Naturalist.

[26]  G. S. Bakken Measurement and Application of Operative and Standard Operative Temperatures in Ecology , 1992 .

[27]  B. Sinclair,et al.  High temperature tolerance and thermal plasticity in emerald ash borer Agrilus planipennis , 2011 .

[28]  A. Hoffmann,et al.  Thermal Tolerance in Widespread and Tropical Drosophila Species: Does Phenotypic Plasticity Increase with Latitude? , 2011, The American Naturalist.

[29]  N. Moran,et al.  Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts , 2007, PLoS biology.

[30]  W. Porter,et al.  Toxicant-disease-environment interactions associated with suppression of immune system, growth, and reproduction. , 1984, Science.

[31]  D. Wethey,et al.  Shore-level size gradients and thermal refuge use in the predatory sea star Pisaster ochraceus: the role of environmental stressors , 2015 .

[32]  M. Tagliarolo,et al.  Sub-lethal and sub-specific temperature effects are better predictors of mussel distribution than thermal tolerance , 2015 .

[33]  Curtis Deutsch,et al.  Climate change tightens a metabolic constraint on marine habitats , 2015, Science.

[34]  R. Huey,et al.  Cost and Benefits of Lizard Thermoregulation , 1976, The Quarterly Review of Biology.

[35]  Glenn J Tattersall,et al.  Heat Exchange from the Toucan Bill Reveals a Controllable Vascular Thermal Radiator , 2009, Science.

[36]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[37]  J. Kingsolver,et al.  Beyond Thermal Performance Curves: Modeling Time-Dependent Effects of Thermal Stress on Ectotherm Growth Rates , 2016, The American Naturalist.

[38]  M. Švob [Male sterility]. , 1970, Medicinski arhiv.

[39]  D. Miles The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards , 2004 .

[40]  B. Heinrich,et al.  A Field Study of Flight Temperatures in Moths in Relation to Body Weight and Wing Loading , 1973 .

[41]  C. Harley,et al.  Beyond long-term averages: making biological sense of a rapidly changing world , 2014, Climate Change Responses.

[42]  M. Feder,et al.  Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. , 1999, Annual review of physiology.

[43]  Robert D. Stevenson,et al.  Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches , 1979 .

[44]  S. Maloney,et al.  Activity, blood temperature and brain temperature of free-ranging springbok , 1997, Journal of Comparative Physiology B.

[45]  M. McFall-Ngai Giving microbes their due – animal life in a microbially dominant world , 2015, The Journal of Experimental Biology.

[46]  F. Vernberg,et al.  INFLUENCE OF PARASITISM ON THERMAL RESISTANCE OF THE MUD-FLAT SNAIL, NASSARIUS OBSOLETA SAY. , 1963, Experimental parasitology.

[47]  R. Huey,et al.  Temperature, Demography, and Ectotherm Fitness , 2001, The American Naturalist.

[48]  D. Heinrichs,et al.  Paradoxical acclimation responses in the thermal performance of insect immunity , 2016, Oecologia.

[49]  M. Angilletta Thermal Adaptation: A Theoretical and Empirical Synthesis , 2009 .

[50]  J. Stillman,et al.  Multiple Stressors in a Changing World: The Need for an Improved Perspective on Physiological Responses to the Dynamic Marine Environment. , 2016, Annual review of marine science.

[51]  V. Savage,et al.  Increased temperature variation poses a greater risk to species than climate warming , 2014, Proceedings of the Royal Society B: Biological Sciences.

[52]  R. Calsbeek,et al.  Natural selection on thermal performance in a novel thermal environment , 2014, Proceedings of the National Academy of Sciences.

[53]  J. Kingsolver,et al.  Heat stress and the fitness consequences of climate change for terrestrial ectotherms , 2013 .

[54]  B. Lemos,et al.  Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climatic adaptations , 2005, Journal of evolutionary biology.

[55]  B. Helmuth,et al.  Tipping points, thresholds and the keystone role of physiology in marine climate change research. , 2011, Advances in marine biology.

[56]  Jonathon H Stillman,et al.  Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. , 2013, Integrative and comparative biology.

[57]  G. Chelazzi,et al.  Cardiac and behavioural responses of mussels to risk of predation by dogwhelks , 1999, Animal Behaviour.

[58]  J. F. Staples,et al.  Reestablishment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus , 2012, Proceedings of the National Academy of Sciences.

[59]  R. Huey,et al.  Physiological Consequences of Habitat Selection , 1991, The American Naturalist.

[60]  D. Wethey,et al.  Climate change, species distribution models, and physiological performance metrics: predicting when biogeographic models are likely to fail , 2013, Ecology and evolution.

[61]  W. Pitt Effects of multiple vertebrate predators on grasshopper habitat selection: trade-offs due to predation risk, foraging, and thermoregulation , 1999, Evolutionary Ecology.

[62]  D. Renault,et al.  Insects in fluctuating thermal environments. , 2015, Annual review of entomology.

[63]  Michael Kearney,et al.  The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming , 2009, Proceedings of the National Academy of Sciences.

[64]  J. Pandolfi,et al.  Predicting evolutionary responses to climate change in the sea. , 2013, Ecology letters.

