Fish Physiology and Biochemistry

, Volume 31, Issue 1, pp 65–72 | Cite as

Effect of Acute Hypoxia in Trout (Oncorhynchus mykiss) on Immature Erythrocyte Release and Production of Oxidative Radicals



This paper evaluates the response of trout exposed to acute hypoxia between 8.7 mgO2/l (controls) and 1.4 mgO2/l. Temperature, pH, NH4, oxygen consumption rate and spleen-somatic index (SSI) were evaluated. Blood cell counts, oxidative radicals (ORs) production and immature erythrocytes were assessed to evaluate their relationship with the degree of hypoxia. Acute hypoxia induced a decrease in water pH (p < 0.05), oxygen consumption rate (60% less), SSI (55% less) and a significant increase of water ammonium concentration (p < 0.05). Haematocrit increased significantly starting at 4.8 mgO2/l, as well as an increase in the total number of leukocytes (up to 50% in some fish). Starting at 2 mgO2/l, swelling of erythrocytes was induced and a decrease in the potential production of ORs, showing a negative correlation to immature erythrocyte numbers. These results suggest that lower than normal oxygen concentrations may jeopardize ORs production and hence non-specific defence mechanisms in trout. High percentages of immature erythrocytes can be used as a simple and inexpensive indicator of both hypoxic events and impairment of ORs production in the absence of bleeding, haemolysis, anti-anaemia treatments and/or increased temperature.


