Marine Biology

, Volume 158, Issue 6, pp 1223–1231 | Cite as

Variations in cardiac performance and heat shock protein expression to thermal stress in two differently zoned limpets on a tropical rocky shore

  • Yun-wei DongEmail author
  • Gray A. Williams
Original Paper


Understanding variation in physiological adaptations to thermal stress is vital when investigating intertidal species’ distribution patterns. The thermal sensitivities of two limpets, Cellana grata and C. toreuma, differed in accordance with their vertical distributions. Cardiac performance was maintained at higher temperatures (~47°C) for the high-zone C. grata than the mid-zone C. toreuma (~42°C). At 40°C, C. grata maintained regular heart function for ~4 h, while heart function of C. toreuma decreased rapidly. Heat shock protein expression revealed that C. toreuma had two constitutive isoforms, Hsp77 and Hsp72, and C. grata one inducible form, Hsp75, which was upregulated at 40°C, suggesting C. grata has a more effective heat shock response than C. toreuma. The temperature-adaptive differences in cardiac thermal tolerance and Hsp expression match observed differences in thermally induced mortalities with the onset of summer and may help predict differential effects of climate change on the two congeners.


Heat Stress Heat Shock Protein Heat Shock Response Cardiac Performance Rocky Shore 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



YD was supported by a Sino-British Fellowship Trust Visitorship awarded by The University of Hong Kong, National Natural Science Foundation of China (41076083) and the Fundamental Research Funds for the Central Universities (201012028). We thank Stephen Cartwright for his help in specimen collection, Wai Chuen Ng and Priscilla Leung (all SWIMS) for their help in heat shock protein assay and David Marshall (Universiti Brunei Darussalam) for his suggestions in heart rate measurement. We are also grateful to Tomoyuki Nakano (Museum of National History of Japan) for sharing information on the phylogeography of the two species and especially appreciate comments from Prof. George Somero (Hopkins Marine Station, Stanford University), Prof Hans-Otto Pörtner (Alfred Wegener Institute for Polar and Marine Research, Germany) and three referees, which have improved the manuscript.


