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Physiological consequences of the supralittoral fringe: microhabitat temperature profiles and stress protein levels in the tropical periwinkle Cenchritis muricatus (Linneaus, 1758)

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Abstract

Habitat selection by marine snails is profoundly affected by variations in biotic and abiotic factors. In the supralittoral fringe of Caribbean rocky shores, the littorinid Cenchritis muricatus endures a near-terrestrial existence through a combination of active microhabitat choice and, during dry periods, repose. In this study, we sought to compare knobby periwinkle body size, thermal load, water loss, and stress protein expression among common supralittoral microhabitats to determine the physiological consequences of habitat selection. In this study, we show: (1) body temperatures in these snails exhibit daily fluctuations of more than 20°C and regularly exceed 46°C, (2) microhabitats differ in thermal stress over small spatial scales, with snails on black rocks and within crevices experiencing more extreme temperatures than snails on white rocks or grass, (3) water losses of 8.5% of total snail mass do not affect survival during 1 week, and (4) Hsp70, but not Hsp90, expression varies slightly among microhabitats but at a level much lower than physiologically possible. During arousal following hydration, snails exhibited substantially higher levels of Hsp70s than snails on dry substrates in the field. When inactive, Cenchritis appears to utilize a distinctly different physiological state consistent with aestivation metabolism and does not exhibit significant up-regulation of inducible heat shock proteins (Hsps). In summary, studies lacking detailed thermal and hydration history, and relying only upon Hsp levels, may misrepresent the true physiological consequences of microhabitat choice for high-shore tropical gastropods.

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References

  • Arad, Z., T. Mizrahi, S. Goldenberg & J. Heller, 2010. Natural annual cycle of heat shock protein expression in land snails: desert versus Mediterranean species of Sphincterochila. Journal of Experimental Biology 213: 3487–3495.

    Article  PubMed  CAS  Google Scholar 

  • Atkinson, D., 1994. Temperature and organism size: a biological law for ectotherms? Advances in Ecological Research 3: 1–58.

    Article  Google Scholar 

  • Berger, M. S. & R. B. Emlet, 2007. Heat-shock response of the upper intertidal barnacle Balanus glandula: thermal stress and acclimation. Biological Bulletin 212: 232–241.

    Article  PubMed  CAS  Google Scholar 

  • Bonebrake, T. C. & M. D. Mastrandrea, 2010. Tolerance adaptation and precipitation changes complicate latitudinal patterns of climate change impacts. Proceedings of the National Academy of Sciences (USA) 107: 12581–12586.

    Article  CAS  Google Scholar 

  • Botton, M. L., M. Pogorzelska, L. Smoral, A. Shehata & M. G. Hamilton, 2006. Thermal biology of horseshoe crab embryos and larvae: a role for heat shock proteins. Journal of Experimental Marine Biology and Ecology 336: 65–73.

    Article  CAS  Google Scholar 

  • Britton, J. C., 1992. Evaporative water loss, behavior during emersion, and upper thermal tolerance limits in seven species of eulittoral-fringe Littorinidae (Mollusca: Gastropoda) from Jamaica. In Grahame, J., P. J. Mill & D. G. Reid (eds), Proceedings of the Third International Symposium on Littorinid Biology. Malacological Society of London, London: 69–83.

    Google Scholar 

  • Brun, N. T., V. M. Bricelj, T. H. MacRae & N. W. Ross, 2008. Heat shock protein responses in thermally stressed bay scallops, Argopecten irradians, and sea scallops, Placopecten magellanicus. Journal of Experimental Marine Biology and Ecology 358: 151–162.

    Article  CAS  Google Scholar 

  • Burgett, J. M., J. D. Cubit & R. C. Thompson, 1987. Seasonal growth patterns in the tropical littorinid snails Littorina angulifera and Tectarius muricatus. Veliger 30: 11–23.

    Google Scholar 

  • Chapman, M. G., 1997. Relationships between shell shape, water reserves, survival and growth of high shore littorinids under experimental conditions in New South Wales, Australia. Journal of Molluscan Studies 63: 511–529.

    Article  Google Scholar 

  • Chapman, M. G. & A. J. Underwood, 1996. Influences of tidal conditions, temperature and desiccation on patterns of aggregation of the high-shore periwinkle, Littorina unifasciata, in New South Wales, Australia. Journal of Experimental Marine Biology and Ecology 196: 213–237.

    Article  Google Scholar 

  • Chapperon, C. & L. Seuront, 2011. Behavioral thermoregulation in tropical gastropods: links to climate change scenarios. Global Change Biology 17: 1740–1749.

