Organismal climatology: analyzing environmental variability at scales relevant to physiological stress

SUMMARY Predicting when, where and with what magnitude climate change is likely to affect the fitness, abundance and distribution of organisms and the functioning of ecosystems has emerged as a high priority for scientists and resource managers. However, even in cases where we have detailed knowledge of current species' range boundaries, we often do not understand what, if any, aspects of weather and climate act to set these limits. This shortcoming significantly curtails our capacity to predict potential future range shifts in response to climate change, especially since the factors that set range boundaries under those novel conditions may be different from those that set limits today. We quantitatively examine a nine-year time series of temperature records relevant to the body temperatures of intertidal mussels as measured using biomimetic sensors. Specifically, we explore how a ‘climatology’ of body temperatures, as opposed to long-term records of habitat-level parameters such as air and water temperatures, can be used to extrapolate meaningful spatial and temporal patterns of physiological stress. Using different metrics that correspond to various aspects of physiological stress (seasonal means, cumulative temperature and the return time of extremes) we show that these potential environmental stressors do not always occur in synchrony with one another. Our analysis also shows that patterns of animal temperature are not well correlated with simple, commonly used metrics such as air temperature. Detailed physiological studies can provide guidance to predicting the effects of global climate change on natural ecosystems but only if we concomitantly record, archive and model environmental signals at appropriate scales.

[1]  M. Saier,et al.  Climate Change, 2007 , 2007 .

[2]  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 .

[3]  M. Huber,et al.  Quantifying the quality of coral bleaching predictions , 2009, Coral Reefs.

[4]  Michael O'Donnell,et al.  Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale , 2008 .

[5]  G. Hofmann,et al.  Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. , 2001, The Journal of experimental biology.

[6]  G. Somero,et al.  Complex patterns of expression of heat‐shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytilus californianus and snail Nucella ostrina , 2006 .

[7]  Lauren B. Buckley,et al.  Linking Traits to Energetics and Population Dynamics to Predict Lizard Ranges in Changing Environments , 2007, The American Naturalist.

[8]  Laura J. Falkenberg,et al.  Synergistic effects of climate change and local stressors: CO2 and nutrient‐driven change in subtidal rocky habitats , 2009 .

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

[10]  R. Etter PHYSIOLOGICAL STRESS AND COLOR POLYMORPHISM IN THE INTERTIDAL SNAIL NUCELLA LAPILLUS , 1988, Evolution; international journal of organic evolution.

[11]  N. Mieszkowska,et al.  Changes in the Range of Some Common Rocky Shore Species in Britain – A Response to Climate Change? , 2006, Hydrobiologia.

[12]  Roberto Danovaro,et al.  Exponential Decline of Deep-Sea Ecosystem Functioning Linked to Benthic Biodiversity Loss , 2008, Current Biology.

[13]  M. Kearney,et al.  Modelling species distributions without using species distributions: the cane toad in Australia under current and future climates , 2008 .

[14]  G. Hofmann,et al.  Genomics-fueled approaches to current challenges in marine ecology. , 2005, Trends in ecology & evolution.

[15]  B. Menge,et al.  Experimental demonstration of plasticity in the heat shock response of the intertidal mussel Mytilus californianus , 2004 .

[16]  R. Burton,et al.  Proline biosynthesis genes and their regulation under salinity stress in the euryhaline copepod Tigriopus californicus. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[17]  R. Huey,et al.  Life history consequences of temperature transients in Drosophila melanogaster , 2007, Journal of Experimental Biology.

[18]  S. Gaines,et al.  Spatial patterns of growth in the mussel, Mytilus californianus, across a major oceanographic and biogeographic boundary at Point Conception, California, USA , 2007 .

[19]  D. Wethey,et al.  Water flow influences oxygen transport and photosynthetic efficiency in corals , 2006, Coral Reefs.

[20]  Christopher D G Harley,et al.  The impacts of climate change in coastal marine systems. , 2006, Ecology letters.

[21]  J. Widdows Physiological adaptation ofMytilus edulis to cyclic temperatures , 2004, Journal of comparative physiology.

[22]  Christopher D G Harley,et al.  Contingencies and compounded rare perturbations dictate sudden distributional shifts during periods of gradual climate change , 2009, Proceedings of the National Academy of Sciences.

[23]  W. Bradshaw,et al.  Evolutionary Response to Rapid Climate Change , 2006, Science.

[24]  W. Bradshaw,et al.  Climate change. Evolutionary response to rapid climate change. , 2006, Science.

[25]  Elizabeth P Dahlhoff,et al.  Biochemical indicators of stress and metabolism: applications for marine ecological studies. , 2004, Annual review of physiology.

