Influence of Environmental Temperature on the Immune Response in Fish

  • R. R. Avtalion
  • A. Wojdani
  • Z. Malik
  • R. Shahrabani
  • M. Duczyminer
Conference paper
Part of the Current Topics in Microbiology and Immunology / Ergebnisse der Mikrobiologie und Immunitätsforschung book series (CT MICROBIOLOGY, volume 61)


At the end of the last century and the beginning of this century, the problems of immunity in lower vertebrates and the influence of environmental temperature attracted attention for the first time (Ernst, 1890; Widal and Sicard, 1897; Metchnikoff, 1901). However, relatively little work has been done on this subject until recently. The early investigators were chiefly interested in the immuno-pathological problems. They immunized various species of lower vertebrates essentially with bacterial vaccines; agglutinating, neutralizing and protective antibodies were detected in their blood. The influence of environmental temperature on the immune response was investigated, since this subject represented great economical and theoretical importance. Epizootic diseases were observed to occur in relation to the cold season of the year, when the decrease or spontaneous increase of water temperature occurred (Schaperclaus, 1965; Besse et al., 1965; Klontz et al., 1965 Wood, 1966). The immunological deficiency of fish, caused by their natural or experimental stay in cold water, is now evident for both humoral and cellular immunity. In this review we will focus on two points: We shall attempt (1) to explain the mechanism by which the environmental temperature influences the immune resistance of fish to pathogens, (2) to determine the chronological location of this temperature-sensitive stage in the process of antibody formation, and to make some approaches to the general antibody formation mechanism.


Rainbow Trout Environmental Temperature Antibody Production Antigenic Stimulation Brook Trout 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adam, H.: Peritrophic membranes in the intestine of the hagfish (Myxine glutinosa). In: Phylogeny of immunity (ed. by R. T. Smith, P. A. Miescher and R. A. Good), p. 147. Florida: University Press 1965Google Scholar
  2. Ambrosius, H., Lehmann, R.: Beiträge zur Immunobiologie poikilothermer Wirbeltiere. III. Der Einfluß von Adjuvanten auf die Antikörper-Production. Acta. biol. med. German. 14, 830–944 (1965).PubMedGoogle Scholar
  3. Aeser, C. S.: Gjeddepsten in 1923. Norsk Veterinaertidsskr. (1925) (Cit. by Pliska).Google Scholar
  4. Avetikyan, B. G.: Immunological reaction in fishes. Akad. Nauk SSSR, Ikht, Kom. 8, 387–392 (1958).Google Scholar
  5. Avrameas, S., Ternynck, T.: Biologically active water-insoluble protein polymers. I. Their use for isolation of antigens and antibodies. J. biol. Chem. 242, 1651–1659 (1967).PubMedGoogle Scholar
  6. Avtalion, R. R.: Influence de la temperature ambiante sur la production des anticorps chez la carpe. Verh. int. Verein. Limnol. 17, 630–636 (1969a).Google Scholar
  7. Avtalion, R. R.: Temperature effect on antibody production and immunological memory in carp (Cyprinus carpio) immunized against bovine serum albumin (BSA). Immunology 17, 927–931 (1969b).PubMedGoogle Scholar
