Thermal tolerance and climate warming sensitivity in tropical snails

Abstract Tropical ectotherms are predicted to be especially vulnerable to climate change because their thermal tolerance limits generally lie close to current maximum air temperatures. This prediction derives primarily from studies on insects and lizards and remains untested for other taxa with contrasting ecologies. We studied the HCT (heat coma temperatures) and ULT (upper lethal temperatures) of 40 species of tropical eulittoral snails (Littorinidae and Neritidae) inhabiting exposed rocky shores and shaded mangrove forests in Oceania, Africa, Asia and North America. We also estimated extremes in animal body temperature at each site using a simple heat budget model and historical (20 years) air temperature and solar radiation data. Phylogenetic analyses suggest that HCT and ULT exhibit limited adaptive variation across habitats (mangroves vs. rocky shores) or geographic locations despite their contrasting thermal regimes. Instead, the elevated heat tolerance of these species (HCT = 44.5 ± 1.8°C and ULT = 52.1 ± 2.2°C) seems to reflect the extreme temperature variability of intertidal systems. Sensitivity to climate warming, which was quantified as the difference between HCT or ULT and maximum body temperature, differed greatly between snails from sunny (rocky shore; Thermal Safety Margin, TSM = −14.8 ± 3.3°C and −6.2 ± 4.4°C for HCT and ULT, respectively) and shaded (mangrove) habitats (TSM = 5.1 ± 3.6°C and 12.5 ± 3.6°C). Negative TSMs in rocky shore animals suggest that mortality is likely ameliorated during extreme climatic events by behavioral thermoregulation. Given the low variability in heat tolerance across species, habitat and geographic location account for most of the variation in TSM and may adequately predict the vulnerability to climate change. These findings caution against generalizations on the impact of global warming across ectothermic taxa and highlight how the consideration of nonmodel animals, ecological transitions, and behavioral responses may alter predictions of studies that ignore these biological details.

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

[2]  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.

[3]  F J Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[4]  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.

[5]  T. J. Webb,et al.  Marine and terrestrial ecology: unifying concepts, revealing differences. , 2012, Trends in ecology & evolution.

[6]  Theodore Garland,et al.  Why tropical forest lizards are vulnerable to climate warming , 2009, Proceedings of the Royal Society B: Biological Sciences.

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

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

[9]  G. Barker,et al.  Behavioural ecology: on doing the right thing, in the right place at the right time. , 2001 .

[10]  H. Pörtner,et al.  Can respiratory physiology predict thermal niches? , 2016, Annals of the New York Academy of Sciences.

[11]  K. A. S. Mislan,et al.  Predicting intertidal organism temperatures with modified land surface models , 2011 .

[12]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[13]  K. Mach,et al.  Spreading the risk: Small-scale body temperature variation among intertidal organisms and its implications for species persistence , 2011 .

[14]  D. Reid,et al.  Global diversification of mangrove fauna: a molecular phylogeny of Littoraria (Gastropoda: Littorinidae). , 2010, Molecular phylogenetics and evolution.

[15]  K. A. S. Mislan,et al.  When to worry about the weather: role of tidal cycle in determining patterns of risk in intertidal ecosystems , 2009 .

[16]  Per Capita,et al.  About the authors , 1995, Machine Vision and Applications.

[17]  L. Seuront,et al.  Behavioral thermoregulation in a tropical gastropod: links to climate change scenarios , 2011 .

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

[19]  H. A. Rutjes,et al.  LAND SNAIL DIVERSITY IN A SQUARE KILOMETRE OF TROPICAL RAINFORST INSABAH, MALAYSIAN BORNEO , 2001 .

[20]  R. Nespolo,et al.  Natural Selection Reduces Energy Metabolism in the Garden Snail, Helix aspersa (Cornu aspersum) , 2009, Evolution; international journal of organic evolution.

[21]  R. B. Cowles,et al.  A preliminary study of the thermal requirements of desert reptiles. Bulletin of the AMNH ; v. 83, article 5 , 1944 .

[22]  D. Wethey,et al.  Three decades of high-resolution coastal sea surface temperatures reveal more than warming , 2012, Nature Communications.

[23]  Sean C. Anderson,et al.  Paleontological baselines for evaluating extinction risk in the modern oceans , 2015, Science.

[24]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[25]  D. Wethey,et al.  Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Michael J Angilletta,et al.  The Mean and Variance of Environmental Temperature Interact to Determine Physiological Tolerance and Fitness , 2011, Physiological and Biochemical Zoology.

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

[28]  B. Helmuth,et al.  Microhabitats, Thermal Heterogeneity, and Patterns of Physiological Stress in the Rocky Intertidal Zone , 2001, The Biological Bulletin.

[29]  W. Ponder,et al.  Phylogeny of the gastropod superfamily Cerithioidea using morphology and molecules , 2011 .

[30]  S. Balayan,et al.  Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. , 2011, Molecular phylogenetics and evolution.

[31]  B. Helmuth,et al.  Hidden signals of climate change in intertidal ecosystems: What (not) to expect when you are expecting , 2011 .

[32]  Carlo Cerrano,et al.  Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave , 2008 .

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

[34]  M. Schilthuizen,et al.  MICROSNAILS AT MICROSCALES IN BORNEO: DISTRIBUTIONS OF PROSOBRANCHIA VERSUS PULMONATA , 2002 .

[35]  Alejandro Gonzalez-Voyer,et al.  Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities , 2012 .

[36]  Liam J. Revell,et al.  Phylogenetic signal and linear regression on species data , 2010 .