erythrocytes haematology hypoxia Oncorhynchus mykiss oxidative radicals 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen, D.B., Maguire, J.J., Mahdavian, M., Wicke, C., Marcocci, L., Scheuenstuhl, H., Chang, M., Le, A.X., Hopf, H.W., Hunt, T.K. 1997Wound hypoxia and acidosis limit neutrophil bacterial killing mechanismsArch. Surg.132991996PubMedGoogle Scholar
  2. Anderson, R.S., Brubacher, L.L., Calvo, L.R., Unger, M.A., Burreson, E.M. 1998Effects of tributyl and hypoxia on the progression of Perkinsus marinum infections and host defence mechanisms in oyster, Crassostrea virginica (Gmelin)J. Fish Dis.21371379CrossRefGoogle Scholar
  3. Anderson, D.P., Siwicki, A.K. 1993Measuring the effects of contaminants on fish by hematolgucal and serological methodsStolen, J.Anderson, D.P.Selikoff, J.Twerdok, L.Kaattari,  eds. Modulators of Fish Immune ResponseSOS PublicationsFair Haeven, NJ97116Google Scholar
  4. Babior, B.M. 1999NADPH Oxidase: An UpdateBlood9314641476PubMedGoogle Scholar
  5. Beck, W. 1981. Hematopoyesis an Introduction to the anemias in Haematology Edited by William S. Beck, 3rd Edition.Google Scholar
  6. Blanco, C.C. 1995. La trucha, cría industrial. 2da Edición. Ediciones Mundi-Prensa. Madrid.Google Scholar
  7. Boleza, K.A., Burnett, L.E., Burnett, K.G. 2001Hypercapnic hypoxia compromises bactericidal activity of fish anterior kidney cells against opportunistic environmental pathogensFish Shellfish Immunol.11593610CrossRefPubMedGoogle Scholar
  8. Boyd, J.N., Burnett, L.E. 1999Reactive oxygen intermediate production by oyster haemocytes exposed to hypoxiaJ. Exp. Biol.20231353143PubMedGoogle Scholar
  9. Burleson, M.L., Wilhelm, B.D., Smatresk, N.J. 2001The influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bassJ. Fish Biol.5913361349Google Scholar
  10. Burnett, L.E. 1997The challenges of living in hypoxic and hypercapnic aquatic environmentsAm. Zool.37633640Google Scholar
  11. Campbell, T.W., Murru, F. 1990An introduction to fish haematologyCompendium Continuing Edu. Vet. Sci.12525533Google Scholar
  12. Chung, S., Secombes, C.J. 1988Analysis of events occurring within teleost macrophages during the respiratory burstComp. Biochem. Physiol.89B539544Google Scholar
  13. Groot, H., Littauer, A. 1989Hypoxia. Reactive oxygen and cell injuryFree. Radic. Biol. Med.6541551PubMedGoogle Scholar
  14. Dröge, W. 2002Free radicals in the physiological control of cell functionPhysiol Rev.824895Google Scholar
  15. Edwards, S.W., Hallett, M.B., Campbell, A.K. 1984Oxygen radicals production may be limited by oxygen concentrationBiochem. J.217851854PubMedGoogle Scholar
  16. Feldman, G.M., Dannenberg, A.M., Seed, J.L. 1990Physiologic oxygen tensions limit oxidant-mediated killing of schistosome eggs by inflammatory cells and isolated granulomasJ. Leukoc. Biol.47344354PubMedGoogle Scholar
  17. Fukuda, Y., Maita, M., Satoh, K., Okamoto, N. 1997Influence of dissolved oxygen concentration on the mortality of Yellowtail experimentally infected with Enterococcus seriolicidaFish Pathol.32129130Google Scholar
  18. Gabig, T.G., Babior, B.M. 1981The killing of pathogens by phagocytesAnnu. Rev. Med.32313326CrossRefPubMedGoogle Scholar
  19. Hackam, D.J., Grinstein, S., Nathens, A., Watson, W.G., Marshall, J.C., Rotstein, O.D. 1996Exudative neutrophils show impaired pH regulation compared with circulating neutrophilsArch Surg.13112961301PubMedGoogle Scholar
  20. Kiceniuk, J.W., Colbourne, E. 1997Relating oxygen levels in the Newfoundland offshore waters to the physiology of Atlantic cod (Gadus morhua)Can. J. Fish Aquat. Sci.548187CrossRefGoogle Scholar
  21. Kita, J., Itazawa, Y. 1989Release of erythrocytes from the spleen during exercise and splenic constriction by adrenaline infusion in the rainbow troutJpn. J. Ichthyol.364852Google Scholar
  22. Kita, J., Itazawa, Y. 1990Effects of adrenaline on the blood flow through the spleen of rainbow trout (Salmo gairdneri)Comp. Biochem. Physiol.95A591595Google Scholar
  23. Klontz, G.W. 1994Fish hematologyStolen, J.D.Rowley, A.F.Zelikoff, J.T.Kaatari, S.L.Smith, S.A. eds. Techniques in Fish ImmunologySOS PublicationsFair Haven, USAGoogle Scholar
  24. Leklin, T., Nikinmaa, M. 1999Seasonal and temperature effects on the adrenergic responses on the Artic charr (Salvelinus alpinus) erythrocytesJ. Exp. Biol.20222332238Google Scholar
  25. Leklin, T., Tuominen, A., Nikinmaa, M. 2000The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytesJ. Exp. Biol.20330253031Google Scholar
  26. Moullac, G.C., Soyez, C., Ansquer, D., Saulnier, C., Christophe, D., Levy, P. 1999Effect of hypoxic stress on the immune response and the resistance to Vibriosis of the shrimp Penaeus stylirostrisFish Shellfish Immunol.8621629Google Scholar
