Skip to main content
Log in

Dietary vitamin C, immunity and disease resistance in Atlantic salmon (Salmo salar)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Presmolt Atlantic salmon were fed a fish meal based experimental diet supplemented with graded levels of ascorbate-2-monophosphate (AP), equivalent to 40, 400, 2000 and 4000 mg ascorbic acid (AA)/kg for 6 months prior to a bacterial challenge experiment. The liver AA concentration reflected the dietary intake of AP, but not linearly. Growth, hematology and acid phosphatase activity in zymosan stimulated macrophages were not affected by dietary AP. Serum hemolytic complement activity was higher in fish fed the highest AP level, but the variation was not significant. Production of specific antibodies was significantly higher in fish fed the highest AP level 11 and 17 weeks after vaccination. Bacterial challenge with Aeromonas salmonicida showed increased survival in the 4000 AP group. Lysozyme activity in headkidney and serum complement activity and serum iron in fish surviving the challenge were higher in the 4000 AP group, indicating important roles of vitamin C on lysozyme, complement and iron in non-specific disease resistance. The results indicate that high dietary levels of AP favourably affect health in Atlantic salmon. Disease resistance was, however, not correlated with the AA status in the liver.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References cited

  • Anggawati-Satyabudhy, A.M., Grant, B.F. and Halver, J.E. 1989. Effects of L-ascorbyl phosphates (AsPP) on growth and immunoresistance of rainbow trout (Oncorhynchus mykiss) to infectious hematopoietic necrosis (IHN) virus. In Proc. Third Int. Symp. on Feeding and Nutrition in Fish. pp. 411–426. Toba, Japan.

  • Austreng, E., Storebakken, T. and Åsgård, T. 1987. Growth rate estimates for cultured Atlantic salmon and rainbow trout. Aquaculture 60: 57–60.

    Article  Google Scholar 

  • Beisel, W.R. 1982. Single nutrients and immunity. Am. J. Clin. Nutr. (supplement) 35: 417–468.

    PubMed  CAS  Google Scholar 

  • Bell, G.R., Higgs, D.A. and Traxler, G.S. 1984. The effect of dietary ascorbate, zinc and manganese on the development of experimentally induced bacterial kidney disease in sockeye salmon (Oncorhynchus nerka). Aquaculture 36: 293–311.

    Article  CAS  Google Scholar 

  • Blazer, V.S. 1982. The effects of marginal deficiencies of ascorbic acid and α-tocopherol on the natural resistance and immune response of rainbow trout (Salmo gairdneri). Ph. D. dissertation, University of Rhode Island, U.S.A.

  • Chandra, R.K. 1988. Nutritional regulation of immunity: An introduction. In Nutrition and Immunology. p. 342. Edited by R.K. Chandra. Alan R. Liss Inc., New York.

    Google Scholar 

  • Dabrowski, K., El-Fiky, N., Köck, G., Frigg, M. and Wieser, W. 1990. Requirement and utilization of ascorbic acid and ascorbic sulfate in juvenile rainbow trout. Aquaculture 91: 317–337.

    Article  CAS  Google Scholar 

  • Durve, V.S. and Lovell, R.T. 1982. Vitamin C and disease resistance in channel catfish (Ictalurus punctatus). Can. J. Fish Aquat. Sci. 39: 948–951.

    CAS  Google Scholar 

  • El Naggar, G.O. and Lovell, R.T. 1991. L-ascorbyl-2-monophosphate has equal antiscorbutic activity as L-ascorbic acid but L-ascorbyl-2-sulfate is inferior to L-ascorbic acid in channel catfish. J. Nutr. 121: 1622–1626.

    PubMed  Google Scholar 

  • Ellis, A.E. 1990. Lysozyme assays. In Techniques in Fish Immunology. pp. 101–103. Edited by J.S. Stolen, T.C. Fletcher, D.P. Anderson, B.S. Robertson and W.B. van Muiswinkel. SOS Publications, Fair Haven.

    Google Scholar 

  • Erdal, J.I. and Reitan, L.J. 1991. Immune response and protective immunity after vaccination of Atlantic salmon (Salmo salar L.) against furunculosis. J. Fish Shellfish Immunol. 2: 99–108.

    Google Scholar 

  • Erdal, J.I., Evensen, Ø., Kaurstad, O.K., Lillehaug, A., Solbakken, R. and Thorud, K. 1991. Relationship between diet and immune response in Atlantic salmon (Salmo salar L.) after feeding various levels of ascorbic acid and omega-3-fatty acids. Aquaculture 98: 363–379.

    Article  CAS  Google Scholar 

  • Ghoneum, M., Sadek, I.A., Gill, G. and Cooper, E.L. 1990. Ascorbic acid suppresses natural killer cell activity in Bufo marinus. Dis. Aquat. Org. 9: 1–4.