[26]  Kevin J. Gaston,et al.  Macrophysiology: large‐scale patterns in physiological traits and their ecological implications , 2004 .

[27]  D. Wethey,et al.  Linking Thermal Tolerances and Biogeography: Mytilus edulis (L.) at its Southern Limit on the East Coast of the United States , 2009, The Biological Bulletin.

[28]  Brian Helmuth,et al.  Confronting the physiological bottleneck: A challenge from ecomechanics , 2009, Integrative and comparative biology.

[29]  W. Du,et al.  Embryonic development rate and hatchling phenotypes in the Chinese three-keeled pond turtle (Chinemys reevesii): The influence of fluctuating temperature versus constant temperature , 2009 .

[30]  W. Skirving,et al.  Sea-surface temperature and thermal stress in the Coral Triangle over the past two decades , 2009, Coral Reefs.

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

[32]  M. Chapman,et al.  Recruitment determines differences between assemblages on shaded or unshaded seawalls , 2006 .

[33]  William J. Skirving,et al.  A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions , 2004, Coral Reefs.

[34]  R. Paine,et al.  Marine rocky shores and community ecology : an experimentalist's perspective , 1995 .

[35]  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.

[36]  B. Helmuth,et al.  Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure , 2005 .

[37]  L. W. Hutchins The Bases for Temperature Zonation in Geographical Distribution , 1947 .

[38]  H. Pörtner,et al.  Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

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

[40]  D. Morritt,et al.  Summer mortality: effects on the distribution and abundance of the acorn barnacle Tetraclita japonica on tropical shores , 2006 .

[41]  E. Sanford Water Temperature, Predation, and the Neglected Role of Physiological Rate Effects in Rocky Intertidal Communities1 , 2002, Integrative and comparative biology.

[42]  J. Liu,et al.  Changes of reanalysis-derived Northern Hemisphere summer warm extreme indices during 1948-2006 and links with climate variability , 2008 .

[43]  K. Fabricius Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching? , 2006 .

[44]  J. Lawton,et al.  Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change , 1998 .

[45]  A. Strong,et al.  APPLYING MCSST TO CORAL REEF BLEACHING , 1995 .

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

[47]  Barry Sinervo,et al.  Field physiology: physiological insights from animals in nature. , 2004, Annual review of physiology.

[48]  F. B. Smith,et al.  Radionuclide deposition from the Chernobyl cloud , 1986, Nature.

[49]  C. Bayne,et al.  The physiological ecology of Mytilus californianus Conrad , 1976, Oecologia.

[50]  D. Wethey Biogeography, Competition, and Microclimate: The Barnacle Chthamalus fragilis in New England1 , 2002, Integrative and comparative biology.

[51]  K. A. S. Mislan,et al.  Predator–prey interactions under climate change: the importance of habitat vs body temperature , 2009 .

[52]  T. H. Clutton-Brock,et al.  Why large-scale climate indices seem to predict ecological processes better than local weather , 2004, Nature.

[53]  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.

[54]  D. Wethey Intrapopulation variation in growth of sessile organisms: natural populations of the intertidal barnacle Balanus balanoides , 1983 .

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

[56]  P. W. Glynn,et al.  Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality , 1990, Coral Reefs.

[57]  R. S. Appeldoorn,et al.  Sea surface temperatures and coral reef bleaching off La Parguera, Puerto Rico (northeastern Caribbean Sea) , 1998, Coral Reefs.

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

[59]  Mark R. Patterson,et al.  A Chemical Engineering View of Cnidarian Symbioses , 1992 .

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

[61]  J. Wiens,et al.  Climatic zonation drives latitudinal variation in speciation mechanisms , 2007, Proceedings of the Royal Society B: Biological Sciences.

[62]  J. Widdows Physiological Indices of Stress in Mytilus Edulis , 1978, Journal of the Marine Biological Association of the United Kingdom.

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

[64]  G. Somero,et al.  Time Course and Magnitude of Synthesis of Heat‐Shock Proteins in Congeneric Marine Snails (Genus Tegula) from Different Tidal Heights , 2000, Physiological and Biochemical Zoology.

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

[66]  Brian Helmuth,et al.  From cells to coastlines: how can we use physiology to forecast the impacts of climate change? , 2009, Journal of Experimental Biology.

[67]  A. Farrell,et al.  Physiology and Climate Change , 2008, Science.

[68]  F. Vernberg,et al.  Compartive physiology: latitudinal effects on physiological properties of animal populations. , 1962, Annual review of physiology.

