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Cortisol influences the host–parasite interaction between the rainbow trout (Oncorhynchus mykiss) and the crustacean ectoparasite Argulus japonicus

Published online by Cambridge University Press:  05 December 2003

C. HAOND ,
D. T. NOLAN ,
N. M. RUANE ,
J. ROTLLANT  and
S. E. WENDELAAR BONGA
C. HAOND
Affiliation:
Department of Animal Ecology and Ecophysiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands Present address: Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8000-810 Faro, Portugal.
D. T. NOLAN
Affiliation:
Department of Animal Ecology and Ecophysiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands
N. M. RUANE
Affiliation:
Department of Animal Ecology and Ecophysiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands Present address: Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8000-810 Faro, Portugal.
J. ROTLLANT
Affiliation:
Department of Animal Ecology and Ecophysiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands Present address: Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8000-810 Faro, Portugal.
S. E. WENDELAAR BONGA
Affiliation:
Department of Animal Ecology and Ecophysiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands
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Abstract

The host–parasite interaction between the rainbow trout Oncorhynchus mykiss and the fish louse Argulus japonicus was investigated by administering low levels of dietary cortisol before infecting the fish with low numbers of the parasite. After 24 h, the dietary cortisol treatment elevated blood cortisol and glucose levels and stimulated the synthesis of secretory granules in the upper layer of skin cells. Infection with 6 lice per fish caused skin infiltration by lymphocytes, also in areas without parasites. The lymphocyte numbers in the blood at 48 h post-parasite infection were reduced. Other changes, typical for exposure to many stressors and mediated by cortisol, were also found in the epidermis of parasitized fish, although neither plasma cortisol nor glucose levels were noticeably affected. Glucocorticoid receptors were localized immunohistochemically and found in the upper epidermal layer of pavement and filament cells, and in the leucocytes migrating in these layers. Cortisol-fed fish had reduced numbers of parasites and the changes in the host skin are likely involved in this reduction. Thus a mild cortisol stress response might be adaptive in rejecting these parasites. Further, the data suggest that this effect of cortisol is mediated by the glucocorticoid receptor in the skin epidermis, as these are located directly at the site of parasite attachment and feeding in the upper skin cells that produce more secretory granules in response to cortisol feeding.

Keywords

host–parasite interactionArgulus japonicuscortisolepidermislymphocyte
Type
Research Article
Information
Parasitology , Volume 127 , Issue 6 , December 2003 , pp. 551 - 560
Copyright
2003 Cambridge University Press