    Article  Google Scholar 

  • Chapple, J. P., G. R. Smerdon & A. J. S. Hawkins, 1997. Stress-protein induction in Mytilus edulis: tissue-specific responses to elevated temperature reflect relative vulnerability and physiological function. Journal of Experimental Marine Biology and Ecology 217: 225–235.

    Article  CAS  Google Scholar 

  • Connell, J. H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle, Chthamalus stellatus. Ecology 42: 133–146.

    Article  Google Scholar 

  • Connell, J. H., 1972. Community interactions on marine rocky intertidal shores. Annual Review of Ecology and Systematics 3: 169–192.

    Article  Google Scholar 

  • Dahlhoff, E. P., B. A. Buckley & B. A. Menge, 2001. Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82: 2816–2829.

    Google Scholar 

  • Denny, M. W. & C. D. G. Harley, 2006. Hot limpets: predicting body temperature in a conductance-mediated thermal system. Journal of Experimental Biology 209: 2409–2419.

    Article  PubMed  Google Scholar 

  • Deutsch, C. A., J. J. Tewksbury, R. B. Huey, K. S. Sheldon, C. K. Ghalambor, D. C. Haak & P. R. Martin, 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences (USA) 105: 6668–6672.

    Article  CAS  Google Scholar 

  • Elton, C., 1927. Animal Ecology. Sidgwick & Jackson, London: 209.

    Google Scholar 

  • Emson, R. H. & R. J. Faller-Fritsch, 1976. An experimental investigation into the effect of crevice availability on the abundance and size structure in a population of Littorina rudis (Maton); Gastropoda; prosobranchia. Journal of Experimental Marine Biology and Ecology 23: 285–297.

    Article  Google Scholar 

  • Emson, R. H., D. Morritt, E. B. Andrews & C. M. Young, 2002. Life on a hot dry beach: behavioral, physiological, and ultrastructural adaptations of the littorinid gastropod Cenchritis (Tectarius) muricatus. Marine Biology 140: 723–732.

    Article  Google Scholar 

  • Feder, M. E. & G. E. Hofmann, 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61: 243–282.

    Article  PubMed  CAS  Google Scholar 

  • Garrity, S. D., 1984. Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 59: 559–574.

    Article  Google Scholar 

  • Gray, D. R. & A. N. Hodgson, 2004. The importance of a crevice environment to the limpet Helcion pectunculus (Patellidae). Journal of Molluscan Studies 70: 67–72.

    Article  Google Scholar 

  • Halpin, P. M., B. A. Menge & G. E. Hofmann, 2004. Experimental demonstration of plasticity in the heat shock response of the intertidal mussel Mytilus californianus. Marine Ecology Progress Series 276: 137–145.

    Article  CAS  Google Scholar 

  • Harley, C. D. G., 2003. Abiotic stresses and herbivory interact to set range limits across a two-dimensional stress gradient. Ecology 84: 1477–1488.

    Article  Google Scholar 

  • Helmuth, B. S. T. & G. E. Hofmann, 2001. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biological Bulletin 201: 374–384.

    Article  PubMed  CAS  Google Scholar 

  • Helmuth, B., C. D. G. Harley, P. M. Halpin, M. O’Donnell, G. E. Hofmann & C. A. Blanchette, 2002. Climate change and latitudinal patterns of intertidal thermal stress. Science 298: 1015–1017.

    Article  PubMed  CAS  Google Scholar 

  • Hofmann, G. E., B. A. Buckley, S. P. Place & M. L. Zippay, 2002. Molecular chaperones in ectothermic marine animals: biochemical function and gene expression. Integrative and Comparative Biology 42: 808–814.

    Article  PubMed  CAS  Google Scholar 

  • Huey, R. B., 1991. Physiological consequences of habitat selection. American Naturalist 137: S91–S115.

    Article  Google Scholar 

  • Jackson, A. C., 2010. Effects of topography on the environment. Journal of the Marine Biological Association of the UK 90: 169–192.

    Article  Google Scholar 

  • Janzen, D. H., 1967. Why mountain passes are higher in the tropics. American Naturalist 101: 233–249.

    Article  Google Scholar 

  • Jones, K. M. M. & E. G. Boulding, 1999. State-dependent habitat selection by an intertidal snail: the cost of selecting a physically stressful microhabitat. Journal of Experimental Marine Biology and Ecology 242: 149–177.

    Article  Google Scholar 

  • Judge, M. L., R. Duell, L. Burriesci & W. Moarsi, 2009. Life in the supralittoral fringe: microhabitat choice, mobility and growth in the tropical periwinkle Cenchritis (=Tectarius) muricatus (Linneaus, 1758). Journal of Experimental Marine Biology and Ecology 369: 148–154.