  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42Google Scholar
  2. Anestis A, Pörtner H, Lazou A, Michaelidis B (2008) Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water: implications for vertical zonation. J Exp Biol 211:2889–2898CrossRefGoogle Scholar
  3. Branch GM (1981) The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr Mar Biol Annu Rev 19:235–380Google Scholar
  4. Broekhuysen GJ (1940) A preliminary investigation of the importance of desiccation, temperature, and salinity as factors controlling the vertical distribution of certain intertidal marine gastropods in False Bay, South Africa. Trans R Soc South Afr 28:255–292CrossRefGoogle Scholar
  5. Cartwright SR (2010) Facilitation of intertidal species against environmental stress by barnacles in tropical Hong Kong. Ph.D. thesis. The University of Hong Kong, Hong KongGoogle Scholar
  6. Chan BKK, Morritt D, De Pirro M, Leung KMY, Williams GA (2006) Summer mortality: effects on the distribution and abundance of the acorn barnacle Tetraclita japonica on tropical shores. Mar Ecol Prog Ser 328:195–204CrossRefGoogle Scholar
  7. Chelazzi G, Williams GA, Gray DR (1999) Field and laboratory measurement of heart rate in a tropical limpet, Cellana grata. J Mar Biol Assoc UK 79:749–751CrossRefGoogle Scholar
  8. Chelazzi G, De Pirro M, Williams GA (2001) Cardiac responses to abiotic factors in two tropical limpets, occurring at different levels of the shore. Mar Biol 139:1079–1085CrossRefGoogle Scholar
  9. Davenport J, Davenport JL (2005) Effects of shore height, wave exposure and geographical distance on thermal niche width of intertidal fauna. Mar Ecol Prog Ser 292:41–50CrossRefGoogle Scholar
  10. Denny MW, Harley CDG (2006) Hot limpets: predicting body temperature in a conductance-mediated thermal system. J Exp Biol 209:2420–2431CrossRefGoogle Scholar
  11. Denny M, Helmuth B (2009) Confronting the physiological bottleneck: a challenge from ecomechanics. Integr Comp Biol 49:197–201CrossRefGoogle Scholar
  12. Depledge MH, Andersen BB (1990) A computer-aided physiological monitoring system for continuous, long-term recording of cardiac activity in selected invertebrates. Comp Biochem Physiol 96:474–477CrossRefGoogle Scholar
  13. Dong YW, Miller LP, Sanders JG, Somero GN (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. Biol Bull 215:173–181CrossRefGoogle Scholar
  14. Evans RG (1948) The lethal temperatures of some common British littoral molluscs. J Anim Ecol 17:165–173CrossRefGoogle Scholar
  15. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282CrossRefGoogle Scholar
  16. Firth LB, Williams GA (2009) The influence of multiple environmental stressors on the limpet Cellana toreuma during the summer monsoon season in Hong Kong. J Exp Mar Biol Ecol 375:70–75CrossRefGoogle Scholar
  17. Garrity SD (1984) Some adaptation of gastropods to physical stress on a tropical rocky shore. Ecology 65:559–574CrossRefGoogle Scholar
  18. Harley CDG, Denny MW, Mach KJ, Miller LP (2009) Thermal stress and morphological adaptations in limpets. Funct Ecol 23:292–301CrossRefGoogle Scholar
  19. Harper KD, Williams GA (2001) Variation in abundance and distribution of the chiton Acanthopleura japonica and associated molluscs on a seasonal, tropical rocky shore. J Zool 253:293–300CrossRefGoogle Scholar
  20. Helmuth BST (2002) How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Integr Comp Biol 42:837–845CrossRefGoogle Scholar
  21. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  22. Hofmann GE, Somero GN (1996) 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 125:65–75CrossRefGoogle Scholar
  23. Huang R (2001) Spatial variation in Cellana grata populations: the interplay of population dynamics and food availability. PhD thesis. The University of Hong Kong, Hong KongGoogle Scholar
  24. Kaehler S, Williams GA (1996) Distribution of algae on tropical rocky shores: spatial and temporal patterns of non-coralline encrusting algae in Hong Kong. Mar Biol 125(1):177–187CrossRefGoogle Scholar
  25. Leung WM (2006) Climate change—the Hong Kong perspective. Living in a warmer world: climate change and Hong Kong. The University of Hong Kong, December 11–12th, 2006Google Scholar
  26. Little C, Williams GA, Trowbridge CD (2009) The biology of rocky shores, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  27. Marshall DJ, McQuaid DC (1992) Relationship between heart rate and oxygen consumption in the intertidal limpets Patella granularis and Siphonaria oculus. Comp Biochem Physiol 103A:297–300CrossRefGoogle Scholar
  28. McMahon RF (1990) Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193:241–260CrossRefGoogle Scholar
  29. McQuaid CD, Branch GM (1984) Influence of sea temperature, substratum and wave exposure on rocky intertidal communities: an analysis of faunal and floral biomass. Mar Ecol Prog Ser 19:145–151CrossRefGoogle Scholar
  30. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  31. Miller LP, Harley CDG, Denny MW (2009) The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Funct Ecol 23:756–767CrossRefGoogle Scholar
  32. Moore HB (1972) Aspects of stress in the tropical marine environment. Adv Mar Biol 10:217–269CrossRefGoogle Scholar
  33. Morton BS, Morton JE (1983) The seashore ecology of Hong Kong. Hong Kong University Press, Hong KongGoogle Scholar
  34. Newell RC (1979) Biology of intertidal animals. Marine Ecological Survey, FavershamGoogle Scholar
  35. Ng JSS (2007) Resource partitioning and coexistence of molluscan grazers on Hong Kong rocky shores. Ph.D. thesis. The University of Hong Kong, Hong KongGoogle Scholar
  36. Ngan A (2006) Environmental stress and its implications for behavioural plasticity of foraging in Cellana grata. Ph.D. thesis. The University of Hong Kong, Hong KongGoogle Scholar
  37. Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol 132A:739–761CrossRefGoogle Scholar
  38. Pörtner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893CrossRefGoogle Scholar
  39. Pörtner HO, Knust P (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefGoogle Scholar
  40. Pörtner HO, Bennett AE, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman FH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79(2):295–313CrossRefGoogle Scholar
  41. Sanders BM, Hope C, Pascoe VM, Martin LS (1991) Characterization of stress protein response in two species of Collisella limpets with different temperature tolerance. Physiol Zool 64:1471–1489CrossRefGoogle Scholar
  42. Santini G, Chelazzi G (1995) Glycogen content and rates of depletion in two limpets with different foraging regimes. Comp Biochem Physiol 111:271–277CrossRefGoogle Scholar
  43. Santini G, De Pirro M, Chelazzi G (1999) In situ and laboratory assessment of heart rate in a Mediterranean limpet using a noninvasive technique. Physiol Biochem Zool 72:198–204CrossRefGoogle Scholar
  44. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789CrossRefGoogle Scholar
  45. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920CrossRefGoogle Scholar
  46. Sorte CJB, Hofmann GE (2005) Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella with different biogeography ranges. Mar Biol 146:985–993CrossRefGoogle Scholar
  47. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301(5629):65CrossRefGoogle Scholar
  48. Stillman JH, Somero GN (1996) Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (Genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution. J Exp Biol 1999:1845–1855Google Scholar
  49. Tomanek L, Sanford E (2003) Heat-shock protein 70 (Hsp70) as a biochemical stress indicator: an experimental field test in two congeneric intertidal gastropods (genus Tegula). Biol Bull 205:276–284CrossRefGoogle Scholar
  50. 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 202:2925–2936PubMedGoogle Scholar
  51. 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 73:249–256CrossRefGoogle Scholar
  52. Vermeij GJ (1971) Temperature relationships of some tropical Pacific intertidal gastropods. Mar Biol 10(4):308–314CrossRefGoogle Scholar
  53. Williams GA (1993a) Seasonal variation in algal species richness and abundance in the presence of molluscan herbivores on a tropical rocky shore. J Exp Mar Biol Ecol 167:261–275CrossRefGoogle Scholar
  54. Williams GA (1993b) The relationship between herbivorous molluscs and algae on moderately exposed Hong Kong Shores. In: Morton B (ed) The marine biology of the South China Sea: Proceedings of the first international conference on the marine biology of Hong Kong and the South China Sea, Hong Kong 28 October–3 November 1990. Hong Kong University Press, Hong Kong, pp 459–470Google Scholar
  55. Williams GA (1994) The relationship between shade and molluscan grazing in structuring communities on a moderately-exposed tropical rocky shore. J Exp Mar Biol Ecol 178:79–95CrossRefGoogle Scholar
  56. Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103CrossRefGoogle Scholar
  57. Williams GA, De Pirro M, Leung KMY, Morritt D (2005) Physiological responses to heat stress on a tropical shore, the benefits of mushrooming behaviour in the limpet Cellana grata. Mar Ecol Prog Ser 292:213–224CrossRefGoogle Scholar
  58. Williams GA, De Pirro M, Cartwright S, Khangura K, Ng WC, Leung PTY, Morritt D (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. Func Ecol 25:101–110CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.The State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen UniversityXiamenPeople’s Republic of China
  2. 2.The Swire Institute of Marine Science and Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong KongHong Kong SARPeople’s Republic of China

Personalised recommendations