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References

REFERENCES

BALM, P. H. M. & POTTINGER, T. G. ( 1995). Corticotrope and melanotrope POMC-derived peptides in relation to interrenal function during stress in rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 98, 279–288.CrossRefGoogle Scholar
BALM, P. H. M., IGER, Y., PRUNET, P., POTTINGER, T. G. & WENDELAAR BONGA, S. E. ( 1995). Skin ultrastructure in relation to prolactin and MSH function in rainbow trout (Oncorhynchus mykiss) exposed to environmental acidification. Cell and Tissue Research 279, 351–358.CrossRefGoogle Scholar
BARTON, B. A., SCHRECK, C. B. & BARTON, L. D. ( 1987). Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Diseases of Aquatic Organisms 2, 173–185.Google Scholar
BJORN, P. A. & FINSTAD, B. ( 1997). The physiological effects of salmon lice infection on sea trout post smolts. Nordic Journal of Freshwater Research 73, 60–72.Google Scholar
BROKKEN, L. J. S., VERBOST, P. M., ATSMA, W. & WENDELAAR BONGA, S. E. ( 1998). Isolation, partial characterization and localization of integumental peroxidase, a stress-related enzyme in the skin of a teleostean fish (Cyprinus carpio L.). Fish Physiology and Biochemistry 18, 331–342.CrossRefGoogle Scholar
BUCHMANN, K. & BRESCIANI, J. ( 1997). Parasitic infections in pond-reared rainbow trout Oncorhynchus mykiss in Denmark. Diseases of Aquatic Organisms 28, 125–138.CrossRefGoogle Scholar
BUCHMANN, K., ULDAL, A. & LYHOLT, H. C. K. ( 1995). Parasite infections in Danish trout farms. Acta Veterinaria Scandinavica 36, 283–298.Google Scholar
BURKHARDT-HOLM, P., ESCHER, M. & MEIER, W. ( 1997). Waste-water management plant effluents cause cellular alterations in the skin of brown trout. Journal of Fish Biology 50, 744–758.CrossRefGoogle Scholar
BURY, N. R., LI, J., LOCK, R. A. C. & WENDELAAR BONGA, S. E. ( 1998). Cortisol protects against copper induced necrosis and promotes apoptosis in fish gill chloride cells in vitro. Aquatic Toxicology 40, 193–202.CrossRefGoogle Scholar
DHABHAR, F. S. & McEWEN, B. S. ( 1997). Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leucocyte trafficking. Brain Behaviour and Immunology 11, 286–306.CrossRefGoogle Scholar
ELLIS, A. E. ( 1981). Stress and the modulation of defence mechanisms in fish. In Stress and Fish ( ed. Pickering, A. D. ), pp. 147–169. Academic Press, London.
GRIGNARD, J.-C., MELARD, C. & KESTEMONT, P. ( 1996). A preliminary study of parasites and diseases of perch in an intensive culture system. Journal of Applied Ichthyology 12, 195–199.CrossRefGoogle Scholar
GRIMNES, A. & JAKOBSEN, P. J. ( 1996). The physiological effects of salmon lice infection on post-smolt of Atlantic salmon. Journal of Fish Biology 48, 1179–1194.CrossRefGoogle Scholar
HARRIS, P. D., SOLENG, A. & BAKKE, T. A. ( 2000). Increased susceptibility of salmonids to the monogenean Gyrodactylus salaris following administration of hydrocortisone acetate. Parasitology 120, 57–64.CrossRefGoogle Scholar
IGER, Y. & WENDELAAR BONGA, S. E. ( 1994). Cellular responses of the skin of carp (Cyprinus carpio) exposed to acidified water. Cell and Tissue Research 275, 481–492.CrossRefGoogle Scholar
IGER, Y., BALM, P. H. M., JENNER, H. A. & WENDELAAR BONGA, S. E. ( 1995). Cortisol induces stress-related changes in the skin of rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 97, 188–198.CrossRefGoogle Scholar
IGER, Y., BALM, P. H. M. & WENDELAAR BONGA, S. E. ( 1994 a). Cellular responses of the skin and changes in plasma cortisol levels of trout (Oncorhynchus mykiss) exposed to acidified waters. Cell and Tissue Research 278, 535–542.Google Scholar
IGER, Y., JENNER, H. A. & WENDELAAR BONGA, S. E. ( 1994 b). Cellular responses in the skin of the trout (Oncorhynchus mykiss) exposed to temperature elevation. Journal of Fish Biology 44, 921–935.Google Scholar
