Hostname: page-component-5d59c44645-mrcq8 Total loading time: 0 Render date: 2024-02-27T14:57:18.029Z Has data issue: false hasContentIssue false

Effects of temperature on heat-shock responses and survival of two species of marine invertebrates from sub-Antarctic Marion Island

Published online by Cambridge University Press:  26 June 2013

S. Clusella-Trullas*
Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Stellenbosch 7602, South Africa
L. Boardman
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Stellenbosch 7602, South Africa
K.T. Faulkner
Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Stellenbosch 7602, South Africa
L.S. Peck
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
S.L. Chown
School of Biological Sciences, Monash University, VIC 3800, Australia


This study examined high temperature survival and heat shock protein 70 (Hsp70) responses to temperature variation for two marine invertebrate species on sub-Antarctic Marion Island. The isopod Exosphaeroma gigas Leach and the amphipod Hyale hirtipalma Dana had the same tolerance to high temperature. The mean upper temperature which was lethal for 50% of the population (upper lethal temperature, ULT50) was 26.4°C for both species. However, the isopod E. gigas showed significant plasticity of ULT50, with a positive response to acclimation. In addition, the isopod had a heat shock response of Hsp70 at all acclimations, and the amount of Hsp70 protein increased significantly from basal levels upon an acute warm exposure after a cold acclimation. By contrast, the amphipod H. hirtipalma showed limited plasticity of ULT50 and no evidence for a heat shock response (failure of three different Hsp70 antibodies to bind to the extracted 70kDa proteins). Overall, these results reflect different flexibility of thermal tolerance of intertidal invertebrate species on Marion Island, with possible variation in the underlying cellular mechanisms, suggesting that warming associated with climate change may result in changes in species assemblage structure in sub-polar environments.

