Marine Biology

, Volume 111, Issue 3, pp 343–351 | Cite as

Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis

  • A. de Zwaan
  • P. Cortesi
  • G. van den Thillart
  • J. Roos
  • K. B. Storey


The metabolic responses to a series of low oxygen tensions were compared for two species of Mediterranaean bivalves,Mytilus galloprovincialis andScapharca inaequivalvis. Whereas both species have well-developed and similar tolerances of anoxia, the metabolic responses ofS. inaequivalvis to low oxygen tensions indicate a substantially greater tolerance of hypoxia. Compared withM. galloprovincialis, the responses ofS. inaequivalvis included the ability to maintain a constant oxygen consumption down to a much lower pO2 value (ca. 1.7 vs 3.4 ppm), and a lower critical pO2 for the recruitment of fermentative pathways of ATP production (ca. 1 vs 3 ppm). Furthermore, a graded increase in the output of anaerobic products (succinate, alanine) occured at oxygen tensions below 3 ppm inM. galloprovincialis and reached a maximum at 1.6 ppm whereas inS. inaequivalvis the net accumulation of anaerobic products at the lowest oxygen tension tested (0.5 ppm) was still substantially less than the level of production output in complete anoxia. This suggests that fermentative pathways are maximally activated at all oxygen tensions below 1.6 ppm inM. galloprovincialis whereas rates of anaerobic pathways are still less than maximum at 0.5 ppm inS. inaequivalvis. These results indicate that in situations of declining oxygen tensions, such as occur due to eutrophication,M. galloprovincialis would not only begin to experience metabolic stress at higher oxygen tensions thanS. inaequivalvis but would experience greater stress at any given pO2. Such differences in hypoxia tolerances may explain the success of the recently introducedS. inaequivalvis in out-competing the nativeM. galloprovincialis in the Adriatic Sea.


Succinate Bivalve Oxygen Tension Metabolic Response Metabolic Stress 
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.


