Polar Biology

, Volume 29, Issue 8, pp 688–693

Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance

Original Paper


Understanding thermal limits and the ability of species to cope with changing temperatures is crucial for a cause and effect understanding of climate effects on organisms and ecosystems. Data available for marine species from various phyla and climates led to the hypothesis that a mismatch between oxygen demand and limited capacity of oxygen supply to tissues is the first mechanism to restrict survival at thermal extremes. Here we show that doubling the oxygen content of the ambient seawater from 160 mmHg partial pressure to 350 mmHg raised the upper temperature limits of the Antarctic marine bivalve Laternula elliptica by about 2.5°C. It reduced the accumulation of the anaerobic end product succinate or of total CO2 as a sign of respiratory distress. These findings provide further evidence that oxygen supply does limit thermal tolerance in marine animals. As water temperatures rise animals will face a double problem of progressively reduced oxygen solubility in the water and enhanced costs reflected in increased metabolic rates.


  1. Angel MV (1991) Variations in time and space: Is biogeography relevant to studies of long-time scale change? J Mar Biol Assoc UK 71:191–206CrossRefGoogle Scholar
  2. Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol 279:R1531–R1538Google Scholar
  3. Gille ST (2002) Warming of the Southern Ocean since the 1950s. Science 295:1275–1277CrossRefPubMedGoogle Scholar
  4. Hardewig I, Peck LS, Pörtner HO (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid, Lepidonotothen nudifrons. J Comp Physiol B 169:597–604CrossRefGoogle Scholar
  5. Heise K, Puntarulo S, Nikinmaa M, Abele D, Pörtner HO (2006) Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout (Zoarces viviparus). J Exp Biol 209:353–363CrossRefPubMedGoogle Scholar
  6. Jensen MN (2003) Consensus on ecological impact remains elusive. Science 299:38CrossRefPubMedGoogle Scholar
  7. Lannig G, Bock C, Sartoris FJ, Pörtner HO (2004) Oxygen limitation of thermal tolerance in cod, Gadus morhua L. studied by non-invasive NMR techniques and on-line venous oxygen monitoring. Am J Physiol 287:R902–R910Google Scholar
  8. Mark sFC, Bock C, Pörtner HO (2002) Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and 31P-MRS. Am J Physiol 283:R1254–R1262Google Scholar
  9. Mark FC, Hirse T, Pörtner HO (2005) Thermal sensitivity of cellular energy budgets in Antarctic fish hepatocytes. Pol Biol 28:805–814CrossRefGoogle Scholar
  10. Murawski SA (1993) Climate change and marine fish distributions: forecasting from historical analogy. Trans Am Fish Soc 122:647–658CrossRefGoogle Scholar
  11. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  12. Paul RJ, Lamkemeyer T, Maurer J, Pinkhaus O, Pirow R, Seidl M, Zeis B (2004) Thermal acclimation in the microcrustacean Daphnia: a survey of behavioural, physiological and biochemical mechanisms. J Therm Biol 29:655–662CrossRefGoogle Scholar
  13. Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12:361–371CrossRefGoogle Scholar
  14. Peck LS, Uglow RF (1990) Two methods for the assessment of the oxygen content of small samples of seawater. J Exp Mar Biol Ecol 141:53–62CrossRefGoogle Scholar
  15. Peck LS, Conway LZ (2000) The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalve molluscs. In: Harper E, Crame AJ (eds) Evolutionary biology of the bivalvia. Geological Society of London Special Publication vol 177. Cambridge University Press, Cambridge, pp 441–450Google Scholar
  16. Peck LS, Pörtner HO, Hardewig I (2002) Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula elliptica. Physiol Biochem Zool 75:123–133CrossRefPubMedGoogle Scholar
  17. Peck LS, Webb KE, Bailey D (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630CrossRefGoogle Scholar
  18. Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwiss 88:137–146CrossRefPubMedGoogle Scholar
  19. 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
  20. Pörtner HO (2006) Climate dependent evolution of Antarctic ectotherms: an integrative analysis. Deep Sea Res (in press)Google Scholar
  21. Pörtner HO, Zielinski S (1998) Environmental constraints and the physiology of performance in squids. S Afr J Mar Sci 20:207–221Google Scholar
  22. Pörtner HO, Boutilier RG, Tang Y, Toews DP (1990) Determination of intracellular pH and \( P_{{{\text{CO}}_{{\text{2}}} }} \) after metabolic inhibition by fluoride and nitrilotriacetic acid. Respir Physiol 81:255–274Google Scholar
  23. Pörtner HO, Peck LS, Zielinski S, Conway LZ (1999a) Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature. Pol Biol 22:17–30CrossRefGoogle Scholar
  24. Pörtner HO, Hardewig I, Peck LS (1999b) Mitochondrial function and critical temperature in the Antarctic bivalve Laternula elliptica. Comp Biochem Physiol A 124:179–189CrossRefGoogle Scholar
  25. Pörtner HO, van Dijk PLM, Hardewig I, Sommer A (2000) Levels of metabolic cold adaptation: tradeoffs in eurythermal and stenothermal ectotherms. In: Davison W, Williams CW (eds) Antarctic Ecosystems: models for a wider understanding. Christchurch, Caxton, pp 109–122Google Scholar
  26. Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir Physiol Neurobiol 141:243–260CrossRefPubMedGoogle Scholar
  27. Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. In: Farrell AP, Steffensen, JF (eds) The physiology of polar fishes. Randall DR, Farrell AP (eds) Fish Physiol 22:79–154Google Scholar
  28. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefPubMedGoogle Scholar
  29. Somero GN (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1 (DOI: 10.1186/1742-9994-2-1)Google Scholar
  30. Somero GN, De Vries AL (1967) Temperature tolerance of some Antarctic fishes. Science 156:257–258PubMedCrossRefGoogle Scholar
  31. Urban HJ (1998) Upper temperature tolerance of two Antarctic molluscs (Laternula elliptica and Nacella concinna) from Potter Cove, King George Island, Antarctic Peninsula. Ber Polarforsch 299:230–236Google Scholar
  32. van Dijk PLM, Tesch C, Hardewig I, Pörtner HO (1999) Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic, and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202:3611–3621PubMedGoogle Scholar
  33. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  34. Weibel ER, Taylor CR, Hoppler H (1991) The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc Natl Acad Sci USA 88:10357–10361PubMedCrossRefGoogle Scholar
  35. Yeager DP, Ultsch GR (1989) Physiological regulation and conformation: a BASIC program for the determination of critical points. Physiol Zool 62:888–907Google Scholar
  36. Zakhartsev MV, De Wachter B, Sartoris FJ, Pörtner HO, Blust R (2003) Thermal physiology of the common eelpout (Zoarces viviparus). J Comp Physiol B 173:365–378CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Alfred-Wegener-Institute for Polar and Marine Research, Animal EcophysiologyBremerhavenGermany
  2. 2.NERC British Antarctic Survey, High CrossCambridgeUK

Personalised recommendations