    Article  Google Scholar 

  • Kingsolver, J. G., 2009. The well-temperatured biologist. American Naturalist 174: 755–768.

    Article  PubMed  Google Scholar 

  • Lang, R. C., J. C. Britton & T. Metz, 1998. What to do when there is nothing to do: the ecology of Jamaican intertidal Littorinidae (Gastropoda: Prosobranchia) in repose. Hydrobiologia 378: 161–185.

    Article  Google Scholar 

  • Lee, H. J. & E. G. Boulding, 2010. Latitudinal clines in body size, but not thermal tolerance or heat-shock cognate (HSC70), in the highly-dispersing intertidal gastropod Littorina keenae (Gastropoda: Littorinidae). Biological Journal of the Linnean Society 100: 494–505.

    Article  Google Scholar 

  • Levings, S. C. & S. D. Garrity, 1983. Diel and tidal movements of two co-occurring neritid snails: differences in grazing patterns on a tropical rocky shore. Journal of Experimental Marine Biology and Ecology 67: 261–278.

    Article  Google Scholar 

  • Lewis, J. R., 1964. The Ecology of Rocky Shores. English Universities Press, London: 323.

    Google Scholar 

  • Lewis, S., R. D. Handy, B. Cordi, Z. Billinghurst & M. H. Depledge, 1999. Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology 8: 351–368.

    Article  CAS  Google Scholar 

  • Marshall, D. J., C. D. McQuaid & G. A. Williams, 2010. Non-climatic thermal adaptation: implications for species’ responses to climate warming. Biology Letters 6: 669–673.

    Article  PubMed  Google Scholar 

  • McClintock, J., P. Melvin & K. Marion, 2007. Movement of periwinkle snails on the rocky shores of San Salvador. Bahamas Naturalist & Journal of Science 2: 63–68.

    Google Scholar 

  • McMahon, R. F., 1990. Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193: 241–260.

    Article  Google Scholar 

  • McMahon, R. F., 2001. Acute thermal tolerance in intertidal gastropods relative to latitude, superfamily, zonation and habitat with special emphasis on the Littorinoidea. Journal of Shellfish Research 20: 459–467.

    Google Scholar 

  • Miller, L. P., C. D. G. Harley & M. W. Denny, 2009. The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Functional Ecology 23: 756–767.

    Article  Google Scholar 

  • Minton, D. & D. J. Gochfeld, 2001. Is life on a tropical shore really so hard?: the role of abiotic factors in structuring a supralittoral molluscan assemblage. Journal of Shellfish Research 20: 477–483.

    Google Scholar 

  • Moore, H. B., 1972. Aspects of stress in the tropical environments. Advances in Marine Biology 10: 217–269.

    Article  Google Scholar 

  • Morin, P. J., 1989. Realism, precision, and generality in experimental ecology. In Resetarits, W. J. & J. Bernardo (eds), Experimental Ecology: Issues and Perspectives. Oxford, New York: 50–70.

    Google Scholar 

  • Pakay, J. L., P. C. Withers, A. A. Hobbs & M. Guppy, 2002. In vivo downregulation of protein synthesis in the snail Helix apersa during estivation. American Journal of Physiology: Regulatory, Integrative and Comparative 283: R197–R204.

    CAS  Google Scholar 

  • Peckol, P., S. Guarnagia & M. Fisher, 1989. Zonation and behavioral patterns of the intertidal gastropods Nodilittorina (Tectininus) antoni (Philippi, 1846) and Nerita versicolor Gmelin, 1791, in the Bahamas. Veliger 32: 8–15.

    Google Scholar 

  • Porter, W. P. & D. M. Gates, 1969. Thermodynamic equilibria of animals with environment. Ecological Monographs 39: 227–244.

    Article  Google Scholar 

  • Raffaelli, D. C. & R. N. Hughes, 1978. The effects of crevice size and availability on populations of Littorina rudis and Littorina neritoides. Journal of Animal Ecology 47: 71–83.

    Article  Google Scholar 

  • Roberts, D. A., G. E. Hofmann & G. N. Somero, 1997. Heat shock protein expression in Mytilus californianus: Acclimatization (seasonal and tide-height comparisons) and acclimation effects. Biological Bulletin 192: 309–320.

    Article  CAS  Google Scholar 

  • Schill, R. O., P. M. H. Gayle & H. R. Köhler, 2002. Daily stress protein (hsp70) cycle in chitons (Acanthopleura granulata Gmelin, 1791) which inhabit the rocky intertidal shoreline in a tropical ecosystem. Comparative Biochemistry and Physiology-Part C: Toxicology and Pharmacology 131: 253–258.