[69]  B. Helmuth,et al.  Morphological and Ecological Determinants of Body Temperature of Geukensia demissa, the Atlantic Ribbed Mussel, and Their Effects On Mussel Mortality , 2007, The Biological Bulletin.

[70]  F. Micheli,et al.  Implications of spatial heterogeneity for management of marine protected areas (MPAs): examples from assemblages of rocky coasts in the northwest Mediterranean. , 2003, Marine environmental research.

[71]  L. Tomanek The Importance of Physiological Limits in Determining Biogeographical Range Shifts due to Global Climate Change: The Heat‐Shock Response , 2008, Physiological and Biochemical Zoology.

[72]  D. M. Gates,et al.  THERMODYNAMIC EQUILIBRIA OF ANIMALS WITH ENVIRONMENT , 1969 .

[73]  K. J. Willis,et al.  The ability of climate envelope models to predict the effect of climate change on species distributions , 2007 .

[74]  A. Southward Note on the Temperature Tolerances of some Intertidal animals in Relation to Environmental Temperatures and Geographical Distribution , 1958, Journal of the Marine Biological Association of the United Kingdom.

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

[76]  David S. Wethey,et al.  Ecological hindcasting of biogeographic responses to climate change in the European intertidal zone , 2008, Hydrobiologia.

[77]  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 .

[78]  Masson-Delmotte,et al.  The Physical Science Basis , 2007 .

[79]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[80]  P. Schulte,et al.  Swimming Performance and Energetics as a Function of Temperature in Killifish Fundulus heteroclitus , 2008, Physiological and Biochemical Zoology.

[81]  T. Dawson,et al.  Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? , 2003 .

[82]  G. Somero,et al.  Rhythms of Gene Expression in a Fluctuating Intertidal Environment , 2008, Current Biology.

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

[84]  D. Jenni A Study of the Ecology of Four Species of Herons during the Breeding Season at Lake Alice, Alachua County, Florida , 1969 .

[85]  J. Kingsolver,et al.  Biophysics, physiological ecology, and climate change: does mechanism matter? , 2005, Annual review of physiology.

[86]  S. Solomon The Physical Science Basis : Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change , 2007 .

[87]  S. Gaines,et al.  New Tools to Meet New Challenges: Emerging Technologies for Managing Marine Ecosystems for Resilience , 2008 .

[88]  Vincent R. Gray Climate Change 2007: The Physical Science Basis Summary for Policymakers , 2007 .

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

[90]  A. Mysterud,et al.  Review article. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[91]  K. Mach,et al.  Thermal stress and morphological adaptations in limpets , 2009 .

[92]  K. Gaston,et al.  The geographical range structure of the Holly Leaf-miner. III. Cold hardiness physiology , 2003 .

[93]  G. Somero Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits , 2005, Frontiers in Zoology.

[94]  S. Hawkins,et al.  Seventy years' observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature , 1995 .

[95]  K. Schneider Heat Stress in the Intertidal: Comparing Survival and Growth of an Invasive and Native Mussel Under a Variety of Thermal Conditions , 2008, The Biological Bulletin.

[96]  Lauren Yamane,et al.  Opposite responses by an intertidal predator to increasing aquatic and aerial temperatures , 2009 .

[97]  J. Beukema,et al.  Some like it cold: populations of the tellinid bivalve Macoma balthica (L.) suffer in various ways from a warming climate , 2009 .

[98]  B. Helmuth,et al.  Living on the Edge of Two Changing Worlds: Forecasting the Responses of Rocky Intertidal Ecosystems to Climate Change , 2006 .

[99]  L. Benedetti-Cecchi,et al.  Variability in abundance of algae and invertebrates at different spatial scales on rocky sea shores , 2001 .

[100]  B. Menge,et al.  INTERTIDAL MUSSELS EXHIBIT ENERGETIC TRADE‐OFFS BETWEEN REPRODUCTION AND STRESS RESISTANCE , 2008 .

[101]  L. Tomanek,et al.  Heat-Shock Protein 70 (Hsp70) as a Biochemical Stress Indicator: an Experimental Field Test in Two Congeneric Intertidal Gastropods (Genus: Tegula) , 2003, The Biological Bulletin.

[102]  Christopher D G Harley,et al.  Hot limpets: predicting body temperature in a conductance-mediated thermal system , 2006, Journal of Experimental Biology.

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

[104]  Benjamin S Halpern,et al.  Interactive and cumulative effects of multiple human stressors in marine systems. , 2008, Ecology letters.

[105]  B. Helmuth,et al.  Testing the effects of wave exposure, site, and behavior on intertidal mussel body temperatures: applications and limits of temperature logger design , 2004 .