Abstract
Various endocrinological and immunological parameters involved with the seasonal changes of immunocompetence in common carp, Cyprinus carpio reared under natural conditions were investigated. Plasma concentrations of steroid hormones, IgM levels, IgM-secreting cell (IgMSC) numbers, and water temperature were considered as major parameters. Testosterone, 11-ketotestosterone in males and estradiol-17β in females detected by RIA, increased simultaneously with gonadal maturation, but no significant correlation was found with IgM production measured by ELISA. IgM levels were very high during the spawning season, but did not fluctuate much during the other seasons even at high water temperatures. These changes of IgM are certainly related to sexual maturation. In addition, IgMSC numbers were also high during the spawning season. This positive interaction between endocrine and immune parameters could contribute to the immune systems of common carp being more effective during spawning season. Interestingly, cortisol levels increased with the water temperature and were high during the spawning season, but had no suppressive effect on the IgM levels and IgMSC numbers.
Similar content being viewed by others
References
Aida, K., Kato, T. and Awaji, M. 1984. Effects of castration on the smoltification of precocious male masu salmon Oncorhynchus masou. Bull. Jap. Soc. Sci. Fish. 50: 565–571.
Avtalion, R.R. 1969. Temperature effect on antibody production and immunological memory, in carp Cyprinus carpio immunized against bovine serum albumin (BSA). Immunol. 17: 927–931.
Bly, J.E. and Clem, L.W. 1991. Temperature-mediated processes in teleost immunity: in vitro immunosuppression induced by in vivo low temperature in channel catfish. Vet. Immunol. Immunopathol. 28: 365–377.
Daggfeldt, A., Bengten, E. and Pilstrom L. 1993. A cluster type organization of the loci of the immunoglobulin light chain in Atlantic cod (Gadus morhua L.) and rainbow trout (Oncorhynchus mykiss Walbaum) indicated by nucleotide sequences of cDNAs and hybridization analysis. Immunogenetics 38: 199–209.
Ellsaesser, C.F. and Clem, L.W. 1987. Cortisol-induced hematologic and immunologic changes in channel catfish (Ictalurus punctatus). Comp. Biochem. Physiol A. 88: 405–408.
Estevez, J., Leiro, J., Santamarina, M.T. and Ubeira, F.M. 1995. A sandwich immunoassay to quantify low levels of turbot (Scophthalmus maximus) immunoglobulins. Vet. Immunol. Immunopathol. 45: 165–174.
Fujiki, K., Shin, DH., Nakao, M. and Yano, T. 2000. Molecular cloning and expression analysis of carp (Cyprinus carpio) interleukin-1β, high affinity immunoglobulin E Fc receptor γ subunit and serum amyloid A. Fish Shellfish Immunol. 10: 229–242.
Hou, Y., Suzuki, Y. and Aida, K. 1999a. Changes in immunoglobulin producing cells in response to gonadal maturation in rainbow trout. Fisheries Sci. 65: 844–849.
Hou, Y., Suzuki, Y. and Aida, K. 1999b. Effects of steroids on immunoglobulin M (IgM) in rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 20: 155–162.
Hou, Y., Suzuki, Y. and Aida, K. 1999c. Effects of steroids on the antibody producing activity of lymphocytes in rainbow trout. Fisheries Sci. 65: 850–855.
Kanlis, G., Suzuki, Y., Tauchi, M., Numata, T., Shirojo, Y. and Takashima, F. 1995. Immunoglobulin in oocytes, fertilized eggs, and yolk sac larvae of red sea bream. Fisheries Sci. 61; 787–790.
Klesius, P.H. 1990. Effect of size and temperature on the quantity of immunoglobulin in channel catfish, Ictalurus punctatus. Vet. Immunol. Immunopathol. 24: 187–195.
Kobayashi, M., Aida, K. and Hanyu, I. 1986. Gonadotropin surge during spawning in male gold fish. Gen. Comp. Endocrinol. 62: 70–79.