  8. Avtalion, R. R.: Secondary response and immunological memory in carp (Cyprinus carpio) immunized against bovine serum albumin. Israel J. med. Sci. 5, 441–442 (1969c).Google Scholar
  9. Avtalion, R. R., Malik, Z., Lefler, E., Katz, E.: Temperature effect on immune resistance of fish to pathogens. Bamidge Bull. Fish. Cul. Isr. 22, 33–38 (1970).Google Scholar
  10. Babes, V., Riegler, P.: Über eine Fischepidemie bei Bukarest. Zbl. Bakt., I. Abt. Orig. 33, 488 (1903) (Cit. by Bisset, 1947a).Google Scholar
  11. Barrow, J. H., Jr.: Social behavior in fresh-water fish and its effect on resistance to trypanosomes. Proc. nat. Acad. Sci. (Wash.) 41, 676–679 (1955).PubMedCrossRefGoogle Scholar
  12. Bergman, A.: Smittosam Ogonsjukdom, Keretomalei, nos torsk vid sveriges sydkast. Skand. Vet. Tidskr. (1911) (Cit. by Pliska).Google Scholar
  13. Besse, P., Levaditi, J. C., Guillon, J. C., Kinkelin, P. de: Occurrence of viral diseases in the rainbow trout hatcheries in France. First histopathological results. Ann. N.Y. Acad. Sci. 126, 543–546 (1965).PubMedCrossRefGoogle Scholar
  14. Bisset, K. A.: The effect of temperature on non-specific infections of fish. J. Path. Bact. 58, 251–258 (1946).PubMedCrossRefGoogle Scholar
  15. Bisset, K. A.: Bacterial infection and immunity in lower vertebrates and invertebrates. J. Hyg. (Lond.) 45, 128–135 (1947a).CrossRefGoogle Scholar
  16. Bisset, K. A.: The effect of temperature on immunity in amphibia. J. Path. Bact. 59, 301–306 (1947b).PubMedCrossRefGoogle Scholar
  17. Bisset, K. A.: Natural and acquired immunity in frogs and fish. J. Path. Bact. 59, 679–682 (1947c).PubMedCrossRefGoogle Scholar
  18. Bisset, K. A.: The effect of temperature upon antibody production in cold-blooded vertebrates. J. Path. Bact. 60, 87–92 (1948).PubMedCrossRefGoogle Scholar
  19. Bisset, K. A.: The influence of adrenal cortical hormones upon immunity in cold blooded vertebrates. J. Endocr. 6, 99–103 (1949)PubMedCrossRefGoogle Scholar
  20. Bullock, G. L., McDaniel, D. W.: Bacterial diseases. U.S. Fish and Wildl. Ser., Prog. in Sport Fish. Res., Resource Publ. 64, 18–20 (1968).Google Scholar
  21. Clem, L. W., Sigel, M. M.: Comparative immunochemical and immunological reactions in marine fishes with soluble, viral and bacterial antigens. Fed. Proc. 22, 1138 (1965).Google Scholar
  22. Cushing, J. E.: An effect of temperature upon antibody production in fish. J. Immunol. 45, 123–126 (1942).Google Scholar
  23. Duff, D. C. B.: The oral immunization of trout against Bacterium salmonicida. J. Immunol. 44, 87–94 (1942).Google Scholar
  24. Ernst, P.: Brit. J. Path. 8, 203 (1890) (Cit. by Bisset, 1948).Google Scholar
  25. Evans, E. E., Cowles, R. B.: Effect of temperature on antibody synthesis in the reptile Dipsosaurus dorsalis. Proc. Soc. exp. Biol. (N.Y.) 101, 482–483 (1959).Google Scholar
  26. Evans, E. E., Kent, S. P., Marie, H.: Antibody synthesis in poikilothermic vertebrates. Ann. N.Y. Acad. Sci. 126, 629–646 (1965).PubMedCrossRefGoogle Scholar
  27. Evelyn, T. P. T.: The agglutinin response in sockeye salmon vaccinated intraperitoneally with a heat-killed preparation of the bacterium responsible for salmonid kidney disease. J. Wildl. Dis. 7, 328–335 (1971).PubMedGoogle Scholar
