Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T04:44:37.307Z Has data issue: false hasContentIssue false

Susceptibility of eye fluke-infected fish to predation by bird hosts

Published online by Cambridge University Press:  07 December 2005

O. SEPPÄLÄ
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä, Finland
A. KARVONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä, Finland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014, University of Jyväskylä, Finland

Abstract

Host manipulation by trophically transmitted parasites may predispose infected hosts to predation and in this way enhance parasite transmission. In most study systems, however, the evidence comes from laboratory studies, and therefore knowledge of the effect of manipulation on parasite transmission efficiency in the wild is still limited. Here we examined the effect of Diplostomum spathaceum (Trematoda) eye flukes on the susceptibility of fish intermediate hosts to predation by bird definitive hosts. Our earlier studies have shown that the parasite alters fish phenotype and increases their susceptibility to artificial predation under laboratory conditions. In the present field study, we allowed wild birds to feed on fish from cages placed into a lake, and found that predation vulnerability of infected fish did not differ from that of controls. However, we suggest that the experimental set-up likely affected the result because the cages allowed gulls, which caught most of the fish in the study, to feed on fish in an easy, unnatural manner by standing on the edges of the cages. Nevertheless, considerable predation was observed, which provides important initial evidence of how this question should be addressed in the wild.

Type
Research Article
Copyright
2005 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

Betterton, C. ( 1974). Studies on the host specificity of the eyefluke, Diplostomum spathaceum, in brown and rainbow trout. Parasitology 69, 1129.CrossRefGoogle Scholar
Bugoni, L. and Vooren, C. M. ( 2004). Feeding ecology of the Common Tern Sterna hirundo in a wintering area in southern Brazil. Ibis 146, 438453.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. ( 1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Chappell, L. H., Hardie, L. J. and Secombes, C. J. ( 1994). Diplostomiasis: the disease and host-parasite interactions. In Parasitic Diseases of Fish ( ed. Pike, A. W. and Lewis, J. W.), pp. 5986. Samara Publishing, Dyfed, UK.
Dobson, A. P., Hudson, P. J. and Lyles, A. M. ( 1992). Macroparasites: it's a wormy world. In Natural Enemies. The Population Biology of Predators, Parasites and Diseases ( ed. Crawley, M. J.), pp. 329348. Blackwell Scientific, Oxford.
Field, J. S., McKeown, C. A. and Irwin, S. W. B. ( 1994). A proposed standard method for the maintenance of Diplostomum spp. (Digenea: Diplostomatidae) in the laboratory. Parasitology Research 80, 253254.Google Scholar
Götmark, F. ( 1984). Food and foraging in five European Larus gulls in the breeding season: a comparative review. Ornis Fennica 61, 918.Google Scholar
Holmes, J. C. ( 1979). Parasite populations and host community structure. In Host–Parasite Interfaces ( ed. Nickol, B. B.). Academic Press, New York.
Holmes, J. C. and Bethel, W. M. ( 1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission ( ed. Canning, E. U. and Wright, C. A.), pp. 123149. Academic Press, London.
Karvonen, A., Cheng, G.-H., Seppälä, O. and Valtonen, E. T. ( 2006). Community structure and fecundity of two species of Diplostomum parasites in definitive hosts. Parasitology (in the Press).Google Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. ( 2004 a). Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473478.Google Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. ( 2004 b). Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129, 159164.Google Scholar
Lafferty, K. D. and Morris, K. ( 1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 13901397.CrossRefGoogle Scholar
Levri, E. P. and Lively, C. M. ( 1996). The effect of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum. Animal Behaviour 51, 891901.CrossRefGoogle Scholar
Manly, B. F. J. ( 1974). A model for certain types of selection experiments. Biometrics 30, 281294.CrossRefGoogle Scholar
Marcogliese, D. J., Dumont, P., Gendron, A. D., Mailhot, Y., Bergeron, E. and McLaughlin, J. D. ( 2001). Spatial and temporal variation in abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white suckers (Catostomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 79, 355369.Google Scholar
Mauco, L. and Favero, M. ( 2004). Diet of the common tern (Sterna hirundo) during the nonbreeding season in Mar Chiquita Lagoon, Buenos Aires, Argentina. Ornitologia Neotropical 15, 121131.Google Scholar
McCarthy, H. O., Fitzpatrick, S. and Irwin, S. W. B. ( 2000). A transmissible trematode affects the direction and rhythm of movement in a marine gastropod. Animal Behaviour 59, 11611166.CrossRefGoogle Scholar
Moore, J. ( 1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 10001015.CrossRefGoogle Scholar
Moore, J. ( 2002). Parasites and the Behavior of Animals. Oxford University Press, New York.
Mouritsen, K. N. and Poulin, R. ( 2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 10431050.CrossRefGoogle Scholar
Poulin, R. and Latham, A. M. ( 2002). Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda: Talitridae). Animal Behaviour 63, 269275.CrossRefGoogle Scholar
Rothschild, M. ( 1962). Changes in behaviour in the intermediate hosts of trematodes. Nature, London 193, 13121313.CrossRefGoogle Scholar
Rushton, W. ( 1937). Blindness in freshwater fish. Nature, London 140, 1014.CrossRefGoogle Scholar
Rushton, W. ( 1938). Blindness in freshwater fishes. Nature, London 141, 289.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. ( 2004). Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behaviour 68, 257263.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. ( 2005 a). Impaired crypsis of fish infected with a trophically transmitted parasite. Animal Behaviour 70, 895900.Google Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. ( 2005 b). Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889894.Google Scholar
Shariff, M., Richards, R. H. and 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, 455465.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, 291300.CrossRefGoogle Scholar
Thomas, F. and Poulin, R. ( 1998). Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431436.Google Scholar
Valtonen, E. T. and Gibson, D. I. ( 1997). Aspects of the biology of diplostomid metacercarial (Digenea) populations occuring in fishes in different localities of northern Finland. Annales Zoologici Fennici 34, 4759.Google Scholar
Voříšek, P., Votýpka, J., Zvára, K. and Svobodova, M. ( 1998). Heteroxenous coccidia increase the predation risk of parasitized rodents. Parasitology 117, 521524.CrossRefGoogle Scholar
Wall, T. and Bjerkås, E. ( 1999). A simplified method of scoring cataracts in fish. Bulletin of the European Association of Fish Pathologists 19, 162165.Google Scholar