Kobayashi, M., Aida, K. and Hanyu, I. 1987. Hormone changes during ovulation and effects of steroid hormones on plasma gonadotropin levels and ovulation in goldfish. Gen. Comp. Endocrinol. 67: 24–32.
Laing K.J., Zou, J.J., Wang, T., Bols, N., Hirono, I., Aoki, T. and Secombes, C.J. 2002. Identification and analysis of an interleukin 8–like molecule in rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 26: 433–444.
Lee, E.Y., Park, H.H., Kim, Y.T. and Choi, T.J. 2001. Cloning and sequence analysis of the interleukin-8 gene from flounder (Paralichthys olivaceous). Gene. 274; 237–243.
Lobb, C.J., Olson, M.O. and Clem, L.W. 1984. Immunoglobulin light chain classes in a teleost fish. J. Immunol. 132: 1917–1923.
Lou, S.W., Aida, K., Hanyu, I., Sakai, K., Nomura, M., Tanaka, M. and Tazaki S. 1986. Endocrine profiles in the females of a twice-annually spawning strain of rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 64: 212–219.
Maule, A.G. and Schreck, C.B. 1990. Glucocorticoid receptors in leukocytes and gill of juvenile coho salmon (Oncorhynchus kistuch). Gen. Comp. Endocrinol. 77: 448–455.
Maule, A.G., Schrock, R., Slater, C., Fitzpatrick, M.S. and Schreck, C.B. 1996. Immune and endocrine responses of adult chinook salmon during fresh water immigration and sexual maturation. Fish Shellfish Immunol. 6: 221–233.
Maule, A.G., Tripp, R.A., Kaattari, S.L. and Schreck, C.B. 1989. Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha). J. Endocrinol. 120: 135–142.
Nagae, M., Fuda, H., Hara, A., Kawamura, H. and Yamauchi, K. 1993. Changes in serum immunoglobulin M (IgM) concentrations during early development of chum salmon (Oncorhynchus keta) as determined by sensitive ELISA technique. Comp. Biochem. Physiol. 106A: 69–77.
Nagae, M., Fuda, H., Ura, K., Kawamura, H., Adachi, S., Hara, A. and Yamauchi, K. 1994. The effect of cortisol on blood plasma immunoglobulin M(IgM) concentrations in masu salmon (Oncorhynchus masou). Fish Physiol. Biochem. 13: 41–48.
Nakanishi, T. 1986. Seasonal changes in the humoral immune response and the lymphoid tissues of the marine teleost, Sebastiscus marmoratus. Vet. Immunol. Immunopathol. 12: 213–221.
Pickering A.D. 1986. Changes in blood cell composition of the brown trout, Salmo trutta L., during the spawning season. J. Fish Biol. 29: 335–347.
Pickering, A.D. and Christie, P. 1980. Sexual differences in the incidence and severity of ectoparasitic infestation of the brown trout, Salmo trutta L. J. Fish Biol. 16: 669–683.
Pickering, A.D. and Pottinger T.G. 1987. Lymphocytopenia and interrenal activity during sexual maturation in the brown trout, Salmo trutta L. J. Fish Biol. 30: 41–50.
Richards, R.H. and Pickering A.D. 1978. Frequency and distribution patterns of Saprolegnia infection in wild and hatchery-reared brown trout, Salmo trutta L. and char Salvelinus alpinus (L.). J. Fish Dis. 1: 69–62.
Rijkers, G.T., Frederix-Woltersw, E.M.H. and van Muiswinkel W.B. 1980. The immune system of cyprinid fish. Kinetics and temperature dependence of antibody producing cells in carp (Cyprinus carpio). Immunol. 41: 91–97.
Robertson, D. 1979. Host parasite interactions between Ichthyobodo necator (Henneguy, 1883) and farmed salmonids. J. Fish Dis. 2: 481–493.
Saha, N.R., Usami, T. and Suzuki, Y. 2003. A double staining flow cytometric assay for the detection of steroid induced apoptotic leucocytes in common carp (Cyprinus carpio). Dev. Comp. Immunol. 27; 351–363.
