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Rates of warming and the global sensitivity of shallow water marine invertebrates to elevated temperature

Published online by Cambridge University Press:  11 March 2014

S.A. Morley*
Affiliation:
British Antarctic Survey, High Cross, Madingley Road, Cambridge, Cambridgeshire, CB3 0ET, UK
A.E. Bates
Affiliation:
National Oceanography Centre, University of Southampton Waterfront Campus, Southampton SO14 3ZH, UK
M Lamare
Affiliation:
Department of Marine Science, University of Otago, Dunedin, New Zealand
J Richard
Affiliation:
Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer, Laboratoire de Sciences de l'Environnement Marin (UMR CNRS 6539), Technopôle Brest-Iroise, Place Copernic, F-29280 Plouzané, France
K.D. Nguyen
Affiliation:
Tropical Marine Science Institute, National University of Singapore, 14 Kent Ridge Road, Singapore 119223, Singapore
J Brown
Affiliation:
Environmental Management Division, Environment and Natural Resources Directorate, St Helena Government, Essex House, Jamestown, St Helena STHL 1ZZ
L.S. Peck
Affiliation:
British Antarctic Survey, High Cross, Madingley Road, Cambridge, Cambridgeshire, CB3 0ET, UK
*
Correspondence should be addressed to: S. A. Morley, British Antarctic Survey, High Cross, Madingley Road Cambridge, Cambridgeshire, CB3 0ET, UK email: smor@bas.ac.uk

