Journal of Oceanography

, Volume 60, Issue 4, pp 731–741

Effects of CO2 on Marine Fish: Larvae and Adults

  • Atsushi Ishimatsu
  • Takashi Kikkawa
  • Masahiro Hayashi
  • Kyoung-Seon Lee
  • Jun Kita
Article

Abstract

CO2-enriched seawater was far more toxic to eggs and larvae of a marine fish, silver seabream, Pagrus major, than HCl-acidified seawater when tested at the same seawater pH. Data on the effects of acidified seawater can therefore not be used to estimate the toxicity of CO2, as has been done in earlier studies. Ontogenetic changes in CO2 tolerance of two marine bony fishes (Pag. major and Japanese sillago, Sillago japonica) showed a similar, characteristic pattern: the cleavage and juvenile stages were most susceptible, whereas the preflexion and flexion stages were much more tolerant to CO2. Adult Japanese amberjack, Seriola quinqueradiata, and bastard halibut, Paralichthys olivaceus, died within 8 and 48 h, respectively, during exposure to seawater equilibrated with 5% CO2. Only 20% of a cartilaginous fish, starspotted smooth-hound, Mustelus manazo, died at 7% CO2 within 72 h. Arterial pH initially decreased but completely recovered within 1-24 h for Ser. quinqueradiata and Par. olivaceus at 1 and 3% CO2, but the recovery was slower and complete only at 1% for M. manazo. During exposure to 5% CO2, Par. olivaceus died after arterial pH had been completely restored. Exposure to 5% CO2 rapidly depressed the cardiac output of Ser. quinqueradiata, while 1% CO2 had no effect. Both levels of ambient CO2 had no effect on blood O2 levels. We tentatively conclude that cardiac failure is important in the mechanisms by which CO2 kills fish. High CO2 levels near injection points during CO2 ocean sequestration are likely to have acute deleterious effects on both larvae and adults of marine fishes.

Physiological effects of CO2 CO2 mortality marine fish developmental stage acid-base regulation blood circulation 