    Article  PubMed  Google Scholar 

  • Sigma Chemical, 2010. Product information monoclonal anti-heat shock protein 70 (HSP70) clone BRM-22. http://www.sigmaaldrich.com/etc./medialib/docs/Sigma/Datasheet/2/h5147dat.Par.0001.File.tmp/h5147dat.pdf. Accessed 24 August 2010.

  • Sørensen, J. G., T. N. Kristensen & V. Loeschcke, 2003. The evolutionary and ecological role of heat shock proteins. Ecology Letters 6: 1025–1037.

    Article  Google Scholar 

  • Sørensen, J. G., L.-H. Heckmann & M. Holmstrup, 2010. Temporal gene expression profiles in a palaearctic springtail as induced by desiccation, cold exposure and during recovery. Functional Ecology 24: 838–846.

    Article  Google Scholar 

  • Stephenson, T. A. & A. B. Stephenson, 1949. Universal features of zonation between tide marks on rocky coasts. Journal of Ecology 37: 289–305.

    Article  Google Scholar 

  • Stevenson, R. D., 1985. Body size and limits to the daily range of body temperature in terrestrial ectotherms. American Naturalist 125: 102–117.

    Article  Google Scholar 

  • Storey, K. B. & J. M. Storey, 1990. Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. The Quarterly Review of Biology 65: 145–174.

    Article  PubMed  CAS  Google Scholar 

  • Tomanek, L., 2005. Two-dimensional gel analysis of the heat-shock response in marine snails (genus Tegula): interspecific variation in protein expression and acclimation ability. Journal of Experimental Biology 208: 3133–3143.

    Article  PubMed  CAS  Google Scholar 

  • Tomanek, L. & G. N. Somero, 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 thermotolerance and biogeography. Journal of Experimental Biology 202: 2925–2936.

    PubMed  Google Scholar 

  • Tomanek, L. & G. N. Somero, 2000. Time course and magnitude of synthesis of heat shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiological and Biochemical Zoology 73: 249–256.

    Article  PubMed  CAS  Google Scholar 

  • Tomanek, L. & G. N. Somero, 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: 677–685.

    PubMed  CAS  Google Scholar 

  • Underwood, A. J., 1979. The ecology of intertidal gastropods. Advances in Marine Biology 16: 111–210.

    Article  Google Scholar 

  • Werner, E. E., 1989. Ecological experiments and a research program in community ecology. In Resetarits, W. J. & J. Bernardo (eds), Experimental Ecology: Issues and Perspectives. Oxford, New York: 3–26.

    Google Scholar 

  • Williams, G. A. & D. Morritt, 1995. Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Marine Ecology Progress Series 124: 89–103.

    Article  Google Scholar 

  • Williams, G. A., M. De Pirro, S. Cartwright, K. Khangura, W.-C. Ng, P. T. Y. Leung & D. Morritt, 2011. Come rain or shine: the combined effects of physical stresses on physiological and protein-level responses of an intertidal limpet in the monsoonal tropics. Functional Ecology 25: 101–110.

    Article  Google Scholar 

  • Wolcott, T. G., 1973. Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at “limiting factors”. Biological Bulletin 145: 389–422.

    Article  Google Scholar 

  • Zakhartsev, M., B. De Wachter, T. Johansen, H. O. Pörtner & R. Blust, 2005. Hsp70 is not a sensitive indicator of thermal limitation in Gadus morhua. Jouranl of Fish Biology 67: 767–778.

    Article  CAS  Google Scholar 

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Acknowledgments

Earlier drafts of this manuscript were improved by the comments of two anonymous reviewers. We are indebted to Virgin Islands Department of Planning and Natural Resources (Division of Fish and Wildlife, #SST-031-07 & #STX-013-08) and Virgin Islands National Park (US Department of the Interior, #VIIS-2007-SCI-0001) for the necessary permits to conduct this study, and the Virgin Islands Environmental Resource Station for its laboratory and lodging facilities. Several undergraduate research students from Manhattan College (Katie McCloskey) and Fordham College (Andrew Paska, Francesca LaRosa, and Anna-Maria Oprescu) assisted on this project. We gratefully acknowledge funding support from Manhattan College and Fordham University.

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Correspondence to Michael L. Judge.

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Judge, M.L., Botton, M.L. & Hamilton, M.G. Physiological consequences of the supralittoral fringe: microhabitat temperature profiles and stress protein levels in the tropical periwinkle Cenchritis muricatus (Linneaus, 1758). Hydrobiologia 675, 143–156 (2011). https://doi.org/10.1007/s10750-011-0812-3

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