    CAS  Google Scholar 

  • Grinde, B. 1989. Lysozyme activity from rainbow trout, Salmo gairdneri Richardson, as an antibacterial agent against fish pathogens. J. Fish Dis. 12: 95–104.

    Article  CAS  Google Scholar 

  • Hardie, L.J., Fletcher, T.C. and Secombes, C.J. 1991. The effect of dietary vitamin C on the immune response of the Atlantic salmon (Salmo salar L.). Aquaculture 95: 201–214.

    Article  CAS  Google Scholar 

  • Hilton, J.W., Cho, C.Y. and Slinger, S.J. 1977. Evaluation of the ascorbic acid status of rainbow trout (Salmo gairdneri). J. Fish Res. Bd. Can. 34: 2207–2210.

    CAS  Google Scholar 

  • Hilton, J.W. 1984. Ascorbic acid-mineral interactions in fish. In Ascorbic Acid in Domestic Animals. pp. 218–224. Edited by I. Wegger, F.J. Tagwerker and J. Moustgaard. The Royal Danish Agricultural Society, Copenhagen.

    Google Scholar 

  • Håvardstein, L.S., Endresen, C., Hjeltnes, B., Christie, K.E. and Glette, J. 1990. Specific immunoglobulins in serum from Atlantic salmon, Salmo salar L., immunized with Vibrio salmonicida and infectious pancreatic necrosis virus. J. Fish Dis. 13: 101–111.

    Article  Google Scholar 

  • Ingram, G.A. 1990. Complement-fixation test. In Techniques in Fish Immunology. pp. 25–40. Edited by J.S. Stolen, T.C. Fletcher, D.P. Anderson, B.S. Robertson and W.B. van Muiswinkel. SOS Publications, Fair Haven.

    Google Scholar 

  • Komarov, I.P. and Knyazeva, L.M. 1984. Effect of vitamin C-enriched feed on the physiological state of spawning rainbow trout. Aqua. Hydr. Ichtyol. 2: 43–48.

    Google Scholar 

  • Lall, S.P., Olivier, G., Weerakoon, D.E.M. and Hines, J.A. 1989. The effect of vitamin C deficiency and excess on immune response in Atlantic salmon (Salmo salar). Proc. Third Int. Symp. on Feeding and Nutrition in Fish. pp. 427–441. Toba, Japan.

  • Leith, D., Holmes, J. and Kaattari, S. 1989. Effects of vitamin nutrition on the immune response of hatchery-reared salmonids. Final report from Bonneville Power Administration, p. 83. Division of Fish and Wildlife, Portland.

    Google Scholar 

  • Lie, Ø., Evensen, Ø., Sørensen, A. and Frøysadal, E. 1989. Study on lysozyme activity in some fish species. Dis. Aquat. Org. 6: 1–5.

    CAS  Google Scholar 

  • Li, Y. and Lovell, R.T. 1985. Elevated levels of dietary ascorbic acid increase immune responses in channel catfish. J. Nutr. 115: 123–131.

    PubMed  CAS  Google Scholar 

  • Liu, P.R., Plumb, J.A., Guerin, M. and Lovell, R.T. 1989. Effect of megalevels of dietary vitamin C on the immune response of channel catfish Ictalurus punctatus in ponds. Dis. Aquat. Org. 7: 191–194.

    Article  CAS  Google Scholar 

  • Maage, A., Waagbø, R., Olsson, P.E., Julshamn, K. and Sandnes, K. 1990. Ascorbate-2-sulfate as a dietary vitamin C source for Atlantic salmon (Salmo salar): 2. Effects of dietary levels and immunization on the metabolism of trace elements. Fish Physiol. Biochem. 8: 429–436.

    CAS  Google Scholar 

  • Navarre, O. and Halver, J.E. 1989. Disease resistance and humoral antibody production in rainbow trout fed high levels of vitamin C. Aquaculture 79: 207–221.

    Article  CAS  Google Scholar 

  • Parry, R.M., Chandau, R.C. and Shahani, R.M. 1965. A rapid and sensitive assay of muramidase. Proc. Soc. Exp. Biol. Med. 119: 384–386.

    PubMed  CAS  Google Scholar 

  • Roy, R.B., Conetta, A. and Salpeter, J. 1976. Automated fluorometric method for the determination of total vitamin C in food products. J. Assoc. Off. Anl. Chem. 59: 1244–1250.

    CAS  Google Scholar 

  • Sakai, D.K. 1981. Spontaneous and antibody-dependent hemolysis activities of fish sera and inapplicability of mammalian complements to the immune hemolysis reaction of fishes. Bull. Jap. Soc. Sci. Fish 47: 979–991.