  28. Feng, S. Y.: Experimental bacterial injections in oyster (Crassostrea virginica). J. Invert. Path. 8, 505–511 (1966).CrossRefGoogle Scholar
  29. Fijan, N., Cvetnic, S.: Immunitetna reactivnost sarana. I. Reativnost jednogodisnjih sarana kod 13–15°C u akvarijskim uslovima. Vet. Arh. (Zagreb) 1–2, 17–20 (1964).Google Scholar
  30. Fijan, N., Cvetnic, S.: Immunitetna reativnost sarana. II. Reativnost tokom godine kod drzanja u ribnjacima. Vet. Arh. (Zagreb) 3–4, 100–105 (1966).Google Scholar
  31. Fujihara, M. P.: Oral immunization of juvenile coho salmon against Chondrococcus columnaris disease. Bact. Proc. Abstr. M. 164, 92 (1969).Google Scholar
  32. Gee, L. L., Smith, W. W.: Defences against trout furunculosis. J. Bact. 81, 266–267 (1941).Google Scholar
  33. Goncharov, C. D.: Rubella, a viral fish disease. Ann. N.Y. Acad. Sci. 126, 598–600 (1965).PubMedCrossRefGoogle Scholar
  34. Goncharov, G. D., Mikriakov, V. R.: Etude des facteurs de l’immunité des poissons à une infection bacterienne. Bull. off. Int. Epiz. 69, 1373–1376 (1968).Google Scholar
  35. Good, R. A., Finstad, J., Pollara, B., Gabrielsen, A. E.: Morphologic studies on the evolution of the lymphoid tissues among the lower vertebrates, in Phylogeny of Immunity. (Ed. by R. T. Smith, P. A. Miescher and R. A. Good.) p. 149. Florida: University Press 1965.Google Scholar
  36. Guelin, A., Lablin, D.: The survival of bacteria and psychrotrophic bacteriophages in the digestive tubes of trout. Ann. Inst. Pasteur Lille 15, 207–211 (1964).PubMedGoogle Scholar
  37. Heddleston, K. L., Rebers, P. A.: Fowl cholera: active immunity induced in chidkens and turkeys by oral administration of heat killed Pasteurella multocida. Avian Dis. 12, 129–134 (1968).PubMedCrossRefGoogle Scholar
  38. Hildemann, W. H.: Immunogenetic studies of poikilothermic animals. Amer. Naturalist 96, 195–204 (1962).CrossRefGoogle Scholar
  39. Keast, A.: Feeding of some great lakes fishes at low temperatures. J. Fish. Res. Bd. Can. 25, 1199–1218 (1968).CrossRefGoogle Scholar
  40. Klontz, G. W.: Some serological cytological and histopathological aspects of immune response in rainbow trout (Salmo gairdnery) M. Sc. Thesis (1959) (Cit. by Ridgway et al.).Google Scholar
  41. Klontz, G. W., Anderson, D. P.: Oral immunization of salmonids: A review, in a Symposium on Diseases of Fishes and Shellfishes (ed. by S. F. Sneiszko), p. 16–20. Amer. Fish. Soc. Washington D.C. (1970).Google Scholar
  42. Klontz, G. W., Yasutake, W. T., Parisot, T. J.: Viral diseases of salmonidae in western U.S. III. Immunopathological aspects. Ann. N.Y. Acad. Sci. 126, 531–542 (1965).PubMedCrossRefGoogle Scholar
  43. Krantz, G. E., Reddecliff, J. M., Heist, C. E.: Development of antibodies against Aeromonas salmonicida in trout. J. Immunol. 91, 757–760 (1963).PubMedGoogle Scholar
  44. Krantz, G. E., Reddecliff, J. M., Heist, C. E.: Immune response of trout to Aeromonas salmonicida. I. Development of agglutinating antibodies and protective immunity. Prog. Fish. Cult. 26, 3–10 (1964a).CrossRefGoogle Scholar
  45. Krantz, G. E., Reddecliff, J. M., Heist, C. E.: Immune response of trout to Aeromonas salmonicida. II. Evaluation of feeding techniques. Prog. Fish. Cult. 26, 65–69 (1964b).CrossRefGoogle Scholar
