Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-31T22:54:11.640Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish

Published online by Cambridge University Press:  06 August 2004

A. KARVONEN ,
O. SEPPÄLÄ  and
E. T. VALTONEN
A. KARVONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä
O. SEPPÄLÄ
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper examines the efficiency of acquired resistance in protecting the fish host, rainbow trout (Oncorhynchus mykiss), against the trematode parasite Diplostomum spathaceum, and the hypothesis that fish recognize areas where infective stages are aggregated and show avoidance behaviour. We found that when fish with a low level of infection were held in restricted cages in natural conditions they became infected and developed cataracts as a result of this infection. This suggests that acquired resistance is insufficient in protecting fish against the parasite or the deleterious effects of infection in conditions where fish could not avoid the parasite. Behavioural experiments in the laboratory showed that fish reacted to the parasite cercariae by avoiding the infection source, which decreased the rate of parasite establishment. We conclude that by using a combination of behavioural avoidance and physiological resistance, fish could defend against the parasite more effectively.

Keywords

acquired resistancelife-historyDiplostomum spathaceumOncorhynchus mykisscercariaeTrematoda
Type
Research Article
Information
Parasitology , Volume 129 , Issue 2 , August 2004 , pp. 159 - 164
Copyright
2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ALTIZER, S. M., OBERHAUSER, K. S. & BROWER, L. P. (2000). Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Entomology 25, 125–139.CrossRefGoogle Scholar
BORTZ, B. M., KENNY, G. E., PAULEY, G. B., GARCIA-ORTIGOZA, E. & ANDERSON, D. P. (1984). The immune response in immunized and naturally infected rainbow trout (Salmo gairdneri) to Diplostomum spathaceum as detected by enzyme-linked immunosorbent assay (ELISA). Developmental and Comparative Immunology 8, 813–822.CrossRefGoogle Scholar
BUCHMANN, K. & ULDAL, A. (1994). Effects of eyefluke infections on the growth of rainbow trout (Oncorhynchus mykiss) in a mariculture system. Bulletin of the European Association of Fish Pathologists 14, 104–107.Google Scholar
BURROUGH, R. J. (1978). The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata in roach and rudd. Journal of Fish Biology 13, 19–32.CrossRefGoogle Scholar
CROWDEN, A. E. & BROOM, D. M. (1980). Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28, 287–294.CrossRefGoogle Scholar
FOLSTAD, I., NILSSEN, A. C., HALVORSEN, O. & ANDERSEN, J. (1991). Parasite avoidance – the cause of post-calving migrations in reindeer. Canadian Journal of Zoology 69, 2423–2429.CrossRefGoogle Scholar
HART, B. L. (1994). Behavioural defence against parasites – interaction with parasite invasiveness. Parasitology 109 (Suppl.), S139–S151.Google Scholar
HART, B. L. (1997). Behavioural defence. In Host–Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. & Moore, J.), pp. 59–77. Oxford University Press, Oxford.
HUTCHINGS, M. R., KYRIAZAKIS, I., ANDERSON, D. H., GORDON, I. J. & COOP, R. L. (1998). Behavioural strategies used by parasitized and non-parasitized sheep to avoid ingestion of gastro-intestinal nematodes associated with faeces. Animal Science 67, 97–106.CrossRefGoogle Scholar
HÖGLUND, J. & THUVANDER, A. (1990). Indications of non-specific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 91–97.CrossRefGoogle Scholar
KARVONEN, A., HUDSON, P. J., SEPPÄLÄ, O. & VALTONEN, E. T. (2004 a). Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92, 183–188.Google Scholar
KARVONEN, A., KIRSI, S., HUDSON, P. J. & VALTONEN, E. T. (2004 b). Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 00–00.Google Scholar
KARVONEN, A., PAUKKU, S., VALTONEN, E. T. & HUDSON, P. J. (2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217–224.CrossRefGoogle Scholar
LAITINEN, M., SIDDALL, R. & VALTONEN, E. T. (1996). Bioelectronic monitoring of parasite-induced stress in brown trout and roach. Journal of Fish Biology 48, 228–241.CrossRefGoogle Scholar
MANNING, M. J. (1994). Chapter title needed. In Immunology. A Comparative Approach (ed. Turner, R. J.), pp. 69–100. John Wiley and Sons, Chichester.
MOORE, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford.
OWEN, S. F., BARBER, I. & HART, P. J. B. (1993). Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 42, 803–806.Google Scholar
PENNYCUICK, L. (1971). Differences in the parasite infections in three-spined sticklebacks (Gasterosteus aculeatus L.) of different sex, age and size. Parasitology 63, 407–418.Google Scholar
POULIN, R., MARCOGLIESE, D. J. & McLAUGHLIN, J. D. (1999). Skin-penetrating parasites and the release of alarm substances in juvenile rainbow trout. Journal of Fish Biology 55, 47–53.CrossRefGoogle Scholar
SEPPÄLÄ, O., KARVONEN, A. & VALTONEN, E. T. (2004). Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behaviour (in the Press).CrossRefGoogle Scholar
SHARIFF, M., RICHARDS, R. H. & SOMMERVILLE, C. (1980). The histopathology of acute and chronic infections of rainbow trout Salmo gairdneri Richardson with eye flukes, Diplostomum spp. Journal of Fish Diseases 3, 455–465.CrossRefGoogle Scholar
SHELDON, B. C. & VERHULST, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle Scholar
STABLES, J. N. & CHAPPELL, L. H. (1986). Putative immune response of rainbow trout, Salmo gairdneri, to Diplostomum spathaceum infections. Journal of Fish Biology 29, 115–122.CrossRefGoogle Scholar
SWEETING, R. A. (1974). Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.CrossRefGoogle Scholar
TURNER, R. J. (1994). In Immunology. A Comparative Approach (ed. Turner, R. J.), pp. 173–213. John Wiley and Sons, Chichester.
VÄYRYNEN, T., SIDDALL, R., VALTONEN, E. T. & TASKINEN, J. (2000). Patterns of trematode parasitism in lymnaeid snails from northern and central Finland. Annales Zoologici Fennici 37, 189–199.Google Scholar
WAKELIN, D. (1996). Immunity to Parasites. How Parasitic Infections Are Controlled. Cambridge University Press, Cambridge.
WHYTE, S. K., ALLAN, J. C., SECOMBES, C. J. & CHAPPELL, L. H. (1987). Cercariae and diplostomules of Diplostomum spathaceum (Digenea) elicit an immune response in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology 31, 185–190.CrossRefGoogle Scholar
WHYTE, S. K., CHAPPELL, L. H. & SECOMBES, C. J. (1989). Cytotoxic reactions of rainbow trout, Salmo gairdneri Richardson, macrophages for larvae of the eye fluke Diplostomum spathaceum (Digenea). Journal of Fish Biology 35, 333–345.CrossRefGoogle Scholar
WHYTE, S. K., CHAPPELL, L. H. & SECOMBES, C. J. (1990). Protection of rainbow trout, Oncorhynchus mykiss (Richardson), against Diplostomum spathaceum (Digenea): the role of specific antibody and activated macrophages. Journal of Fish Diseases 13, 281–291.CrossRefGoogle Scholar
WILSON, K., BJØRNSTAD, O. N., DOBSON, A. P., MERLER, S., POGLAYEN, G., RANDOLPH, S. E., READ, A. F. & SKORPING, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford.
ZUK, M. & STOEHR, A. M. (2002). Immune defence and host life history. American Naturalist 160, S9–S22.CrossRefGoogle Scholar