Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits.

The impact of warming on the persistence and distribution of ectotherms is often forecasted from their warming tolerance, inferred as the difference between their upper thermal limit and macroclimate temperature. Ectotherms, however, are thermally adapted to their microclimates, which can deviate substantially from macroscale conditions. Ignoring microclimates can therefore bias estimates of warming tolerance. We compared warming tolerance of an insect across its ontogeny when calculated from macro- and microclimate temperatures. We used a heat balance model to predict experienced microclimate temperatures from macroclimate, and we measured thermal limits for several life stages. The model shows a concomitant increase in microclimate temperatures and thermal limits across insect ontogeny, despite the fact that they all share the same macroclimate. Consequently, warming tolerance; as estimated from microclimate temperature, remained constant across ontogeny. When calculated from macroclimate temperature, however, warming tolerance was overestimated by 7-10 degrees C, depending on the life stage. Therefore, errors are expected when predicting persistence and distribution shifts of ectotherms in changing climates using macroclimate rather than microclimate.

[1]  Jérôme Casas,et al.  Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods , 2014 .

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

[3]  E. Desouhant,et al.  The impact of thermal fluctuations on reaction norms in specialist and generalist parasitic wasps , 2014 .

[4]  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.

[5]  Ary A. Hoffmann,et al.  Microclimate modelling at macro scales: a test of a general microclimate model integrated with gridded continental‐scale soil and weather data , 2014 .

[6]  M. Lima,et al.  The role of temperature variability on insect performance and population dynamics in a warming world , 2014 .

[7]  Brett R. Scheffers,et al.  Microhabitats reduce animal's exposure to climate extremes , 2014, Global change biology.

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

[9]  M. Kearney,et al.  Activity restriction and the mechanistic basis for extinctions under climate warming. , 2013, Ecology letters.

[10]  H. Woods,et al.  Ontogenetic changes in the body temperature of an insect herbivore , 2013 .

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

[12]  Brett R. Scheffers,et al.  Thermal Buffering of Microhabitats is a Critical Factor Mediating Warming Vulnerability of Frogs in the Philippine Biodiversity Hotspot , 2013 .

[13]  P. Marquet,et al.  Heat freezes niche evolution. , 2013, Ecology letters.

[14]  S. Chown,et al.  Upper thermal limits in terrestrial ectotherms: how constrained are they? , 2013 .

[15]  K. Paaijmans,et al.  Temperature variation makes ectotherms more sensitive to climate change , 2013, Global change biology.

[16]  John-Arvid Grytnes,et al.  Local temperatures inferred from plant communities suggest strong spatial buffering of climate warming across Northern Europe , 2013, Global change biology.

[17]  D. Biron,et al.  On the canopy structure manipulation to buffer climate change effects on insect herbivore development , 2013, Trees.

[18]  Paul Sunnucks,et al.  Stage‐dependent physiological responses in a butterfly cause non‐additive effects on phenology , 2012 .

[19]  Nicholas K. Dulvy,et al.  Thermal tolerance and the global redistribution of animals , 2012 .

[20]  S. Pincebourde,et al.  Climate uncertainty on leaf surfaces: the biophysics of leaf microclimates and their consequences for leaf‐dwelling organisms , 2012 .

[21]  Jérôme Casas,et al.  Temporal coincidence of environmental stress events modulates predation rates. , 2012, Ecology letters.

[22]  R. Huey,et al.  Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  P. L. Ribeiro,et al.  Considerations for Assessing Maximum Critical Temperatures in Small Ectothermic Animals: Insights from Leaf-Cutting Ants , 2012, PloS one.

[24]  Mauro Santos,et al.  Comment on ‘Ecologically relevant measures of tolerance to potentially lethal temperatures’ , 2012, Journal of Experimental Biology.

[25]  S. Diamond,et al.  Who likes it hot? A global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants , 2012 .

[26]  H. Woods,et al.  No evidence for the evolution of thermal or desiccation tolerance of eggs among populations of Manduca sexta , 2012 .

[27]  Mauro Santos,et al.  Making sense of heat tolerance estimates in ectotherms: lessons from Drosophila , 2011 .

[28]  S. Chown,et al.  Ecologically relevant measures of tolerance to potentially lethal temperatures , 2011, Journal of Experimental Biology.

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

[30]  F. Bozinovic,et al.  An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[31]  N. Dulvy,et al.  Global analysis of thermal tolerance and latitude in ectotherms , 2011, Proceedings of the Royal Society B: Biological Sciences.

[32]  G. Davidowitz,et al.  Cross‐stage consequences of egg temperature in the insect Manduca sexta , 2011 .