  27. López-Barneo, J., Pardal, R., Ortega-Sáenz, P. 2001Cellular mechanisms Of Oxygen SensingAnnu. Rev. Physiol.6325987PubMedGoogle Scholar
  28. Miale, J.B. 1982Laboratory Medicine. Haematology6The C. V. Mosley CompanyUSA1084Google Scholar
  29. Nikinmaa, M. 1997Oxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transportJ. Exp. Biol.200369380PubMedGoogle Scholar
  30. Nikinmaa, M., Soivio, A. 1982Blood oxygen transport of hypoxic Salmo gairdneriJ. Exp. Zool.219173178CrossRefPubMedGoogle Scholar
  31. Nixon, W.W. 1995Coastal marine eutrophication: a definition, social causes, and future concernsOphelia41199219Google Scholar
  32. Paerl, H.W., Pinckney, J.L., Fear, J.M., Peierls, B.L. 1999Ecosystem responses to internal and watershed organic matter loading-consequences for hypoxia in the eutrophying Neuse River estuary, NCMar. Ecol. Prog. Ser.1661725Google Scholar
  33. Perry, S.F., Reid, S.D. 1992Relationship between blood O2 content and catecholamines levels during hypoxia in rainbow trout and American eelAm. J. Physiol. Regul. Integr. Comp. Physiol.263240249Google Scholar
  34. Perry, S.F., Reid, S.G., Wankiewicz, E., Iyer, V., Gilmour, K.M. 1996Physiological responses of rainbow trout (Oncorhynchus mykiss) to prolonged exposure to softwaterPhysiol. Zool.6914191441Google Scholar
  35. Pierson, P.M., Lamers, A., Flik, G., Mayer-Gostan, N. 2004The stress axis, stanniocalcin, and ion balance in rainbow troutGen. Comp. Endocrinol.137263271CrossRefPubMedGoogle Scholar
  36. Powell, M.D., Perry, S.F. 1997Respiratory and acid-base disturbances in rainbow trout blood during exposure to chloramine-T under hypoxia and hyperoxiaJ. Fish Biol.50418428Google Scholar
  37. Rabalais, N.N., Wiseman, W.J.,Jr, Turner, R.E. 1994Comparison of continuous records of near-bottom dissolved oxygen from the hypoxia zone along the Louisiana coastEstuaries17850861Google Scholar
  38. Reid, S.G., Perry, S.F. 1991The effects and physiological consequences of raised levels of cortisol on rainbow trout (Oncorhynchus mykiss) erythrocyte β-adrenoceptorsJ. Exp. Biol.158217240PubMedGoogle Scholar
  39. Swallow, C., Grinstein, S., Sudsberg, R., Rostein, O.D. 1993Relative roles of Na+/H+ exchange and vacuolar-type H+-ATPases in regulating cytoplasmic pH and function in murine peritoneal macrophagesJ. Cell Physiol.157453460CrossRefPubMedGoogle Scholar
  40. Taft, J.L., Taylor, W.R., Hartwig, E.O., Loftus, R. 1980Seasonal oxygen depletion in the Chesapeake BayEstuaries3242247Google Scholar
  41. Taylor, J.C., Miller, J.M. 2001Physiological performance of juvenile southern flounder, Paralichthys lethostigma (Jordan and Gilbert, 1884), in chronic and episodic hypoxiaJ. Exp. Mar. Biol. Ecol258195214CrossRefPubMedGoogle Scholar
  42. Turner, R.E., Schroeder, W.W., Wiseman, W.J.,Jr. 1987The role of stratification in the deoxygenation of Mobile Bay and the adjacent shelf bottom watersEstuaries101319Google Scholar
  43. Vogelbein, W.K., Zwerner, D.E., Kator, H., Rhodes, M. and Cardinal, J. 1999. Epizootic mycobacteriosis in Chesapeake Bay striped bass. In: Proceedings of the 24th Annual Eastern Fish Health Workshop, 8–11 March 1999, National Fish Health Research Laboratory, Atlantic Beach, NC. West Virginia.Google Scholar
  44. Wedemeyer, G.A., Barton, B.A., McLeay, D.J. 1990Stress and acclimationSchreck, C.B.Moyle, P.B. eds. Methods for Fish BiologyAmerican Fisheries SocietyBethesda, Maryland451489Google Scholar
  45. Wojtaszek, J., Dziewulska-Szwajkowska, D., Lozinska-Gabska, M., Adamowicz, A., Dzugaj, A. 2002Hematological effects of high dose of cortisol on the carp (Ciprinus carpio L.): Cortisol effect on the Carp BloodGen. Comp. Endocrinol.125176183CrossRefPubMedGoogle Scholar
  46. Winn, R.N., Knott, D.M. 1992An overview of environmental health in populations exposed to hypoxia in the Savannah River estuaryMar. Ecol. Prog. Ser.88161179Google Scholar
  47. Zar, J.H. 1994Biostatistical AnalysisEnglewood CliffsNJ662Google Scholar
  48. Zulueta, J.J., Yu, F.S., Thannickal, V.J., Hassoun, P.M. 1995Release of hydrogen peroxide in response to hypoxiareoxygenation: role of an NAD(P)H oxidase-like enzyme in endothelial cell plasma membraneAm. J. Resp. Cell Mol. Biol.124149Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • A. Valenzuela
    • 1
  • V. Silva
    • 2
  • E. Tarifeño
    • 3
  • A. Klempau
    • 4
  1. 1.Ph.D. Program in Biological Science, Fish Culture Laboratory, Oceanography DepartmentUniversity of ConcepciónConcepciónChile
  2. 2.Faculty of Pharmacy, Clinical Biochemistry and Immunology DepartmentUniversity of ConcepciónConcepciónChile
  3. 3.Faculty of Natural Sciences and Oceanography, Zoology DepartmentUniversity of ConcepciónConcepciónChile
  4. 4.Faculty of Natural Sciences and Oceanography, Oceanography DepartmentUniversity of ConcepciónConcepciónChile

Personalised recommendations