Abstract
We investigated physiological traits responsible for determining the tide-height and latitudinal distributions of Northeastern Pacific Nucella congeners. First, we determined the thermotolerances of two species of intertidal dogwhelks, N. ostrina and N. canaliculata, which co-occur on the Oregon coast. We found that N. ostrina, which are distributed higher on the shore, and thus experience higher habitat temperatures, than N. canaliculata, had correspondingly higher heat-coma temperatures. Second, we acclimated individuals of all five Northeastern Pacific Nucella congeners to a common temperature and determined their thermotolerances, measured as recovery from thermal exposure, after a 5-day, 3-week, and 7-week acclimation period. The south-latitude (N. emarginata) and mid-latitude (N. ostrina) high-intertidal species were more thermotolerant than the mid-latitude low-intertidal (N. canaliculata and N. lamellosa) and north-latitude high-intertidal (N. lima) species. The results of these two experiments suggest that temperature plays a role in determining the tide-height and latitudinal distributions of these Nucella species. Finally, we measured total and inducible levels of an evolutionarily conserved and ecologically relevant protein, the 70-kDa heat-shock protein (Hsp70), which has been found to confer thermotolerance in model laboratory organisms. The results showed that the level of total, not stress inducible, Hsp70 was a better predictor of thermotolerance and that there were species-specific differences in the relationship between Hsp70 expression and thermotolerance. We suggest that Hsp70 expression may be important in conferring thermotolerance in Nucella species in nature and that higher levels of molecular chaperones may underlie increased thermotolerance between conspecifics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bertness MD, Schneider DE (1976) Temperature relations of Puget Sound Thaids in reference to their intertidal distribution. Veliger 19:47–58
Bertness MD, Leonard GH, Levine JM, Bruno JF (1999) Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place. Oecologia 120:446–450
Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279
Buckley BA, Owen M-E, Hofmann GE (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. J Exp Biol 204:3571–3579
Collins TM, Frazer K, Palmer AR, Vermeij GJ, Brown WM (1996) Evolutionary history of northern hemisphere Nucella (Gastropoda, Muricidae): molecular, morphological, ecological, and paleontological evidence. Evolution 50:2287–2304
Dahlhoff EP, Buckley BA, Menge BA (2001) Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82:2816–2829
Dietz TJ, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). Proc Natl Acad Sci USA 89:3389–3393
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Feder ME, Cartaño NV, Milos L, Krebs RA, Lindquist SL (1996) Effect of engineering Hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster. J Exp Biol 199:1837–1844
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Halpin PM, Sorte CJ, Hofmann GE, Menge BA (2002) Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Integr Comp Biol 42:815–824
Hartl FU, Hayer-Hartl, M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858
Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384
Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017
Hoffmann AA, Blows MW (1994) Species borders: ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227
Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889–900
Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and HSP70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518
Hofmann GE, Somero GN (1996a) Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol Mar Biol Biotech 5:175–184
Hofmann GE, Somero GN (1996b) Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat-shock response and protein ubiquitination. Mar Biol 126:65–75
Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:S91-S115
Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N (1982) Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42:2457–2461
Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191
Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757
Newell RC (1979) Biology of intertidal animals. Marine Ecological Surveys, Faversham, UK
Palmer AR (1980) A comparative and experimental study of feeding and growth in thaidid gastropods. PhD dissertation, University of Washington, Seattle, Wash.
Palmer AR, Gayron SD, Woodruff DS (1990) Reproductive, morphological, and genetic evidence for two cryptic species of Northeastern Pacific Nucella. Veliger 33:325–338
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–439
Roberts DA, Hofmann GE, Somero GN (1997) Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol Bull 192:309–320
Sagarin RD, Gaines SD (2002) The ‘abundant centre’ distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147
Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75
Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097
Sanford E (2002) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218
Sokolova IM, Pörtner H-O (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207
Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68
Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789
Sorte CJB (2003) The ecophysiological underpinnings of biogeographic patterns: temperature effects on the distributions of Nucella congeners. MA thesis, University of California, Santa Barbara, Calif.
Sorte CJB, Hofmann GE (2004) Changes in latitudes, changes in aptitudes: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge. Mar Ecol Progr Ser 274:263–268
Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65
Tomanek L, Somero GN (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. J Exp Biol 202:2925–2936
Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiol Biochem Zool 73:249–256
Acknowledgements
We would like to thank our Alaskan collectors, A. Baldwin and M. Ahlgren, for supplying us with Nucella lima and S. Sorte for help in the field. Members of the Lubchenco-Menge Lab (OSU) and Foltz Lab (UCSB) generously provided equipment and lab space. J. Burnaford, K. Foltz, S. Gaines, P. Halpin, B. Helmuth, B. Menge, E. Sanford, and members of the Hofmann Lab (UCSB) gave helpful comments on the research and manuscript. This study would not have been possible without M. Bracken’s help with fieldwork, statistical savvy, and insightful comments. This research was supported by a Grant-in-Aid of Research from Sigma Xi, the Scientific Research Society to C.J.B.S., National Science Foundation grant IBN0097100 to G.E.H., and support from Susan and Bruce Worster to G.E.H. as the Worster Scholar at UCSB. The described experiments and specimen collections comply with the current laws of the United States of America and the regulations of the California Department of Fish and Game.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco, Chauvin
Rights and permissions
About this article
Cite this article
Sorte, C.J.B., Hofmann, G.E. Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella species with different biogeographical ranges. Marine Biology 146, 985–993 (2005). https://doi.org/10.1007/s00227-004-1508-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-004-1508-2