Marine Biology

, Volume 156, Issue 10, pp 1977–1984 | Cite as

Thermal dependency of burrowing in three species within the bivalve genus Laternula: a latitudinal comparison

  • Simon Anthony Morley
  • Koh Siang Tan
  • Robert W. Day
  • Stephanie M. Martin
  • Hans-O. Pörtner
  • Lloyd S. Peck
Original Paper


The upper thermal limits for burrowing and survival were compared with micro-habitat temperature for anomalodesmatan clams: Laternula elliptica (Antarctica, 67°S); Laternula recta, (temperate Australia, 38°S) and Laternula truncata (tropical Singapore, 1°N). Lethal limits (LT50) were higher than burrowing limits (BT50) in L. elliptica (7.5–9.0 and 2.2°C) and L. recta (winter, 32.8–36.8 and 31.1–32.8°C) but the same range for L. truncata (33.0–35.0 and 33.4–34.9°C). L. elliptica and L. truncata had a BT50 0.4 and 2.4–3.9°C, respectively, above their maximum experienced temperature. L. recta, which experience solar heating during midday low tides, had a BT50 0.7–2.4°C below and a range for LT50 that spanned their predicted environmental maximum (33.5°C). L. recta showed no seasonal difference in LT50 or BT50. Our single genus comparisons contrast with macrophysiological studies showing that temperate species cope better with elevated temperatures.


Bivalve Thermal Limit Sediment Temperature Aerobic Scope Burial Time 
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.



This research was funded by NERC core funding to the BAS Bioreach/Bioflame program, the Antarctic Funding Initiative (AFI2/34) and A*Star proposal (SERC project no. 0821010024). We thank the Biodiversity Centre and Sungei Buloh Wetland Reserve (National Parks Board Singapore) and Zoology Department, University of Melbourne for facilitating this project. Antarctic scientific diving was supported by the NERC National Scientific Diving Facility. Pete Rothery provided expert statistical advice. The comments of Pete Convey and two anonymous reviewers improved this manuscript. All experiments comply with the current laws of the countries in which they were conducted.

Supplementary material

227_2009_1228_MOESM1_ESM.docx (206 kb)
Supplementary material 1 (DOCX 206 kb)