IGER, Y., JENNER, H. A. & WENDELAAR BONGA, S. E. ( 1994 c). Cellular responses in the skin of rainbow trout (Oncorhynchus mykiss) exposed to Rhine water. Journal of Fish Biology 45, 1119–1132.Google Scholar
IGER, Y., LOCK, R. A. C., VAN DER MEIJ, J. C. A. & WENDELAAR BONGA, S. E. ( 1994 d). Effects of water-borne cadmium on the skin of the common carp (Cyprinus carpio). Archives of Environmental Contamination and Toxicology 26, 342–350.Google Scholar
JAFRI, S. I. H. & AHMED, S. S. ( 1994). Some observations on mortality in major carps due to fish lice and their chemical control. Pakistan Journal of Zoology 26, 274–276.Google Scholar
JOHNSON, S. C. & ALBRIGHT, L. J. ( 1992 a). Comparative susceptibility and histopathology of the response of naive Atlantic, chinook and coho salmon to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae). Diseases of Aquatic Organisms 14, 179–193.Google Scholar
JOHNSON, S. C. & ALBRIGHT, L. J. ( 1992 b). Effects of cortisol implants on the susceptibility and the histopathology of the responses of naive coho salmon Oncorhynchus kisutch to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae). Diseases of Aquatic Organisms 14, 195–205.Google Scholar
MENEZES, J., RAMOS, M. A., PEREIRA, T. G. & DA SILVA, A. M. ( 1990). Rainbow trout culture failure in a small lake as a result of massive parasitosis related to careless fish introductions. Aquaculture 89, 123–126.CrossRefGoogle Scholar
MUSTAFA, A. & MacKINNON, B. M. ( 1999). Atlantic salmon, Salmo salar L., and Artic char, Salvelinus alpinus (L.): comparative correlation between iodine-iodide levels, plasma cortisol levels, and infection intensity with the sea louse Caligus elongatus. Canadian Journal of Zoology 77, 1092–1101.Google Scholar
MUSTAFA, A., MacWILLIAMS, C., FERNANDEZ, N., MATCHETT, K., CONBOY, G. A. & BURKA, J. F. ( 2000). Effects of sea lice (Lepeophtheirus salmonis Krøyer, 1837) infestation on macrophage functions in Atlantic salmon (Salmo salar L.). Fish and Shellfish Immunology 10, 47–59.CrossRefGoogle Scholar
NOLAN, D. T., HADDERINGH, R. H., JENNER, H. A. & WENDELAAR BONGA, S. E. ( 1998). The effects of exposure to Rhine water on the sea trout smolt (Salmo trutta trutta L.): an ultrastructural and physiological study. In New Concepts for the Sustainable Management of River Basins ( ed. Nienhuis, P. H., Leuven, R. S. E. W. & Ragas, A. M. ), pp. 261–271. Backhuys Publishers, Amsterdam.
NOLAN, D. T., HADDERINGH, R. H., SPANINGS, F. A. T., JENNER, H. A. & WENDELAAR BONGA, S. E. ( 2000). Acute temperature elevation in tap and Rhine water affects skin and gill epithelia, hydromineral balance and gill specific Na+/K+-ATPase activity of brown trout (Salmo trutta L.) smolts. Canadian Journal of Fisheries and Aquatic Sciences 57, 708–718.CrossRefGoogle Scholar
NOLAN, D. T., REILLY, P. & WENDELAAR BONGA, S. E. ( 1999 a). Infection with low numbers of the sea louse Lepeophtheirus salmonis (Krøyer) induces stress-related effects in post-smolt Atlantic salmon (Salmo salar L.). Canadian Journal of Fisheries and Aquatic Sciences 56, 947–959.Google Scholar
NOLAN, D. T., VAN DER SALM, A. L. & WENDELAAR BONGA, S. E. ( 1999 b). In vitro effects of short-term cortisol exposure on proliferation and apoptosis in the skin epidermis of rainbow trout (Oncorhynchus mykiss Walbaum). In Recent Developments in Comparative Endocrinology and Neurobiology ( ed. Roubos, E., Wendelaar Bonga, S. E., Vaudry, H. & De Loof, A. ), pp. 161–162. Shaker Publishers, Maastricht.
NORTHCOTT, S. J., LYNDON, A. R. & CAMPBELL, A. D. ( 1997). An outbreak of freshwater fish lice, Argulus foliaceus L., seriously affecting a Scottish stillwater fishery. Fisheries Management and Ecology 4, 73–75.CrossRefGoogle Scholar