Sanchez, C., Babin, M., Tomillo, J. Ubeira, F.M and Dominguez, J. 1993. Quantification of low levels of rainbow trout immunoglobulins by enzyme immunoassay using two monoclonal antibodies. Vet. Immunol. Immunopathol. 36: 65–74.
Schmidt, P.J. and Idler, D.R. 1962. Steroid hormones in the plasma of salmon at various stages of maturation. Gen. Comp. Endocrinol. 2: 204–214.
Schreck, C.B. 1992. Glucocorticoids: Metabolism, growth and development. In “The Endocrinology of Growth, Development and Metabolism in Vertebrates”. pp. 367–392. Edited by M.P. Schreibman, C.G. Scanes and P.K.T. Pang. Academic press, New York.
Secombes, C.J., Zou, J., Daniels, G., Cunningham, C., Koussounadis, A and Kemp, G. 1998. Rainbow trout cytokine and cytokine receptor genes. Immunological reviews 166: 333–340.
Slater, C.H. and Schreck, C.B. 1993. Testosterone alters the immune response of chinnok salmon (Oncorhynchus tshawytscha). Gen. Comp. Endocrinol. 89: 291–298.
Slater, C.H., Fitzpatrick, M.S. and Schreck, C.B. 1995. Androgens and immunocompetence in salmonids: specific binding of and reduced immunocompetence of salmonid lymphocytes exposed to natural and synthetic androgens. Aquaculture 136: 363–370.
Slater, C.H. and Schreck, C.B. 1998. Season and physiological parameters modulate salmonid leucocyte androgen receptor affinity and abundance. Fish Shellfish Immunol. 8: 379–391.
Suzuki, Y., Orito, M., Furukawa, K. and Aida, K. 1994. Existence of low molecular weight immunoglobulin M in carp eggs. Fisheries Sci. 60: 159–162.
Suzuki, Y., Orito, M., Iigo, M., Kenzuka, H., Kobayashi, M. and Aida, K. 1996. Seasonal changes in blood IgM levels in goldfish, with special reference to water temperature to water temperature and gonadal maturation. Fisheries Sci. 62: 754–759.
Suzuki, Y., Otaka, T., Sato, S., Hou, Y.Y. and Aida, K. 1997. Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol. Biochem. 17: 415–421.
Tanaka, T., Furukawa, K., Suzuki, Y. and Aida, K. 1999. Transfer of maternal immunity from mother to egg may have no protective meaning for larvae of red sea bream Pagrus major, a marine teleost. Fisheries Sci. 65; 240–243.
Tripp, R.A., Maule, A.G., Schreck, C.B. and Kaattari, S.L. 1987. Cortisol mediated suppression of salmonid lymphocyte responses in vitro. Dev. Comp. Immunol. 11: 565–576.
Weyts, F.A.A., Verburg-van Kemenade, B.M.L., Flik, G., Lambert, J.G.D. and Wendelaar Bonga, S.E. 1997. Conservation of apoptosis as an immune regulatory mechanism: effects of cortisol and cortisone on carp lymphocytes. Brain, Behavior, and Immunity. 11: 95–105.
Wingfield, J.C. and Grimm, A.S. 1977. Seasonal changes in plasma cortisol, testosterone, and estradiol-17β in plaice, Pleuronectes platessa L. Gen. Comp. Endocrinol. 31: 1–11.
Wishkovsky, A. and Avtalion, R.R. 1987. Induction immunosuppression to bacterial antigens in carp, Cyprinus carpio. J. Fish. Biol. 31(Suppl. A): 101–106.
Zapta, A.G., Varas, A. and Torroba, M. 1992. Seasonal variations in the immune system of lower vertebrates. Immunol. Today 13: 142–147.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Saha, N., Usami, T. & Suzuki, Y. Seasonal changes in the immune activities of common carp (Cyprinus carpio). Fish Physiology and Biochemistry 26, 379–387 (2002). https://doi.org/10.1023/B:FISH.0000009275.25834.67
Issue Date:
DOI: https://doi.org/10.1023/B:FISH.0000009275.25834.67