  1. Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc Lond B 267:739–745CrossRefGoogle Scholar
  2. Alexander R, Stanton R, Dodd J (1993) Influence of sediment grain size on the burrowing of bivalves: correlation with distribution and stratigraphic persistence of selected neogene clams. Palaios 8:289–303CrossRefGoogle Scholar
  3. Ansell AD, McLachlan A (1980) Upper temperature tolerances of three molluscs from South African Sandy Beaches. J Exp Mar Biol Ecol 48:243–251CrossRefGoogle Scholar
  4. Ansell AD, Barnett PRO, Bodoy A, Massé H (1980a) Upper temperature tolerances of some European molluscs. I Tellina fibula and T. tenuis. Mar Biol 58:33–39CrossRefGoogle Scholar
  5. Ansell AD, Barnett PRO, Bodoy A, Massé H (1980b) Upper temperature tolerances of some European molluscs. II Donax vittatus, D. semistriatus and D. trunculus. Mar Biol 58:41–46CrossRefGoogle Scholar
  6. Ansell AD, Barnett PRO, Bodoy A, Massé H (1981) Upper temperature tolerances of some European molluscs. III Cardium glaucum, C. tuberculatum and C. edule. Mar Biol 65:177–183CrossRefGoogle Scholar
  7. Barnes DKA, Fuentes V, Clarke A, Schloss IR, Wallace MI (2006) Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep-Sea Res PT II 53:853–865CrossRefGoogle Scholar
  8. Calosi P, Bilton DT, Spicer JL (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett 4:99–102PubMedCrossRefGoogle Scholar
  9. Chou R, Lee HB (1997) Commercial fish farming in Singapore. Aquac Res 28:767–776CrossRefGoogle Scholar
  10. Chown SL, Gaston KJ (2008) Macrophysiology for a changing world. Proc Roy Soc B 275:1469–1478CrossRefGoogle Scholar
  11. Chown SL, Gaston KJ, Robinson D (2004) Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Funct Ecol 18:159–167CrossRefGoogle Scholar
  12. Chown SL, Jumbam KR, Sørensen JG, Terblanche JS (2008) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct Ecol. doi: 10.1111/j.1365-2435.2008.01481.x
  13. Clarke A, Crame JA (1992) The Southern Ocean benthic fauna and climate change: a historical perspective. Philos T Roy Soc B 338:299–309CrossRefGoogle Scholar
  14. Clarke A, Gaston KJ (2006) Climate, energy and diversity. Proc Roy Soc B 273:2257–2266CrossRefGoogle Scholar
  15. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  16. Compton TJ, Rijkenberg MJA, Crent J, Piersma T (2007) Thermal tolerance and climate variability: a comparison between bivalves from differing climates. J Exp Mar Biol Ecol 352:200–211CrossRefGoogle Scholar
  17. Davenport J, Wong TM (1992) Effects of temperature and aerial exposure on three tropical oyster species, Crassostrea belcheri, Crassostrea iredaelei and Saccostrea cucullata. J Therm Biol 17:135–139CrossRefGoogle Scholar
  18. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. PNAS 105:6668–6672PubMedCrossRefGoogle Scholar
  19. Finke GR, Navarrete SA, Bozinovic F (2007) Tidal regimes of temperate coasts and their influences on aerial exposure for intertidal organisms. Mar Ecol Prog Ser 343:57–62CrossRefGoogle Scholar
  20. Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in the spider crab, Maja squinado. Am J Physiol 279:R1531–R1538Google Scholar
  21. Gaston KJ (2006) The structure and dynamics of geographic ranges. Oxford Series in Ecology and Evolution. Oxford University Press, OxfordGoogle Scholar
  22. Gaston KJ, Chown CL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500CrossRefGoogle Scholar
  23. Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017PubMedCrossRefGoogle Scholar
  24. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  25. Huey RB, Kingsolver JG (1993) Evolution of resistance to high temperature in ectotherms. Am Nat 142:S21–S46CrossRefGoogle Scholar
  26. McLachlan A, Jaramillo E, Defeo O, Dugan J, de Ruyck A, Coetzee P (1995) Adaptations of bivalves to different beach types. J Exp Mar Biol Ecol 187:147–160CrossRefGoogle Scholar
  27. Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604CrossRefGoogle Scholar
  28. Miyazawa K, Lechowicz MJ (2004) Comparative seedling ecology of eight north American spruce (Picea) species in relation to their geographic ranges. Ann Bot-London 94:635–644CrossRefGoogle Scholar
  29. Morley SA, Peck LS, Tan KS, Martin SM, Pörtner HO (2007) Slowest of the slow: latitudinal insensitivity of burrowing capacity in the bivalve Laternula. Mar Biol 151:1823–1830CrossRefGoogle Scholar
  30. Morley SA, Hirse T, Pörtner HO, Peck LS (2009) Geographic variation in thermal tolerance within Southern Ocean marine ectotherms. Comp Biochem Physiol A. doi: 10.1016/j.cbpa.2009.02.001
  31. Morton B (1976) The structure, mode of operation and variation in form of the shell of the Laternulidae (Bivalvia: Anomalodesmata: Pandoracea). J Mollus Stud 42:261–278Google Scholar
  32. Peck LS (2005) Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature change. Ant Sci 17:497–507CrossRefGoogle Scholar
  33. Peck LS, Conway LZ (2000) The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In: Harper E, Crame AJ (eds) Evolutionary Biology of the Bivalvia. Geology Society of London Special Publication 177. Cambridge University Press, Cambridge, pp 441–450Google Scholar