Biological Sciences
Copyright © Antarctic Science Ltd 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Angilletta, M.J. Jr, 2009. Thermal adaptation: a theoretical and empirical synthesis. New York: Oxford University Press, 320 pp.Google Scholar
Barua, D. Heckathorn, S.A. 2004. Acclimation of the temperature set-points of the heat shock response. Journal of Thermal Biology, 29, 185193.CrossRefGoogle Scholar
Bedulina, D.S., Evgen'ev, M.B., Timofeyev, M.A., Protopopova, M.V., Garbuz, D.G., Pavlichenko, V.V., Luckenbach, T., Shatilina, Z.M., Axenov-Gribanov, D.V., Gurkov, A.N., Sokolova, I.M. Zatsepina, O.G. 2013. Expression patterns and organization of the hsp70 genes correlate with thermotolerance in two congener endemic amphipod species (Eulimnogammarus cyaneus and E. verrucosus) from Lake Baikal. Molecular Ecology, 22, 14161430.CrossRefGoogle Scholar
Branch, M.L., Griffiths, C.L., Kensley, B. Sieg, J. 1991. The benthic Crustacea of sub-Antarctic Marion and Prince Edward Islands: illustrated keys to the species and results of the 1982–1989 University of Cape Town surveys. South African Journal of Antarctic Research, 21, 344.Google Scholar
Buckley, B.A., Owen, M.-E. Hofmann, G.E. 2001. Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. The Journal of Experimental Biology, 204, 35713579.CrossRefGoogle ScholarPubMed
Chapple, J.P., Smerdon, G.R., Berry, R.J. Hawkins, A.J.S. 1998. Seasonal changes in stress-70 protein levels reflect thermal tolerance in the marine bivalve Mytilus edulis L. Journal of Experimental Marine Biology and Ecology, 229, 5368.CrossRefGoogle Scholar
Clark, M.S., Fraser, K.P.P. Peck, L.S. 2008a. Antarctic marine molluscs do have an Hsp70 heat shock response. Cell Stress and Chaperones, 13, 3949.CrossRefGoogle ScholarPubMed
Clark, M.S., Fraser, K.P.P. Peck, L.S. 2008b. Lack of an HSP70 heat shock response in two Antarctic marine invertebrates. Polar Biology, 31, 10591065.CrossRefGoogle Scholar
Claussen, D.L. 1980. Thermal acclimation in the crayfish, Orconectes rusticus and O. virilis . Comparative Biochemistry and Physiology, 66A, 377384.Google Scholar
Davenport, J. Davenport, J.L. 2005. Effects of shore height, wave exposure and geographical distance on thermal niche width of intertidal fauna. Marine Ecology Progress Series, 292, 4150.Google Scholar
Davenport, J. MacAlister, H. 1996. Environmental conditions and physiological tolerances of intertidal fauna in relation to shore zonation at Husvik, South Georgia. Journal of Marine Biological Association of the United Kingdom, 76, 9851002.CrossRefGoogle Scholar
De Villiers, A.F. 1976. Littoral ecology of Marion and Prince Edward Islands (Southern Ocean). South African Journal of Antarctic Research, 1, 140.Google Scholar
Deere, J.A. Chown, S.L. 2006. Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. American Naturalist, 168, 630644.Google Scholar
Deere, J.A., Sinclair, B.J., Marshall, D.J. Chown, S.L. 2006. Phenotypic plasticity of thermal tolerances in five oribatid mite species from sub-Antarctic Marion Island. Journal of Insect Physiology, 52, 693700.CrossRefGoogle ScholarPubMed
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. Martin, P.R. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America, 105, 66686672.CrossRefGoogle ScholarPubMed
Dong, Y., Miller, L.P., Sanders, J.G. Somero, G.N. 2008. Heat-shock protein 70 (Hsp70) expression in four limpets of the Genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. The Biological Bulletin, 215, 173181.Google Scholar
Ferreira, T. Rasband, W. 2011. The ImageJ user guide., accessed October 2011.Google Scholar
Fraser, C.I., Nikula, R. Waters, J.M. 2011. Oceanic rafting by a coastal community. Proceedings of the Royal Society, B278, 649655.Google Scholar
Gabriel, W. Lynch, M. 1992. The selective advantage of reaction norms for environmental tolerance. Journal of Evolutionary Biology, 5, 4159.CrossRefGoogle Scholar
Gaston, K.J. Spicer, J.I. 1998. Do upper thermal tolerances differ in geographically separated populations of the beachflea Orchestia gammarellus (Crustacea: Amphipoda)? Journal of Experimental Marine Biology and Ecology, 229, 265276.CrossRefGoogle Scholar
Karl, I., Sørensen, J.G., Loeschcke, V. Fischer, K. 2009. HSP70 expression in the Copper butterfly Lycaena tityrus across altitudes and temperatures. Journal of Evolutionary Biology, 22, 172178.Google Scholar
Kelly, M.W., Sanford, E. Grosberg, R.K. 2011. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proceedings of the Royal Society, B279, 349356.Google Scholar
Kivivuori, L. Lagerspetz, K.Y.H. 1990. Thermal resistance and behaviour of the isopod Saduria entomon (L.). Annales Zoologici Fennici, 27, 287290.Google Scholar
La Terza, A., Papa, G., Miceli, C. Luporini, P. 2001. Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat-shock protein 70 genes. Molecular Ecology, 10, 10611067.Google Scholar
Le Roux, P.C. McGeoch, M.A. 2008. Changes in climate extremes, variability and signature on sub-Antarctic Marion Island. Climatic Change, 86, 309329.Google Scholar
Mélice, J-L., Lutjeharms, J.R.E., Rouault, M. Ansorge, I.J. 2003. Sea-surface temperatures at the sub-Antarctic islands Marion and Gough during the past 50 years. South African Journal of Science, 99, 363366.Google Scholar
Morritt, D. Ingólfsson, A. 2000. Upper thermal tolerance of the beachflea Orchestia gammarellus (Pallas) (Crustacea: Amphipoda: Talitridae) associated with hot springs in Iceland. Journal of Experimental Marine Biology and Ecology, 255, 215227.Google Scholar
Nikula, R., Fraser, C.I., Spencer, H.G. Walters, J.M. 2010. Circumpolar dispersal by rafting in two sub-Antarctic kelp-dwelling crustaceans. Marine Ecology Progress Series, 405, 221230.CrossRefGoogle Scholar
Osovitz, C.J. Hofmann, G.E. 2005. Thermal history-dependent expression of the hsp gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. Journal of Experimental Marine Biology and Ecology, 327, 134143.CrossRefGoogle Scholar
Peck, L.S., Convey, P. Barnes, K.A. 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biological Reviews, 81, 75109.CrossRefGoogle ScholarPubMed
Peck, L.S., Morley, S.A. Clark, M.S. 2010. Poor acclimation capacities in Antarctic marine ectotherms. Marine Biology, 157, 20512059.CrossRefGoogle Scholar
Roberts, D.A., Hofmann, G.E. Somero, G.N. 1997. Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. The Biological Bulletin, 192, 309320.CrossRefGoogle ScholarPubMed
Romero-Calvo, I., Ocón, B., Martínez-Moya, P., Suárez, M.D., Zarzuelo, A., Martínez-Augustin, O. De Medina, F.S. 2010. Reversible Ponceau staining as a loading control alternative to actin in Western blots. Analytical Biochemistry, 401, 318320.Google Scholar
Rouault, M., Mélice, J-L., Reason, C.J.C. Lutjeharms, J.R.E. 2005. Climate variability at Marion Island, Southern Ocean, since 1960. Journal of Geophysical Research, 10.1029/2004JC002492.Google Scholar
Sinclair, E.L.E., Thompson, M.B. Seebacher, F. 2006. Phenotypic flexibility in the metabolic response of the limpet Cellana tramoserica to thermally different microhabitats. Journal of Experimental Marine Biology and Ecology, 335, 131141.CrossRefGoogle Scholar
Sørensen, J.G., Loeschcke, V. Kristensen, T.N. 2013. Cellular damage as induced by high temperature is dependent on the rate of temperature change - investigating consequences of ramping rates on molecular and organismal phenotypes in Drosophila melanogaster Meigen 1830. Journal of Experimental Biology, 216, 809814.Google Scholar
Stillman, J.H. 2003. Acclimation capacity underlies susceptibility to climate change. Science, 301, 65.CrossRefGoogle ScholarPubMed
Stillman, J.H. Somero, G.N. 2000. A comparative analysis of the upper thermal tolerance limits of Eastern Pacific porcelain crabs, Genus Petrolisthes: influences of latitude, vertical zonation, acclimation and phylogeny. Physiological and Biochemical Zoology, 73, 200208.CrossRefGoogle ScholarPubMed
Tomanek, L. 2010. Variation in heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. Journal of Experimental Biology, 213, 971979.Google Scholar
Tomanek, L. Somero, G.N. 1999. Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (Genus Tegula) from different thermal habitats: implications for limits of thermaotolerance and biogeography. Journal of Experimental Biology, 202, 29252936.CrossRefGoogle ScholarPubMed
Tomanek, L. Somero, G.N. 2002. Interspecific- and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. Journal of Experimental Biology, 205, 677685.Google Scholar