[65]  Jason D. K. Dzurisin,et al.  Thermal Variability Increases the Impact of Autumnal Warming and Drives Metabolic Depression in an Overwintering Butterfly , 2012, PloS one.

[66]  B. Sinclair,et al.  Static and dynamic approaches yield similar estimates of the thermal sensitivity of insect metabolism. , 2013, Journal of insect physiology.

[67]  J. Terblanche,et al.  Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence , 2016, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[68]  J. Bale,et al.  Cross-generation plasticity in cold hardiness is associated with diapause, but not the non-diapause developmental pathway, in the blow fly Calliphora vicina , 2014, Journal of Experimental Biology.

[69]  M. Kearney,et al.  Mechanistic models for predicting insect responses to climate change. , 2016, Current opinion in insect science.

[70]  C. Harley,et al.  Climate Change and Latitudinal Patterns of Intertidal Thermal Stress , 2002, Science.

[71]  Paul R. Martin,et al.  Impacts of climate warming on terrestrial ectotherms across latitude , 2008, Proceedings of the National Academy of Sciences.

[72]  L. Bacigalupe,et al.  Geographic variation in thermal physiological performance of the intertidal crab Petrolisthes violaceus along a latitudinal gradient , 2014, Journal of Experimental Biology.

[73]  M. Mangel,et al.  Cold snaps, heatwaves, and arthropod growth , 2016 .

[74]  A. Ward,et al.  Thermal acclimation of interactions: differential responses to temperature change alter predator–prey relationship , 2012, Proceedings of the Royal Society B: Biological Sciences.

[75]  Andrew C. Thomas,et al.  Fisheries Management in a Changing Climate Lessons from the 2012 Ocean Heat Wave in the Northwest Atlantic , 2013 .

[76]  M. Friberg,et al.  Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies , 2011, Proceedings of the Royal Society B: Biological Sciences.

[77]  R. Huey,et al.  How Extreme Temperatures Impact Organisms and the Evolution of their Thermal Tolerance. , 2016, Integrative and comparative biology.

[78]  R. Stevenson,et al.  The Thermal Dependence of Locomotion, Tongue Flicking, Digestion, and Oxygen Consumption in the Wandering Garter Snake , 1985, Physiological Zoology.

[79]  M. H. Smith,et al.  Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature–size rule , 2007, Journal of evolutionary biology.

[80]  A. Clarke,et al.  What Is Cold Adaptation and How Should We Measure It , 1991 .

[81]  M. Bertness,et al.  Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[82]  A. Lago‐Lestón,et al.  Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations , 2009 .

[83]  M. Kearney,et al.  Biomechanics meets the ecological niche: the importance of temporal data resolution , 2012, Journal of Experimental Biology.

[84]  J. R. Brett,et al.  GROWTH RATE AND BODY COMPOSITION OF FINGERLING SOCHEYE SALMON ONCORHYNCHUS MESHA IN RELATION TO TEMPERATURE AND RATION SIZE , 1969 .

[85]  R. Huey,et al.  Why “Suboptimal” Is Optimal: Jensen’s Inequality and Ectotherm Thermal Preferences , 2008, The American Naturalist.

[86]  M. Menaker,et al.  Thermochron iButtons: An Inexpensive Method for Long-Term Recording of Core Body Temperature in Untethered Animals , 2003, Journal of biological rhythms.

[87]  Brian Helmuth,et al.  Thermal tolerance and climate warming sensitivity in tropical snails , 2015, Ecology and evolution.

[88]  S. Simpson,et al.  Insect herbivores can choose microclimates to achieve nutritional homeostasis , 2013, Journal of Experimental Biology.

[89]  Chown,et al.  Critical thermal limits, temperature tolerance and water balance of a sub-Antarctic kelp fly, Paractora dreuxi (Diptera: Helcomyzidae). , 2001, Journal of insect physiology.

[90]  Robert K. Colwell,et al.  Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation , 2014, Proceedings of the National Academy of Sciences.

[91]  M. Ayres,et al.  Jensen's inequality predicts effects of environmental variation. , 1999, Trends in ecology & evolution.

[92]  Peter J. Edwards,et al.  How comparable are species distributions along elevational and latitudinal climate gradients , 2013 .

[93]  Andrew M. Fischer,et al.  Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida , 2006 .

[94]  G. Somero,et al.  The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’ , 2010, Journal of Experimental Biology.

[95]  S. Pincebourde,et al.  Microclimatic challenges in global change biology , 2013, Global change biology.

[96]  Timothy H Keitt,et al.  Resolving the life cycle alters expected impacts of climate change , 2015, Proceedings of the Royal Society B: Biological Sciences.

[97]  J. Kingsolver,et al.  Complex life cycles and the responses of insects to climate change. , 2011, Integrative and comparative biology.

[98]  V. Savage,et al.  Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. , 2014, The Journal of animal ecology.

[99]  S. Collins,et al.  Growth responses of a green alga to multiple environmental drivers , 2015 .

[100]  Natalie J Briscoe,et al.  Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals , 2014, Biology Letters.

[101]  B. Sinclair,et al.  The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect , 2015 .