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References

  1. Auerbach, D. I., J. A. Caufield, E. E. Adams and H. J. Herzog (1997): Impacts of ocean CO2 disposal on marine life: I. A toxicological assessment integrating constant-concentration laboratory assay data with variable-concentration field exposure. Environ. Model. Assess., 2, 333–343.CrossRefGoogle Scholar
  2. Bernier, N. J. and D. J. Randall (1998): Carbon dioxide anaes-thesia in rainbow trout: effects of hypercapnic level and stress on induction and recovery from anaesthetic treatment. J. Fish Biol., 52, 621–637.Google Scholar
  3. Burleson, M. L. and N. J. Smatresk (2000): Branchial chemoreceptors mediate ventilatory responses to hypercap-nic acidosis in channel catfish. Comp. Biochem. Physiol., 125A, 403–414.CrossRefGoogle Scholar
  4. Claiborne, J. B. and D. H. Evans (1992): Acid-base balance and ion transfers in the spiny dogfish (Squalus acanthias) during hypercapnia: A role for ammonia excretion. J. Exp. Zool., 261, 9–17.CrossRefGoogle Scholar
  5. Claiborne, J. B. and N. Heisler (1986): Acid-base regulation and ion transfers in the carp (Cyprinus carpio): pH com-pensation during graded long-and short-term environmental hypercapnia, and the effect of bicarbonate infusion. J. Exp. Biol., 126, 41–61.Google Scholar
  6. Claiborne, J. B., S. L. Edwards and A. I. Morrison-Shetlar (2002): Acid-base regulation in fishes: cellular and molecu-lar mechanisms. J. Exp. Zool., 293, 302–319.CrossRefGoogle Scholar
  7. Crocker, C. E., A. P. Farrell, A. K. Gamperl and J. J. Cech, Jr. (2000): Cardiorespiratory responses of white sturgeon to environmental hypercapnia. Am. J. Physiol., 279, R617–R628.Google Scholar
  8. Cross, C. E., B. S. Packer, J. M. Linta, H. V. Murdaugh, Jr. and E. D. Robin (1969): H+ buffering and excretion in response to acute hypercapnia in the dogfish Squalus acanthias. Am. J. Physiol., 216, 440–452.Google Scholar
  9. Cruz-Neto, A. P. and J. F. Steffensen (1997): The effects of acute hypoxia and hypercapnia on oxygen consumption of the freshwater European eel. J. Fish Biol., 50, 759–769.CrossRefGoogle Scholar
  10. Dejours, P. (1988): Respiration in Water and Air: Adaptations-Regulation-Evolution. Elsevier, New York, 179 pp.Google Scholar
  11. Farrell, A. P. and D. R. Jones (1992): The heart. p. 1–73. In Fish Physiology Vol. XIIA, ed. by W. S. Hoar, D. J. Randall and A. P. Farrell, Academic Press, San Diego.Google Scholar
  12. Gesser, H. and O. Poupa (1983): Acidosis and cardiac muscle contractility: comparative aspects. Comp. Biochem. Physiol., 76A, 559–566.CrossRefGoogle Scholar
  13. Goss, G. G., S. F. Perry and P. Laurent (1995): Ultrastructural and morphometric studies on ion and acid-base transport processes in freshwater fish. p. 257–284. In Fish Physiol-ogy Vol. 14: Cellular and Molecular Approaches to Fish Ionic Regulation, ed. by C. M. Wood and T. J. Shuttleworth, Academic Press, San Diego.CrossRefGoogle Scholar
  14. Graham, M. S., J. D. Turner and C. M. Wood (1990): Control of ventilation in the hypercapnic skate Raja ocellata: I. Blood and extradural fluid. Respir. Physiol., 80, 259–277.CrossRefGoogle Scholar
  15. Grøttum, J. A. and T. Sigholt (1996): Acute toxicity of carbon dioxide on European seabass (Dicentrarchus labrax): Mor-tality and effects on plasma ions. Comp. Biochem. Physiol., 115A, 323–327.CrossRefGoogle Scholar
  16. Hayashi, M., J. Kita and A. Ishimatsu (2004): Acid-base re-sponses to lethal aquatic hypercapnia in three marine fish. Mar. Biol., 144, 153–160.CrossRefGoogle Scholar
  17. Heisler, N. (1986): Acid-base regulation in fishes. p. 309–356. In Acid-Base Regulation in Animals, ed. by N. Heisler, Elsevier, Amsterdam.Google Scholar
  18. Heisler, N. (1993): Acid-base regulation. p. 343–378. In The Physiology of Fishes, ed. by D. H. Evans, CRC Press, Boca Raton.Google Scholar
  19. Ishimatsu, A. and J. Kita (1999): Effects of environmental hy-percapnia on fish. Japan. J. Icthyol., 46, 1–13.Google Scholar
  20. Iwama, G. K. and N. Heisler (1991): Effect of environmental water salinity on acid-base regulation during environmen-tal hypercapnia in the rainbow trout (Oncorhynchus mykiss). J. Exp. Biol., 158, 1–18.Google Scholar
  21. Kaneko, T., S. Hasegawa, Y. Takagi, M. Tagawa and T. Hirano (1995): Hypoosmoregulatory ability of eyed-stage embryos of chum salmon. Mar. Biol., 122, 165–170.CrossRefGoogle Scholar
  22. Kaneko, T., S. Hasegawa, K. Uchida, T. Ogasawara, A. Oyagi and T. Hirano (1999): Acid tolerance of Japanese dace (a cyprinid teleost) in lake Osorezan, a remarkable acid lake. Zool. Sci., 16, 871–877.CrossRefGoogle Scholar
  23. Katoh, F., A. Shimizu, K. Uchida and T. Kaneko (2000): Shift of chloride cell distribution during early life stages in seawater-adapted killifish, Fundulus heteroclitus. Zool. Sci., 17, 11–18.CrossRefGoogle Scholar
  24. Kikkawa, T., A. Ishimatsu and J. Kita (2003): Acute CO2 toler-ance during the early developmental stages of four marine teleosts. Env. Toxicol., 18, 375–382.CrossRefGoogle Scholar
  25. Kikkawa, T., J. Kita and A. Ishimatsu (2004): Comparison of the lethal effect of CO2 and acidification on red sea bream (Pagrus major) during the early developmental stages. Mar. Pol. Bull., 48, 108–110.CrossRefGoogle Scholar
