Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T07:59:54.016Z Has data issue: false hasContentIssue false
  • English
  • Français

Eye fluke-induced cataracts in natural fish populations: is there potential for host manipulation?

Published online by Cambridge University Press:  27 August 2010

O. SEPPÄLÄ ,
A. KARVONEN  and
E. T. VALTONEN
O. SEPPÄLÄ*
Affiliation:
EAWAG, Swiss Federal Institute of Aquatic Science and Technology, and ETH-Zürich, Institute of Integrative Biology, Überlandstrasse 133, PO Box 611, CH-8600, Dübendorf, Switzerland
A. KARVONEN
Affiliation:
Department of Biological and Environmental Science, Centre of Excellence in Evolutionary Research, PO Box 35, FIN-40014, University of Jyväskylä, Finland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, PO Box 35, FIN-40014, University of Jyväskylä, Finland
*
*Corresponding author: EAWAG, Swiss Federal Institute of Aquatic Science and Technology, and ETH-Zürich, Institute of Integrative Biology, Überlandstrasse 133, PO Box 611, CH-8600, Dübendorf, Switzerland. Tel: +41 44 823 5348. Fax: +41 44 823 50 28. E-mail: otto.seppaelae@eawag.ch
Get access Rights & Permissions [Opens in a new window]

Summary

Manipulation of host phenotype (e.g. behaviour, appearance) is suggested to be a common strategy to enhance transmission in trophically transmitted parasites. However, in many systems, evidence of manipulation comes exclusively from laboratory studies and its occurrence in natural host populations is poorly understood. Here, we examined the potential for host manipulation by Diplostomum eye flukes indirectly by quantifying the physiological effects of parasites on fish. Earlier laboratory studies have shown that Diplostomum infection predisposes fish to predation by birds (definitive hosts of the parasites) by reducing fish vision through cataract formation. However, occurrence of cataracts and the subsequent potential for host manipulation in natural fish populations has remained poorly explored. We studied the occurrence of eye fluke-induced cataracts from 7 common fish species (Gymnocephalus cernuus, Rutilus rutilus, Leuciscus leuciscus, Alburnus alburnus, Osmerus eperlanus, Coregonus lavaretus and Gasterosteus aculeatus) from the Bothnian Bay in the Baltic Sea. We found that the parasite-induced cataracts were common in fish and they also reached high levels which are likely to predispose fish to predation. However, we observed such cataracts only in species with the highest parasite abundances, which suggests that only certain hosts may be strongly affected by the infection.

Keywords

Diplostomumparasite–host interactionsparasite transmissionpredationTrematoda
Type
Research Article
Information
Parasitology , Volume 138 , Issue 2 , February 2011 , pp. 209 - 214
Copyright
Copyright © Cambridge University Press 2010

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

Bethel, W. M. and Holmes, J. C. (1973). Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59, 945–956.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.CrossRefGoogle Scholar
Bjerkås, E. and Sveier, H. (2004). The influence of nutritional and environmental factors on osmoregulation and cataracts in Atlantic salmon (Salmo salar L). Aquaculture 235, 101–122.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, 438–453.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, 575–583.CrossRefGoogle Scholar
Crowden, A. E. and Broom, D. M. (1980). Effects of eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28, 287–294.CrossRefGoogle Scholar
Galazzo, D. E., Dayanandan, D., Marcogliese, D. J. and McLaughlin, J. D. (2002). Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNAsequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
Gibson, D. I. (1996). Trematoda. In Guide to the Parasites of Fishes of Canada, Part IV (ed. Margolis, L. and Kabata, Z.), pp. 1–373. Canadian Special Publication of Fisheries and Aquatic Sciences No. 124. NRC Press, Ottawa, Canada.Google Scholar
Holmes, J. C. (1979). Parasite populations and host community structure. In Host–Parasite Interfaces (ed. Nickol, B. B.), pp. 27–46. Academic Press, London, UK.Google Scholar
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. 123–149. Academic Press, London, UK.Google Scholar
Karvonen, A. and Seppälä, O. (2008). Eye fluke infection and lens size reduction in fish: a quantitative analysis. Diseases of Aquatic Organisms 80, 21–26.CrossRefGoogle ScholarPubMed
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, 473–478.CrossRefGoogle ScholarPubMed
Karvonen, A., Seppälä, O. and Valtonen, E. T. (2004 b). Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129, 159–164.CrossRefGoogle ScholarPubMed
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts’ behaviour by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Morris, K. (1996). Altered behaviour of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.CrossRefGoogle Scholar
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Misse, D., Poulin, R. and Thomas, F. (2009). The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 41–48.CrossRefGoogle ScholarPubMed
Locke, S. A., McLaughlin, J. D., Dayanandan, S. and Marcogliese, D. J. (2010). Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 40, 333–343.CrossRefGoogle ScholarPubMed
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, 355–369.CrossRefGoogle 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, 121–131.Google Scholar
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–1015.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Mouritsen, K. M. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.CrossRefGoogle ScholarPubMed
Rothschild, M. (1962). Changes in behaviour in the intermediate hosts of trematodes. Nature, London 193, 1312–1313.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
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 177, 597–610.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, 257–263.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, 895–900.CrossRefGoogle 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, 889–894.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2008 b). Shoaling behaviour of fish under parasitism and predation risk. Animal Behaviour 75, 145–150.CrossRefGoogle Scholar
Seppälä, O., Valtonen, E. T. and Benesh, D. P. (2008 a). Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society of London, B 275, 1611–1615.Google ScholarPubMed
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, 47–59.Google Scholar
Wall, T. and Bjerkås, E. (1999). A simplified method of scoring cataracts in fish. Bulletin of the European Association of Fish Pathologists 19, 162–165.Google Scholar
Wilson, K., Grenfell, B. T. and Shaw, D. J. (1996). Analysis of aggregated parasite distribution: a comparison of methods. Functional Ecology 10, 592–601.CrossRefGoogle Scholar