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Literature cited

  1. Bergmeyer, H. U. (1984). Methods of enzymatic analysis. 3rd edn. Verlag Chemie, Weinheim, GermanyGoogle Scholar
  2. Brooks, S. P. J., Zwaan, A. de, Thillart, G. van den, Cattani, O., Cortesi, P., Storey, K. B. (1991). Differential survival ofVenus gallina andScapharca inaequivalvis during anoxic stress: covalent modification of phosphofructokinase and glycogen phosphorylase during anoxia. J. comp. Physiol. 161: 207–212Google Scholar
  3. Chiancone, E., Boffi, A., Verzili, B., Ascoli, F. (1985). Proprietá delle emoglobine del molluscoScapharca inaequivalvis in rapporto con le condizioni ecologiche del mare Adriatico. Atti 1° Simp. Biochim. mar., Editoriale Grasso, Bologna, p. 13–20Google Scholar
  4. Cortesi, P., Cattani, O., Vitali, G., Carpene, E., Zwaan, A. de, Thillart, G. van den, Roos, J., Lieshout, G. van, and Weber, R. E. (1991). Physiological and biochemical responses of the bivalveS. inaequivalvis to hypoxia and cadmium exposure: erythrocytes versus other tissues. In: Vollenweider, R. A. (ed.) The science of the total environment. Elsevier, Amsterdam (in press)Google Scholar
  5. Ghisotti, F., Rinaldi, E. (1976). Osservazioni sulla popolazione diScapharca insediatasi in questi ultimi anni su un tratto di littorale romagnolo. Conchiglie (Un. malac. ital., Milano) 12: 183–185Google Scholar
  6. Hamilton, M. A., Russo, R. C., Thurston, R. V. (1977). Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Envir. Sci. Technol. 11: 714–719Google Scholar
  7. Ho, M.-S., Zubkoff, P. L. (1982). Anaerobic metabolism of the ribbed mussel,Geukensia demissa. Comp. Biochem. Physiol. 73B: 931–936Google Scholar
  8. Isani, G. (1987) Metabolismo anaerobico in mulluschi bivalvi dell'Adriatico. Ph. D. Thesis, Universita degli studi di Bologna, Bologna, ItalyGoogle Scholar
  9. Isani, G., Cattani, E., Carpene, S., Tacconi, S., Cortesi, P. (1989). Energy metabolism during anaerobiosis and recovery in the posterior adductor muscle of the bivalveScapharca inaequivalvis (Bruguiere). Comp. Biochem. Physiol. 93B: 193–200Google Scholar
  10. Kluytmans, J. H., Graft, M. van, Janus, J., Pieters, H. (1978). Production and excretion of volatile fatty acids in the sea musselMytilus edulis L. J. comp. Physiol. 123: 163–167Google Scholar
  11. Mangum, C. P., Mauro, N. A. (1985). Metabolism of invertebrate red cells: a vacuum in our knowledge. In: Gilles, R. (ed.) Circulation, respiration and metabolism. Springer-Verlag, Heidelberg, p. 280–287Google Scholar
  12. Marchetti, R., Provini, A., Crosa, G. (1989). Nutrient load carried by the river Po into the Adriatic Sea, 1968–1987. Mar. Pollut. Bull. 20: 168–172Google Scholar
  13. Michaelidis, B., Storey, K. B. (1990). Phosphofructokinase from the anterior byssus retractor muscle ofMytilus edulis: modification of the enzyme in anoxia and by endogenous protein kinases. Int. J. Biochem. 22: 759–765Google Scholar
  14. Michaelis, B, Storey, K. B. (1991). Evidence for phosphorylation/dephosphorylation control of phosphofructokinase from organs of the anoxia-tolerant sea musselMytilus edulis. J. exp. Zool. 257: 1–9Google Scholar
  15. Schöttler, U., Grieshaber, M. (1988). Adaptation of the polychaete wormScoloplos armiger. Mar. Biol. 99: 215–222Google Scholar
  16. Schöttler, U., Wienhausen, G., Zebe, E. (1983). The mode of energy production in the lugwormArenicola marina at different oxygen concentrations. J. comp. Physiol. 149B: 547–555Google Scholar
  17. Storey, K. B. (1984). Phosphofructokinase from foot muscle of the whelkBusycotypus canaliculatum: evidence for covalent modification of the enzyme during anaerobiosis. Archs. Biochem. Biophys. 235: 665–672Google Scholar
  18. Thillart, G. van den, Verbeek, R. (1982). Substrates for anaerobic CO2 production by the goldfishCarassius auratus L.: decarboxylation of14C-labelled metabolites. J. comp. Physiol. 149: 75–81Google Scholar
  19. Vooys, C. G. N. de, Zwaan, A. de, Roos, J., Carpené, E., Cattani, O. (1991). Anaerobic metabolism of erythrocytes of the arcid clamS. inaequivalvis (Bruguiere): effects of cadmium. Comp. Biochem. Physiol. 98B: 169–175Google Scholar
  20. Weber, R. E. (1990). Effects of mercury on the functional properties of haemoglobins from the bivalve molluscScapharca inaequivalvis. J. exp. mar. Biol. Ecol. 144: 39–48Google Scholar
  21. Weber, R. E., Lykke-Madsen, M., Bang, A., Zwaan, A. de, Cortesi, P. (1990). Effects of cadmimum on anoxic survival, hematology, erythrocytic volume regulation and hemoglobin-oxygen affinity in the bivalveScapharca inaequivalvis. J. exp. mar. Biol. Ecol. 144: 29–38Google Scholar
  22. Whitwam, R. E., Storey, K. B. (1991). Organ-specific regulation of phosphofructokinase during facultative anaerobiosis in the marine whelkBusycotypus canaliculatum. Can. J. Zool. 69: 70–75Google Scholar
  23. Zwaan, A. de, Bont, A. M. T. de, Verhoeven, A. (1982). Anaerobic energy metabolism in isolated adductor muscle of the sea musselMytilus edulis L. J. comp. Physiol. 149: 137–143Google Scholar
  24. Zwaan, A. de, Bont, A. M. T. de, Zurburg, W., Bayne, B., Livingstone, D. (1983). On the role of strombine formation in the adductor muscle of the sessile bivalveMytilus edulis. J. comp. Physiol. 149: 557–563Google Scholar
  25. Zwaan, A. de, Cortesi, P., Thillart, G. van den, Brooks, S., Storey, K. B., Roos, J., Lieshout, G. van, Cattani, O., Vitali, G. (1991). Energy metabolism of bivalves at reduced oxygen tensions. In: Vollenweider, R. A. (ed.) The science of the total environment. Elsevier, Amsterdam (in press)Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • A. de Zwaan
    • 1
  • P. Cortesi
    • 2
  • G. van den Thillart
    • 3
  • J. Roos
    • 1
  • K. B. Storey
    • 4
  1. 1.Delta Institute for Hydrobiological ResearchYersekeThe Netherlands
  2. 2.Department of BiochemistryUniversity of BolognaBolognaItaly
  3. 3.Department of Animal Physiology, Gorlaeus LaboratoriesUniversity of LeidenLeidenThe Netherlands
  4. 4.Institute of Biochemistry and Department of BiologyCarleton UniversityOttawaCanada

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