  26. Larsen, B. K., H.-O. Pörtner and J. B. Jensen (1997): Extra-and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated expo-sures to hypercapnia and copper. Mar. Biol., 128, 337–346.CrossRefGoogle Scholar
  27. Lee, K. S., J. Kita and A. Ishimatsu (2003): Effects of lethal levels of environmental hypercapnia on cardiovascular and blood-gas status in yellowtail, Seriola quinqueradiata. Zool. Sci., 20, 417–422.CrossRefGoogle Scholar
  28. Lerman, M. (1986): Marine Biology. The Benjamin/Cummings Publishing Company, California, 534 pp.Google Scholar
  29. Max, B. (1991): This and that: the neurotoxicity of carbon di-oxide. Trends Pharmacol. Sci., 12, 408–411.CrossRefGoogle Scholar
  30. McKendry, J. E., W. K. Milsom and S. F. Perry (2001): Branchial CO2 receptors and cardiorespiratory adjustments during hypercarbia in Pacific spiny dogfish (Squalus acanthias). J. Exp. Biol., 204, 1519–1527.Google Scholar
  31. McKenzie, D. J., E. W. Taylor, A. Z. Dalla Valle and J. F. Steffensen (2002): Tolerance of acute hypercapnic acidosis by the European eel (Anguilla anguilla). J. Comp. Physiol., 172B, 339–346.CrossRefGoogle Scholar
  32. McKim, J. M. (1977): Evaluation of tests with early life stages of fish for predicting long-term toxicity. J. Fish. Res. Board Can., 34, 1148–1154.CrossRefGoogle Scholar
  33. Mehrbach, C., C. H. Culberson, J. H. Hawley and J. E. Pytkowwicz (1973): Measurement of the apparent disso-ciation constants of carbonic acid in seawater at atmospheric pressure. Limonol. Oceanogr., 18, 897–907.CrossRefGoogle Scholar
  34. Oikawa, S., M. Hirata, J. Kita and Y. Itazawa (1999): Ontog-eny of respiratory area of a marine teleost, porgy, Pagrus major. Ichthyol. Res., 46, 233–244.CrossRefGoogle Scholar
  35. Oozeki, Y., P.-P. Hwang and R. Hirano (1992): Larval develop-ment of the Japanese whiting, Sillago japonica. Japan. J. Ichthyol., 39, 59–669.Google Scholar
  36. Perry, S. F. and K. M. Gilmour (2002): Sensing and transfer of respiratory gases at the fish gill. J. Exp. Zool., 293, 249–263.CrossRefGoogle Scholar
  37. Perry, S. F., R. Fritsche, T. M. Hoagland, D. W. Duff and K. R. Olson (1999): The control of blood pressure during exter-nal hypercapnia in the rainbow trout (Oncorhynchus mykiss). J. Exp. Biol., 202, 2177–2190.Google Scholar
  38. Pörtner, H.-O., M. Langenbuch and A. Reipschläger (2004): Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. J. Oceanogr., 60, this issue, 705–718.CrossRefGoogle Scholar
  39. Randall, D. J., N. Heisler and F. Drees (1976): Ventilatory re-sponses to hypercapnia in the larger spotted dogfish Scyliorhinus stellaris. Am. J. Physiol., 230, 590–594.Google Scholar
  40. Roos, A. and W. F. Boron (1981): Intracellular pH. Physiol. Rev., 61, 296–434.Google Scholar
  41. Sasai, S., T. Kaneko and K. Tsukamoto (1998): Extrabranchial chloride cells in early life stages of Japanese eel, Anguilla japonica. Ichthyol. Res., 45, 95–98.CrossRefGoogle Scholar
  42. Sato, T. and K. Sato (2002): Numerical prediction of the dilu-tion process and its biological impacts in CO2 ocean se-questration. Mar. Sci. Technol., 6, 169–180.CrossRefGoogle Scholar
  43. Shiraishi, K., T. Kaneko, S. Hasegawa and T. Hirano (1997): Development of multicellular complexes of chloride cells in the yolk-sac membrane of tilapia (Oreochromis mossambicus) embryos and larvae in seawater. Cell Tiss. Res., 288, 583–590.CrossRefGoogle Scholar
  44. Takeda, T. and Y. Itazawa (1983): Possibility of applying.Effects of CO2 on Marine Fish 741 anesthesia by carbon dioxide in the transportation of live fish. Nippon Suisan Gakkaishi, 49, 725–731.CrossRefGoogle Scholar
  45. Toews, D. P., G. F. Holeton and N. Heisler (1983): Regulation of the acid-base status during environmental hypercapnia in the marine teleost fish Conger conger. J. Exp. Biol., 107, 9–20.Google Scholar
  46. Vandenberg, J. I., J. C. Metcalfe and A. A. Grace (1994): Intra-cellular pH recovery during respiratory acidosis in perfused hearts. Am. J. Physiol., 266, C489–C497.Google Scholar
  47. Weiss, R. F. (1974): Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Mar. Chem., 2, 203–215.CrossRefGoogle Scholar
  48. Weitzman, S. H. (1997): Systematics of deep-sea fishes. p. 43–78. In Fish Physiology, Vol. XVI. Deep-Sea Fishes, ed. By D. J. Randall and A. P. Farrell, Academic Press, San Diego.CrossRefGoogle Scholar
  49. Yoshikawa, H., F. Kawai and M. Kanamori (1994): The rela-tionship between the EEG and brain pH in carp, Cyprinus carpio, subjected to environmental hypercapnia at an anesthetic level. Comp. Biochem. Physiol., 107A, 307–312.CrossRefGoogle Scholar
  50. Zadunaisky, J. A. (1984): The chloride cell: The active trans-port of chloride and the paracellular pathways. p. 130–176. In Fish Physiology, Vol. 10B, ed. by W. S. Hoar and D. J. Randall, Academic Press, Orlando.Google Scholar

Copyright information

© The Oceanographic Society of Japan 2004

Authors and Affiliations

  • Atsushi Ishimatsu
    • 1
  • Takashi Kikkawa
    • 1
    • 2
  • Masahiro Hayashi
    • 1
  • Kyoung-Seon Lee
    • 1
  • Jun Kita
    • 3
  1. 1.Marine Research InstituteNagasaki UniversityNagasakiJapan
  2. 2.Central LaboratoryMarine Ecology Research InstituteChibaJapan
  3. 3.Research Institute of Innovative Technology for the Earth (RITE)Kizu-cho, KyotoJapan

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