PICKERING, A. D. & POTTINGER, T. G. ( 1989). Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiology and Biochemistry 7, 253–258.CrossRefGoogle Scholar
POOLE, W. R., NOLAN, D. T. & TULLY, O. ( 2000). Modelling the effects of capture and sea lice Lepeophtheirus salmonis (Krøyer) infestation on the cortisol stress response in trout. Aquaculture Research 31, 835–841.CrossRefGoogle Scholar
RAHMAN, M. M. ( 1995). Some aspects of the biology of a freshwater fish parasite, Argulus foliaceus (L.) (Argulidae, Branchiura, Crustacea). Bangladesh Journal of Zoology 23, 77–86.Google Scholar
RAHMAN, M. M. ( 1996). Effects of a freshwater fish parasite, Argulus foliaceus Linn. infection on common carp, Cyprinus carpio Linn. Bangladesh Journal of Zoology 24, 57–63.Google Scholar
ROSS, N. W., FIRTH, K. J., WANG, A. P., BURKA, J. F. & JOHNSON, S. C. ( 2000). Changes in hydrolytic enzyme activities of naive Atlantic salmon Salmo salar skin mucous due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation. Diseases of Aquatic Organisms 41, 43–51.CrossRefGoogle Scholar
RUANE, N. M., NOLAN, D. T., ROTLLANT, J., COSTELLOE, J. & WENDELAAR BONGA, S. E. ( 2000). Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Krøyer) influences the physiological response to an acute stressor. Fish and Shellfish Immunology 10, 451–463.CrossRefGoogle Scholar
RUANE, N. M., NOLAN, D. T., ROTLLANT, J., TORT, L., BALM, P. H. M. & WENDELAAR BONGA, S. E. ( 1999). Modulation of the response of rainbow trout (Oncorhynchus mykiss Walbaum) to confinement, by an ectoparasitic (Argulus foliaceus L.) infestation and cortisol feeding. Fish Physiology and Biochemistry 20, 43–51.CrossRefGoogle Scholar
RUSHTON-MELLOR, S. K. & BOXSHALL, G. A. ( 1994). The developmental sequence of Argulus foliaceus (Crustacea: Branchiura). Journal of Natural History 28, 763–785.CrossRefGoogle Scholar
SCHMIDT, H., BERNET, D., WAHLI, T., MEIER, W. & BURKHARDT-HOLM, P. ( 1999). Active biomonitoring with brown trout and rainbow trout in diluted sewage plant effluents. Journal of Fish Biology 54, 585–596.CrossRefGoogle Scholar
SHIELDS, R. J. & GOODE, R. P. ( 1978). Host rejection of Lernaea cyprinacea L. (Copepoda). Crustaceana 35, 301–307.CrossRefGoogle Scholar
SINGHAL, R. N., JEET, S. & DAVIES, R. W. ( 1990). The effects of argulosis-saprolegniasis on the growth and production of Cyprinus carpio. Hydrobiologica 202, 27–32.Google Scholar
TULLY, O. & NOLAN, D. T. ( 2002). Population biology of Lepeophtheirus salmonis (Copepoda: Caligidae) and parasite impact on the host fish. Parasitology 124, S165–S182.Google Scholar
TUJAGUE, M., SALIGAUT, D., TEITSMA, C., KAH, O., VALOTAIRE, Y. & DUCOURET, B. ( 1998). Rainbow trout glucocorticoid receptor overexpression in Escherichia coli: production of antibodies for Western blotting and immunohistochemistry. General and Comparative Endocrinology 110, 201–211.CrossRefGoogle Scholar
VAN DER SALM, A., NOLAN, D. T., SPANINGS, F. A. T. & WENDELAAR BONGA, S. E. ( 2000). Effects of infection with the ectoparasite Argulus japonicus (Thiele) and administration of cortisol on cellular proliferation and apoptosis in the epidermis of common carp Cyprinus carpio (L.) skin. Journal of Fish Diseases 23, 173–184.CrossRefGoogle Scholar
WENDELAAR BONGA, S. E. ( 1997). The stress response in fish. Physiological Reviews 77, 591–625.CrossRefGoogle Scholar
WEYTS, F. A. A., FLIK, G., ROMBOUT, J. H. W. M. & VERBURG-VAN KEMENADE, B. M. L. ( 1998). Cortisol induces apoptosis in activated B cells, not in other lymphoid cells of the common carp, Cyprinus carpio L. Developmental and Comparative Immunology 22, 551–562.CrossRefGoogle Scholar
WOO, P. T. K. & SHARIFF, M. ( 1990). Lernaea cyprinacea L. (Copepoda: Caligidea) in Helostoma temminicki Cuvier & Valenciennes: the dynamics of resistance in recovered and naive fish. Journal of Fish Diseases 13, 485–493.Google Scholar