    Google Scholar 

  • Sandnes, K. 1982. Vitamin C in aquaculture. Analysis. Stability in dry feed. Requirement in rainbow trout (Salmo gairdneri) (in Norwegian). Cand. Real. Thesis, University of Bergen, Norway.

  • Sandnes, K. 1991. Vitamin C in fish nutrition—A review. Fisk. Dir. Skr. Ser. Ernæring 4: 3–32.

    CAS  Google Scholar 

  • Sandnes, K., Hansen, T., Killie, J-E.A. and Waagbø, R. 1990. Ascorbate-2-sulfate as a dietary vitamin C source for Atlantic Salmon (Salmo salar): 1. Growth, bioactivity, haematology and humoral immune response. Fish Physiol. Biochem. 8: 419–427.

    CAS  Google Scholar 

  • Sandnes, K., Julshamn, K. and Braekkan, O.R. 1984. Interrelationship between ascorbic acid and trace elements in ovarian development in fish. In Ascorbic Acid in Domestic Animals. pp. 213–217. Edited by I. Wegger, F.J. Tagwerker and J. Moustgaard. The Royal Danish Agricultural Society, Copenhagen.

    Google Scholar 

  • Sandnes, K., Lie, Ø. and Waagbø, R. 1988. Normal ranges of some blood chemistry parameters in adult farmed Atlantic salmon (Salmo salar). J. Fish Biol. 32: 129–136.

    Article  CAS  Google Scholar 

  • Sandnes, K., Torrissen, O.J. and Waagbø, R. 1992. The minimum dietary requirement of vitamin C in Atlantic salmon (Salmo salar) fry using Ca ascorbate-2-monophosphate as dietary source. Fish Physiol. Biochem. 10: 315–319.

    Article  CAS  Google Scholar 

  • Sandnes, K. and Waagbø, R. 1991. Enzymatic hydrolysis of ascorbate-2-monophosphate and ascorbate-2-sulphate in vitro, and bioactivity of ascorbate-2-monophosphate in Atlantic salmon (Salmo salar). Fisk. Dir. Skr. Ser. Ernæring 4: 33–39.

    CAS  Google Scholar 

  • Scott, A.L. and Klesius, P.H. 1981. Chemiluminescence: A novel analysis of phagocytosis in fish. In Int. Symp. Fish Biologics: Serodiagnostics and Vaccines. Develop. Biol. Standard 49, pp. 243–254. Leetown.

  • Secombes, C.J. 1990. Isolation of salmonid macrophages and analysis of their killing activity. In Techniques in Fish Immunology. pp. 137–154. Edited by J.S. Stolen, T.C. Fletcher, D.P. Anderson, B.S. Robertson and W.B. van Muiswinkel. SOS Publications, Fair Haven.

    Google Scholar 

  • Tacon, A.G.J. 1985. Nutritional Pathology. United Nations Development Programme, Food and Agriculture Organization of the United Nations, Rome, Italy.

    Google Scholar 

  • Verlhac, V., Doye, A.N., Gabaudan, J., Troutaud, D. and Deschaux, P. 1993. Vitamin nutrition and fish immunity: Influence of antioxidant vitamins (C and E) on immune response of rainbow trout. Proc. IV Int. Symp. on Fish Nutrition and Feeding, Biarritz, France. (In press).

  • Waagbø, R. and Maage, A. 1992. The influence of dietary lipid sources and vitamin E on iron status in postsmolt Atlantic salmon (Salmo salar). Fisk. Dir. Skr. Ser. Ernæring 5: 77–82.

    Google Scholar 

  • Waagbø, R., Øynes, S. and Sandnes, K. 1991. The stability and biological availability of different forms of vitamin C in feed for Atlantic salmon (Salmo salar). Fisk. Dir. Skr. Ser. Ernæring 4: 95–101.

    Google Scholar 

  • Wahli, T., Meier, W. and Pfister, K. 1986. Ascorbic acid induced immune-mediated decrease in mortality in Ichtyopththirius multifiliis infected rainbow trout (Salmo gairdneri). Acta Tropica 43: 287–289.

    PubMed  CAS  Google Scholar 

  • Weiberg, E.D. 1992. Roles of iron in functions of activated macrophages. J. Nutr. Immunol. 1: 41–63.

    Google Scholar 

  • Yano, T., Nakao, M., Furuichi, M. and Yone, Y. 1988. Effects of dietary choline, pantothenic acid and vitamin C on the serum complement activity of red sea bream. Bull. Jap. Soc. Sci. Fish 54: 141–144.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Waagbø, R., Glette, J., Raa-Nilsen, E. et al. Dietary vitamin C, immunity and disease resistance in Atlantic salmon (Salmo salar). Fish Physiol Biochem 12, 61–73 (1993). https://doi.org/10.1007/BF00004323

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00004323

Keywords

Navigation