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

[38]  D. Morritt,et al.  Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata , 1995 .

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

[40]  C. McQuaid,et al.  Behaviour moderates climate warming vulnerability in high-rocky-shore snails: interactions of habitat use, energy consumption and environmental temperature , 2013 .

[41]  C. McQuaid,et al.  Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology , 2011, Proceedings of the Royal Society B: Biological Sciences.

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

[43]  G. Barker The Biology of Terrestrial Molluscs , 2001 .

[44]  Anthony R. Ives,et al.  Using the Past to Predict the Present: Confidence Intervals for Regression Equations in Phylogenetic Comparative Methods , 2000, The American Naturalist.

[45]  D. Reid,et al.  A global molecular phylogeny of 147 periwinkle species (Gastropoda, Littorininae) , 2012 .

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

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

[48]  S. J. Arnold,et al.  Hot Rocks and Not-So-Hot Rocks: Retreat-Site Selection by Garter Snakes and Its Thermal Consequences , 1989 .

[49]  R. Barry,et al.  Processes and impacts of Arctic amplification: A research synthesis , 2011 .

[50]  J. Kingsolver,et al.  Ectotherm thermal stress and specialization across altitude and latitude. , 2013, Integrative and comparative biology.

[51]  Yun‐wei Dong,et al.  Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism , 2011, Journal of Experimental Biology.

[52]  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.

[53]  F. Turkheimer,et al.  On the Undecidability among Kinetic Models: From Model Selection to Model Averaging , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[54]  T. Wernberg,et al.  A decade of climate change experiments on marine organisms: procedures, patterns and problems , 2012 .

[55]  C. Mora,et al.  Experimental effect of cold, La Niña temperatures on the survival of reef fishes from Gorgona Island (eastern Pacific Ocean) , 2002 .

[56]  T. Blackburn,et al.  Climatic Predictors of Temperature Performance Curve Parameters in Ectotherms Imply Complex Responses to Climate Change , 2011, The American Naturalist.

[57]  D. Wethey,et al.  A biophysical basis for patchy mortality during heat waves. , 2015, Ecology.

[58]  M. Kearney,et al.  Habitat, environment and niche: what are we modelling? , 2006 .

[59]  W. Ponder,et al.  The Global Decline of Nonmarine Mollusks , 2004 .

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

[61]  Montgomery Slatkin,et al.  NULL MODELS FOR THE NUMBER OF EVOLUTIONARY STEPS IN A CHARACTER ON A PHYLOGENETIC TREE , 1991, Evolution; international journal of organic evolution.

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

[63]  J. Diniz‐Filho,et al.  Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. , 2012, Comprehensive Physiology.

[64]  R. Calsbeek,et al.  The impact of climate change measured at relevant spatial scales: new hope for tropical lizards , 2013, Global change biology.

[65]  A. Ellison,et al.  Origins of mangrove ecosystems and the mangrove biodiversity anomaly , 1999 .

[66]  V. Loeschcke,et al.  Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically , 2012, Proceedings of the National Academy of Sciences.

[67]  B. Helmuth Thermal biology of rocky intertidal mussels : Quantifying body temperatures using climatological data , 1999 .

[68]  B. Helmuth,et al.  Interactive effects of food availability and aerial body temperature on the survival of two intertidal Mytilus species. , 2010 .

[69]  G. Williams,et al.  Non-climatic thermal adaptation: implications for species' responses to climate warming , 2010, Biology Letters.

[70]  Lauren B. Buckley,et al.  Conservatism of lizard thermal tolerances and body temperatures across evolutionary history and geography , 2013, Biology Letters.

[71]  G. Vermeij,et al.  Molecular phylogenies and historical biogeography of a circumtropical group of gastropods (Genus: Nerita): implications for regional diversity patterns in the marine tropics. , 2008, Molecular phylogenetics and evolution.

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

[73]  Uang,et al.  The NCEP Climate Forecast System Reanalysis , 2010 .

[74]  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.

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

[76]  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.

[77]  C. Harley Tidal dynamics, topographic orientation, and temperature-mediated mass mortalities on rocky shores , 2008 .

[78]  M. Leal,et al.  Geographic variation in vulnerability to climate warming in a tropical Caribbean lizard , 2012 .

[79]  Joanna R. Bernhardt,et al.  Resilience to climate change in coastal marine ecosystems. , 2013, Annual review of marine science.

[80]  M. Kearney,et al.  Sensitivity to thermal extremes in Australian Drosophila implies similar impacts of climate change on the distribution of widespread and tropical species , 2014, Global change biology.

[81]  Anthony J. Rodriguez,et al.  Evolutionary stasis and lability in thermal physiology in a group of tropical lizards , 2014, Proceedings of the Royal Society B: Biological Sciences.

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

[83]  T. Bonebrake,et al.  Climate heterogeneity modulates impact of warming on tropical insects. , 2012, Ecology.

[84]  Paul R. Martin,et al.  Are mountain passes higher in the tropics? Janzen's hypothesis revisited. , 2006, Integrative and comparative biology.

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

[86]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[87]  D. Marshall,et al.  Boundary layer convective heating and thermoregulatory behaviour during aerial exposure in the rocky eulittoral fringe snail Echinolittorina malaccana , 2012 .

[88]  M. Frey The relative importance of geography and ecology in species diversification: evidence from a tropical marine intertidal snail (Nerita) , 2010 .

[89]  H. Stirling The upper temperature tolerance of prosobranch gastropods of rocky shores at Hong Kong and Dar Es Salaam, Tanzania , 1982 .