Abstract

Assessing the sensitivity of ectotherms to variability in their environment is a key challenge, especially in the face of rapid warming of the Earth's surface. Comparing the upper temperature limits of species from different regions, at different rates of warming, has recently been developed as a method to estimate the long term sensitivity of shallow marine fauna. This paper presents the first preliminary data from four tropical Ascension Island, five temperate New Zealand and six Antarctic McMurdo Sound species. The slopes and intercepts of these three assemblages fitted within the overall pattern for previously measured assemblages from high temperature tolerance in tropical fauna and a shallow slope, to low temperature tolerance and a steep slope in Antarctic fauna. Despite the tropical oceanic Ascension Island being subject to upwelling events, the fit of the intercept and slope within the overall assemblage pattern suggests that the upwelling is sufficiently predictable for the fauna to have evolved the plasticity to respond. This contrasts with previously analysed species from the Peruvian upwelling region, which had a steeper slope than other temperate fauna. The speed and capacity of faunal assemblages to acclimatize their physiology is likely to determine the shape of the rates of warming relationship, and will be a key mechanism underpinning vulnerability to climate warming.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Barnes, D.K.A., Peck, L.S. and Morley, S.A. (2010) Ecological relevance of laboratory determined temperature limits: colonization potential, biogeography and resilience of Antarctic invertebrates to environmental change. Global Change Biology 16, 31643169.CrossRefGoogle Scholar
Calosi, P., Bilton, D.T and Spicer, I. (2008) Thermal tolerance, acclimatory capacity and vulnerability to climate change. Biology Letters 4, 99102.CrossRefGoogle ScholarPubMed
Chou, R. and Lee, H.B. (1997) Commercial fish farming in Singapore. Aquaculture Research 28, 767776CrossRefGoogle Scholar
Chown, S.L., Jumban, K.R., Sørensen, J.G. and Terblanche, J.S. (2009) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Functional Ecology 23, 133140.CrossRefGoogle Scholar
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. and Martin, P.R. (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Science of the United States of America 105, 66686672.CrossRefGoogle ScholarPubMed
Gaston, K.J., Chown, S.L., Calosi, P., Bernado, J., Bilton, D.T., Clarke, A, Clusella-Trullas, S., Ghalambor, C.K., Konarzewski, M., Peck, L.S., Porter, W.P., Pörtner, H.O., Rezende, E.L., Schulte, P.M., Spicer, J.I., Stillman, J.H., Terblanche, J.S. and van Kleunen, M. (2009) Macrophysiology: a conceptual reunification. American Naturalist 174, 595612.CrossRefGoogle ScholarPubMed
Goodwin, E. and Cornelisen, C.D. (2012) Near-surface water temperatures in Doubtful Sound and response to natural and anthropogenic drivers. New Zealand Journal of Marine and Freshwater 46, 411429.CrossRefGoogle Scholar
Helmuth, B.H. (2002) How do we measure the environment? Linking intertidal physiology and ecology through biophysics. Integrative and Comparative Biology 42, 837845.CrossRefGoogle ScholarPubMed
Helmuth, B.H. (2009) From cells to coastlines: how can we use physiology to forecast the impacts of climate change? Journal of Experimental Biology 212, 753760.CrossRefGoogle ScholarPubMed
Helmuth, B., Harley, C.D.G., Halpin, P.M., O'Donnell, M., Hofmann, G.E. and Blanchette, C.A. (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298, 10151017.CrossRefGoogle ScholarPubMed
Hochachka, P.W. and Somero, G.N. (2002) Biochemical adaptation: mechanism and process in physiological evolution. New York: Oxford University Press.CrossRefGoogle Scholar
Hunt, B.M., Hoefling, K. and Cheng, C.H.C. (2003) Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fishes. Antarctic Science 15, 333338.CrossRefGoogle Scholar
Irving, R.A. (1989) A preliminary investigation of the sublittoral habitats and communities of Ascension Island, South Atlantic. Progressive Underwater Science 13, 6578.Google Scholar
Leroi, A.M., Bennett, A.F. and Lenski, R.E. (1994). Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proceedings of the National Academy of Science of the United States of America 91, 19171921.CrossRefGoogle ScholarPubMed
Mora, C. and Moya, M.F. (2006) Effect of the rate of temperature increase of the dynamic method on the heat tolerance of fishes. Journal of Thermal Biology 31, 337341.CrossRefGoogle Scholar
Morley, S.A., Martin, S.M., Bates, A.E., Clark, M.S., Ericson, J., Lamare, M. and Peck, L.S. (2012) Spatial and temporal variation in the heat tolerance limits of two abundant Southern Ocean invertebrates. Marine Ecology Progress Series 450, 8192.CrossRefGoogle Scholar
Nguyen, K.D.T., Morley, S.A., Lai, C.-H., Clark, M.S., Tan, K.S., Bates, A.E. and Peck, L.S. (2011) Upper temperature limits of tropical marine ectotherms: global warming implications. PloS One 6, e29340. doi:10.1371/journal.pone.0029340.CrossRefGoogle ScholarPubMed
Peck, L.S., Clark, M.S., Morley, S.A., Massey, A. and Rossetti, H. (2009) Animal temperature limits and ecological relevance: effects of size, activity and rates of change. Functional Ecology 23, 248256.CrossRefGoogle Scholar
Peck, L.S., Morley, S.A., Richard, J. and Clark, M.S. (2014) Acclimation and thermal tolerance in Antarctic marine ectotherms. Journal of Experimental Biology 217, 1622.CrossRefGoogle ScholarPubMed
Pennisi, E. (2005) What determines species diversity? Science 309, 90.CrossRefGoogle ScholarPubMed
Pinheiro, H.T., Gasparini, J.L. and Joyeux, J.-C. (2010) Reef fish mass mortality event in an isolated island off Brazil, with notes on recent similar events at Ascension, St Helena and Maldives. Marine Biodiversity Records e47, 14. doi:http://dx.doi.org/10.1017/S1755267210000424.Google Scholar
Richard, J., Morley, S.A., Thorne, M.A.S. and Peck, L.S. (2012) Estimating long-term survival temperatures at the assemblage level in the marine environment: towards macrophysiology. PLoS One 7, e34655. doi:10.1371/journal.pone.0034655.CrossRefGoogle ScholarPubMed
Sanchez-Fernandez, D., Aragón, P., Bilton, D.T. and Lobo, J.M. (2012) Assessing the congruence of thermal niche estimations derived from distributions and physiological data. A test using diving beetles. PLoS One 7, e48163. doi:10.1371/journal.pone.0048163.CrossRefGoogle Scholar
Shaw, A.G.P., Kavalieris, L. and Vennell, R. (1999) Seasonal and inter-annual variability of SST off the east coast of South Island, New Zealand. Geocarta International 14, 2934.CrossRefGoogle Scholar
Somero, G.N. (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology 213, 912920.CrossRefGoogle ScholarPubMed
Spicer, J.I. and Gaston, K.J. (1999) Physiological diversity and its ecological implications. Oxford: Blackwell Science.Google Scholar
Stillman, J.H. (2003) Acclimation capacity underlies susceptibility to climate change. Science 301, 65.CrossRefGoogle ScholarPubMed
Stillman, J.H. and Somero, G.N. (2000) A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: influence of latitude, vertical zonation, acclimation, and phylogeny. Physiological and Biochemical Zoology 73, 200208.CrossRefGoogle ScholarPubMed
Sunday, J.M., Bates, A.E. and Dulvy, N.K. (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proceedings of the Royal Society of London, B 278, 18231830.Google ScholarPubMed
Terblanche, J.S., Deere, J.A., Clusella-Trullas, S., Jannion, C. and Chown, S.L. (2007) Critical thermal limits depend on methodological context. Proceedings of the Royal Society of London, B, 274, 29352942.Google ScholarPubMed
Tewksbury, J.J., Huey, R.B. and Deutsch, C.A. (2008) Putting the heat on tropical animals. Science 320, 12961297.CrossRefGoogle ScholarPubMed
Verberk, C.E.P. and Calosi, P. (2012) Oxygen limits heat tolerance and drives heat hardening in the aquatic nymphs of the gill breathing damselfly Calopteryx virgo (Linnaeus, 1758). Journal of Thermal Biology 37, 224229.CrossRefGoogle Scholar
Weber, S.B., Blount, J.D., Godley, B.J., Witt, M.J. and Broderick, A.C. (2011) Rate of egg maturation in marine turtles exhibits ‘universal temperature dependence’. Journal of Animal Ecology 80, 10341041.CrossRefGoogle ScholarPubMed
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