[33]  Mauro Santos,et al.  Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications , 2011 .

[34]  Michael Kearney,et al.  Modelling the ecological niche from functional traits , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[35]  Paul Sunnucks,et al.  Early emergence in a butterfly causally linked to anthropogenic warming , 2010, Biology Letters.

[36]  Elizabeth E Crone,et al.  Causes and consequences of variation in plant population growth rate: a synthesis of matrix population models in a phylogenetic context. , 2010, Ecology letters.

[37]  J. Terblanche,et al.  Within‐generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short‐term responses to temperature , 2010 .

[38]  M. Angilletta,et al.  Can mechanism inform species' distribution models? , 2010, Ecology letters.

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

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

[41]  M. Kearney,et al.  Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. , 2009, Ecology letters.

[42]  J. Kingsolver,et al.  EVOLUTION IN A CONSTANT ENVIRONMENT: THERMAL FLUCTUATIONS AND THERMAL SENSITIVITY OF LABORATORY AND FIELD POPULATIONS OF MANDUCA SEXTA , 2009, Evolution; international journal of organic evolution.

[43]  H. Sinoquet,et al.  Experimental study of fruit temperature dynamics within apple tree crowns , 2009 .

[44]  Gary Langham,et al.  Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change , 2008, PLoS biology.

[45]  J. Terblanche,et al.  Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? , 2008, Biological reviews of the Cambridge Philosophical Society.

[46]  S. Pincebourde,et al.  Body temperature during low tide alters the feeding performance of a top intertidal predator , 2008 .

[47]  R. Huey,et al.  Putting the Heat on Tropical Animals , 2008, Science.

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

[49]  W. Porter,et al.  Model of Japanese serow (Capricornis crispus) energetics predicts distribution on Honshu, Japan. , 2007, Ecological applications : a publication of the Ecological Society of America.

[50]  Jérôme Casas,et al.  Regional climate modulates the canopy mosaic of favourable and risky microclimates for insects. , 2007, The Journal of animal ecology.

[51]  Jérôme Casas,et al.  Herbivory mitigation through increased water-use efficiency in a leaf-mining moth-apple tree relationship. , 2006, Plant, cell & environment.

[52]  B. Menge,et al.  MOSAIC PATTERNS OF THERMAL STRESS IN THE ROCKY INTERTIDAL ZONE: IMPLICATIONS FOR CLIMATE CHANGE , 2006 .

[53]  S. Pincebourde,et al.  MULTITROPHIC BIOPHYSICAL BUDGETS: THERMAL ECOLOGY OF AN INTIMATE HERBIVORE INSECT–PLANT INTERACTION , 2006 .

[54]  Jérôme Casas,et al.  Leaf miner-induced changes in leaf transmittance cause variations in insect respiration rates. , 2006, Journal of insect physiology.

[55]  Jérôme Casas,et al.  Geometrical Games between a Host and a Parasitoid , 2000, The American Naturalist.

[56]  Kevin J. Gaston,et al.  Thermal tolerance, climatic variability and latitude , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  G. Somero,et al.  A Comparative Analysis of the Upper Thermal Tolerance Limits of Eastern Pacific Porcelain Crabs, Genus Petrolisthes: Influences of Latitude, Vertical Zonation, Acclimation, and Phylogeny , 2000, Physiological and Biochemical Zoology.

[58]  M. Feder,et al.  Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster , 1999, Oecologia.

[59]  B. Helmuth INTERTIDAL MUSSEL MICROCLIMATES: PREDICTING THE BODY TEMPERATURE OF A SESSILE INVERTEBRATE , 1998 .

[60]  R. Huey,et al.  WITHIN‐ AND BETWEEN‐GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER , 1996, Evolution; international journal of organic evolution.

[61]  Joel G. Kingsolver,et al.  Evolution of Resistance to High Temperature in Ectotherms , 1993, The American Naturalist.

[62]  D. Hodáňová An introduction to environmental biophysics , 1979, Biologia Plantarum.

[63]  T. Casey ACTIVITY PATTERNS, BODY TEMPERATURE AND THERMAL ECOLOGY IN TWO DESERT CATERPILLARS (LEPIDOPTERA: SPHINGIDAE)" , 1976 .

[64]  P. Jarvis The Interpretation of the Variations in Leaf Water Potential and Stomatal Conductance Found in Canopies in the Field , 1976 .

[65]  B. Huntley,et al.  Habitat microclimates drive fine‐scale variation in extreme temperatures , 2011 .

[66]  M. Lima,et al.  Beyond average: an experimental test of temperature variability on the population dynamics of Tribolium confusum , 2010, Population Ecology.

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