  34. Peck LS, Pörtner HO, Hardewig I (2002) Metabolic demand, oxygen supply and critical temperatures in the Antarctic bivalve Laternula elliptica. Physiol Biochem Zool 75:123–133PubMedCrossRefGoogle Scholar
  35. Peck LS, Webb KE, Bailey DM (2004a) Extreme sensitivity of biological function to temperature in Antarctic species. Funct Ecol 18:625–630CrossRefGoogle Scholar
  36. Peck LS, Ansell AD, Webb KE, Hepburn L, Burrows MT (2004b) Movements and burrowing activity in the Antarctic bivalve molluscs Laternula elliptica and Yoldia eightsi. Polar Biol 27:267–357CrossRefGoogle Scholar
  37. Peck LS, Convey P, Barnes DKA (2006) Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol Rev 81:75–109PubMedCrossRefGoogle Scholar
  38. Peck LS, Morley SA, Pörtner HO, Clark MS (2007) Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica. Oecologia 154:479–484PubMedCrossRefGoogle Scholar
  39. Peck LS, Clark MS, Morley SA, Massey A, Rossetti H (2009) Animal temperature limits and ecological relevance: effects of size, activity and rates of change. Funct Ecol. doi: 10.1111/j.1365-2435.2008.01537.x
  40. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915PubMedCrossRefGoogle Scholar
  41. 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 A 132:739–761Google Scholar
  42. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97PubMedCrossRefGoogle Scholar
  43. Prosser CL (1973) Comparative animal physiology. Saunders, PhiladelphiaGoogle Scholar
  44. Sabatés A, Martín P, Lloret J, Raya VA (2006) Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Glob Change Biol 12:2209–2219CrossRefGoogle Scholar
  45. Sagarin RD, Somero GN (2006) Complex patterns of heat-shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytlius californianus and snail Nucella ostrina. J Biogeogr 33:622–630CrossRefGoogle Scholar
  46. Sagarin RD, Barry JP, Gilman SE, Charles HB (1999) Climate-related change in an intertidal community over short and long time scales. Ecol Monogr 69:465–490CrossRefGoogle Scholar
  47. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits and costs of living. Integr Comp Biol 42:780–789CrossRefGoogle Scholar
  48. Somero GN, DeVries AL (1967) Temperature tolerance of some Antarctic fishes. Science 156:257–258PubMedCrossRefGoogle Scholar
  49. Sommer A, Pörtner HO (1999) Exposure of Arenicola marina (L.) to extreme temperatures: adaptive flexibility of a boreal and a subpolar population. Mar Ecol Prog Ser 181:215–226CrossRefGoogle Scholar
  50. Sommer A, Klein B, Pörtner HO (1997) Temperature induced anaerobiosis in two populations of the polychaete worm Arenicola marina. J Comp Physiol B 167B:25–35CrossRefGoogle Scholar
  51. Southward AJ, Hawkins SJ, Burrows MT (1995) Seventy years’ observation of the changes in distribution and abundance of zooplankton and intertidal organisms in the western English channel in relation to rising sea temperature. J Therm Biol 20:127–155CrossRefGoogle Scholar
  52. Stevens GC (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am Nat 133:240–256CrossRefGoogle Scholar
  53. Stillman JH (2002) Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus Petrolisthes. Integr Comp Biol 42:790–796CrossRefGoogle Scholar
  54. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65PubMedCrossRefGoogle Scholar
  55. Terblanche JS, Deere JA, Clusella-Trullas S, Janion C, Chown SL (2007) Critical thermal limits depend on methodological context. Proc Roy Soc B 274:2935–2942CrossRefGoogle Scholar
  56. Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297PubMedCrossRefGoogle Scholar
  57. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siquelra M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148PubMedCrossRefGoogle Scholar
  58. 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. J Exp Biol 208:3133–3143PubMedCrossRefGoogle Scholar
  59. Visser ME (2008) Keeping up with a warming world: assessing the rate of adaptation to climate change. Proc Roy Soc B 275:649–659CrossRefGoogle Scholar
  60. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological response to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  61. Weibel ER, Taylor CR, Bolis L (1998) Principles of animal design: the optimization and symmorphosis debate. Cambridge University Press, CambridgeGoogle Scholar
  62. Widdows J (1976) Physiological adaptation of Mytlius edulis to cyclic temperatures. J Comp Physiol B 105:115–128CrossRefGoogle Scholar
  63. Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524CrossRefGoogle Scholar
  64. Yamahira K, Conover DO (2002) Intra-vs. interspecific latitudinal variation in growth: adaptation to temperature or seasonality? Ecology 83:1252–1262Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Simon Anthony Morley
    • 1
  • Koh Siang Tan
    • 2
  • Robert W. Day
    • 3
  • Stephanie M. Martin
    • 4
  • Hans-O. Pörtner
    • 5
  • Lloyd S. Peck
    • 1
  1. 1.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK
  2. 2.Tropical Marine Science InstituteNational University of SingaporeSingaporeSingapore
  3. 3.Zoology DepartmentUniversity of MelbourneParkvilleAustralia
  4. 4.CambsUK
  5. 5.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany

Personalised recommendations