  46. Kreuger, R. G., Twedt, K. M.: Cellular demonstration of antibody production in Rana pipiens. J. Immunol. 90, 952 (1963).Google Scholar
  47. Lefler, E.: Antibody production in frog (R. ridibunda) immunized against soluble and particular antigens and temperature effect. M. Sc. Thesis, Bar Ilan University, Israel (1970).Google Scholar
  48. Lefler, E., Avtalion, R. R.: Temperature effect on antibody formation in the frog Rana ridibunda. Israel J. med. Sci. 6, 10 (1970).Google Scholar
  49. Luklyanenko, V. I.: Natural antibodies in fish. Zool. Zh. 44, 300–304 (1965)Google Scholar
  50. Mackie, T. J., Arkwright, J. A., Pryce-Tannatt, T. E., Nottram, J. C., Johnston, W. D., Menzies, W. J. M.: Final report of the furunculosis committee. Edinburgh: H. M. Stationary Office 1935.Google Scholar
  51. Mackie, J T., Menzies, W. J.: Investigations in Great Britain of furunculosis of the salmonidae. J. comp. Path. 51, 1–14 (1938).Google Scholar
  52. Marchalonis, J. J.: Isolation and partial characterization of Immunoglobulins of gold fish (Carrassius auratus) and carp. (Cyprinus carpio). Immunology 20, 161–173 (1971).PubMedGoogle Scholar
  53. Malik, Z.: Temperature effect on antibody production in carp immunized against bacterial antigens and their immune resistance to a pathogenic agent. M. Sc. Thesis, Bar Ilan University, Israel (1970).Google Scholar
  54. Maung, R. T.: Immunity in the tortoise Testudo ibera. J. Path. Bact. 85, 51–66 (1963).PubMedCrossRefGoogle Scholar
  55. Metchnikoff, E.: L’immunite dans les maladies infectieuses, p. 349. Paris: Masson & Cie. 1901.Google Scholar
  56. Meyer, F. P.: Seasonal fluctuations in the incidence of disease on fish farms. In a Symposium on Diseases of Fishes and Shellfishes (ed. by S. F. Sneiszko), p. 21–29. Washington: American Fisheries Society 1970.Google Scholar
  57. Netter, E., Drishane, A. M., Harris, A. H., Yansen, G. T.: Diagnosis of clinical and subclinical salmonellosis by means of serological hemagglutinins (human carriers, polyvalent antigens). New Engl. J. Med. 261, 1162–1165 (1959).CrossRefGoogle Scholar
  58. Nybelin, O.: Über Agglutininbildung bei Fischen. Z. Immun.-Forsch. 84, 74–79 (1935).Google Scholar
  59. Nybelin, O.: The influence of temperature on the formation of agglutinins in fish. Bull. off. Int. Epiz. 69, 1353–1355 (1968).Google Scholar
  60. Ojala, O.: Observations on the occurrence of Aeromonas hydrophila and A. punctata in fish. Bull. off. Int. Epiz. 69, 1107–1123 (1968).Google Scholar
  61. Ortiz-Muniz, G., Sigel, M. M.: Antibody Synthesis in Lymphoid Organs of the two Marine Teleosts. J. Reticuloendothel. Soc. 9, 42–52 (1971).PubMedGoogle Scholar
  62. Ouchi, K.: Effects of water temperature on the scale growth and width of the ridge distance in goldfish. Bul. Jap. Sos. Sci. Fis. 35, 25–31 (1969).CrossRefGoogle Scholar
  63. Papermaster, B. W., Condie, R. M., Good, R. A.: Immune response in the California hagfish. Nature (Lond.) 196, 355–357 (1962).PubMedCrossRefGoogle Scholar
  64. Parisot, T. J., Yasutake, W. T., Klontz, G. W.: Virus diseases of the salmonidae in Western United States. I. Etiology and epizootiology. Ann. N.Y. Acad. Sci. 126, 502–512 (1965).PubMedCrossRefGoogle Scholar
  65. Pliszka, F.: Untersuchungen über die Agglutinine bei Karpfen. Zbl. Bakt. 143, 262–264 (1939a).Google Scholar
  66. Pliszka, F.: Weitere Untersuchungen über Immunitätsreaktionen und über Phagozytose bei Karpfen. Zbl. Bakt. 143, 451–460 (1939b).Google Scholar
  67. Post, G.: Response of rainbow trout (Salmo gairdneri) to antigens of Aeromonas hydrophila. J. Fish. Res. Bd. Can. 23, 1487–1494 (1966).CrossRefGoogle Scholar
  68. Ridgway, G. J.: The application of some special immunological methods to marine population problems. Amer. Naturalist 96, 219–224 (1962).CrossRefGoogle Scholar
  69. Ridgway, G. J., Hodgins, H. O., Klontz, G. W.: The immune response in teleosts. In: Phylogeny of immunity (ed. by R. T. Smith, P. A. Miescher and R. A. Good), p. 199. Florida: University Press 1966.Google Scholar
  70. Rosenberg, M.: Antibody production against BSA, injected in its soluble or particulate forms, in fish and rabbits. M. Sc. Thesis, Bar Ilan University, Israel (1972).Google Scholar
  71. Ross, A. J., Klontz, G. W.: Oral immunization of rainbow trout (Salmo gairdneri) against an etiologic agent of “redmouth disease”. J. Fish. Res. Bd. Can. 22, 713–719 (1965).CrossRefGoogle Scholar
  72. Ross, A. J., Rucker, R. R., Ewing, W. H.: Description of a bacterium associated with redmouth disease of rainbow trout (Salmo gairdneri). Canad. J. Microbiol. 12, 763–770 (1966).CrossRefGoogle Scholar
  73. Schaperclaus, W.: Etiology of infectious carp dropsy. Ann. N. Y. Acad. Sci. 126, 587–597 (1965).PubMedCrossRefGoogle Scholar
  74. Sigel, M., Russell, W. J., Jensen, J. A., Beasley, A. R.: Natural immunity in marine fishes. Bull. off. Int. Epiz. 69, 1349–1351 (1968).Google Scholar
  75. Smith, W. W.: Production of anti-bacterial agglutinins by carp and trout at 10°C. Proc. Soc. exp. Biol. (N.Y.) 45, 726–729 (1940).Google Scholar
  76. Snieszko, S. F.: Therapy of bacterial fish diseases. Trans. Amer. Fish. Soc. 83, 313–330 (1953).CrossRefGoogle Scholar
  77. Snieszko, S. F.: Natural resistance and susceptibility to infections. Prog. Fish. Cult. 20, 133–136 (1958).CrossRefGoogle Scholar
  78. Snieszko, S. F.: Immunization of fish: a review. J. Wildl. Dis. 6, 24–30 (1970).PubMedGoogle Scholar
  79. Snieszko, S. F., Friddle, S. B.: Prophylaxis of furonculosis in brook trout (Salvelinus fontinalis) by oral immunization and sulfamerazine. Prog. Fish. Cult. 11, 161–168 (1949).CrossRefGoogle Scholar
  80. Spence, K. D., Fryer, J. L., Pilcher, K. S.: Active and passive immunization of certain salmonid fishes against Aeromonas salmonicida. Canad. J. Microbiol. 11, 397–405 (1965).CrossRefGoogle Scholar
  81. Stone, H. D., Ritchie, A. E., Boney, W. A.: Immunization of chickens against Newcastle disease with beta propiolactone-killed virus antigen administered in drinking water. Avian Dis. 13, 568–578 (1969).PubMedCrossRefGoogle Scholar
  82. Widal, F., Sicard, A.: C. R. Soc. Biol. (Paris) 49, 1047 (1897) (Cit. by Bisset, 1948).Google Scholar

Copyright information

© Springer-Verlag, Berlin · Heidelberg 1973

Authors and Affiliations

  • R. R. Avtalion
    • 1
  • A. Wojdani
    • 1
  • Z. Malik
    • 1
  • R. Shahrabani
    • 1
  • M. Duczyminer
    • 1
  1. 1.Rapaport Laboratory for Microbiology, Department of Life SciencesBar-Ilan UniversityRamat-GanIsrael

Personalised recommendations