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The ecology of parasites of freshwater fishes: the search for patterns

Published online by Cambridge University Press:  14 April 2009

C. R. KENNEDY*
Affiliation:
School of Biosciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS, UK
*
*Tel: +44 1308 862079. E-mail: C.R. [email protected]

Summary

Developments in the study of the ecology of helminth parasites of freshwater fishes over the last half century are reviewed. Most research has of necessity been field based and has involved the search for patterns in population and community dynamics that are repeatable in space and time. Mathematical models predict that under certain conditions host and parasite populations can attain equilibrial levels through operation of regulatory factors. Such factors have been identified in several host-parasite systems and some parasite populations have been shown to persist over long time-periods. However, there is no convincing evidence that fish parasite populations are stable and regulated since in all cases alternative explanations are equally acceptable and it appears that they are non-equilibrial systems. It has proved particularly difficult to detect replicable patterns in parasite communities. Inter-specific competition, evidenced by functional and numerical responses, has been detected in several communities but its occurrence is erratic and its significance unclear. Some studies have failed to find any nested patterns in parasite community structure and richness, whereas others have identified such patterns although they are seldom constant over space and time. Departures from randomness appear to be the exception and then only temporary. It appears that parasite communities are non-equilibrial, stochastic assemblages rather than structured and organized.

Type
Research Article
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Anderson, R. M. (1978). The regulation of host population growth by parasitic species. Parasitology 76, 119157.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite interactions: I. Regulatory processes. Journal of Animal Ecology 47, 219247.CrossRefGoogle Scholar
Andrewartha, H. A. and Birch, L. C. (1954). Distribution and Abundance of Animals. University of Chicago Press, Chicago, USA.Google Scholar
Ashworth, S. T. and Kennedy, C. R. (1999). Density-dependent effects on Angullicola crassus (Nematoda) within its European eel definitive host. Parasitology 118, 289296.CrossRefGoogle ScholarPubMed
Bates, R. M. and Kennedy, C. R. (1990). Interactions between the acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae in rainbow trout: testing an exclusion hypothesis. Parasitology 100, 435444.CrossRefGoogle ScholarPubMed
Brown, A. F. (1986). Evidence for density-dependent establishment and survival of Pomphorhynchus laevis (Muller, 1776) (Acanthocephala) in laboratory-infected Salmo gairdneri Richardson and its bearing on wild populations in Leuciscus cephalus (L.). Journal of Fish Biology 28, 659669.CrossRefGoogle Scholar
Bush, A. O., Aho, J. M. and Kennedy, C. R. (1990). Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4, 120.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostack, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Bush, A. O., Fernández, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism. The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Byrne, C. J., Holland, C. V., Kennedy, C. R. and Poole, W. R. (2003). Interspecific interactions between Acanthocephala in the intestine of brown trout: are they more frequent in Ireland? Parasitology 127, 399409.CrossRefGoogle ScholarPubMed
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill). Canadian Journal of Zoology 78, 538555.CrossRefGoogle Scholar
Chappell, L. H. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775778.CrossRefGoogle Scholar
Choudhury, A. and Dick, T. A. (2000). Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. Journal of Biogeography 27, 935956.CrossRefGoogle Scholar
Crofton, H. D. (1971 a). A quantitative approach to parasitism. Parasitology 62, 179193.CrossRefGoogle Scholar
Crofton, H. D. (1971 b). A model of host-parasite relationships. Parasitology 63, 343364.CrossRefGoogle Scholar
Dezfuli, B. S., Giari, L., DeBiaggi, S. and Poulin, R. (2001). Association and interactions among intestinal helminths of the brown trout, Salmo trutta, in northern Italy. Journal of Helminthology 75, 331336.CrossRefGoogle ScholarPubMed
Diamond, J. M. (1975). Assembly of species communities. In Ecology and Evolution of Communities (ed. Cody, M. L. and Diamond, J. M.), pp. 342444. Belknap Press of Harvard University Press, Cambridge, MA, USA.Google Scholar
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 66, 317347.CrossRefGoogle Scholar
Dogiel, V. A. (1961). Ecology of the parasites of freshwater fishes. In Parasitology of Fishes (ed. Dogiel, V. A., Petrushevski, G. K. and Polyanski, Yu. I.), pp. 147. Oliver and Boyd, Edinburgh and London, UK.Google Scholar
Dogiel, V. A. (1964). General Parasitology. Oliver and Boyd, Edinburgh and London, UK.Google Scholar
Dogiel, V. A., Petrushevski, G. K. and Polyanski, YU. I. (1961). Parasitology of Fishes. Oliver and Boyd, Edinburgh and London, UK.Google Scholar
Dove, A. D. M. and Fletcher, A. S. (2000). The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. Journal of Helminthology 74, 121127.CrossRefGoogle ScholarPubMed
Esch, G. W., Kennedy, C. R., Bush, A. O. and Aho, J. M. (1988). Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonisation. Parasitology 96, 519532.CrossRefGoogle Scholar
Fazio, G., Sasal, P., Da Silva, C., Furnet, B., Boissier, J., Lecompte-Finiger, R. and Moné, H. (2008). Regulation of Anguillicola crassus (Nematoda) infrapopulations in their definitive host the European eel, Anguilla anguilla. Parasitology 135, 17071716.CrossRefGoogle ScholarPubMed
Font, W. F. (1998). Parasites in paradise: patterns of helminth distribution in Hawaiian stream fishes. Journal of Helminthology 72, 307311.CrossRefGoogle ScholarPubMed
Grey, A. J. and Hayunga, E. G. (1980). Evidence for alternative site selection by Glaridacris laruei (Cestoidea: Caryophyllidea) as a result of intespecific competition. Journal of Parasitology 66, 371372.CrossRefGoogle Scholar
Guégan, J.-F. and Kennedy, C. R. (1993). Maximum local helminth parasite community richeness in British freshwater fish: a test of the colonisation time hypothesis. Parasitology 106, 91–100.CrossRefGoogle Scholar
Holmes, J. C. (1973). Site segregation by parasitic helminths: interspecific I interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333347.CrossRefGoogle Scholar
Holmes, J. C. (1982). Impact of infectious disease agents on the population growth and geographical distribution of animals. In Population Biology of Infectious Diseases (ed. Anderson, R. M. and May, R. M.). pp. 3751. Dahlem Konferenzem. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. Kikkawa, J. and Andersen, D. J.), pp. 187213. Blackwell Scientific Publications, Carlton, Victoria, Australia.Google Scholar
Holmes, J. C., Hobbs, R. P. and Leong, T. S. (1977). Populations in persepective: community organisation and regulation of parasites populations. In Regulation of Parasite Populations (ed. Esch, G. W.), pp. 209245. Academic Press, New York, USA.Google Scholar
Karvonen, A., Bagge, A. M. and Valtonen, E. T. (2007). Inter-specific and intra-specific interactions in the monogenean communities of fish: a question of study scale? Parasitology 134, 12371242.CrossRefGoogle Scholar
Kennedy, C. R. (1970). The population biology of helminths of British freshwater fish. In Aspects of Fish Parasitology (ed. Taylor, A. E. R. and Muller, R.), pp. 145159. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Kennedy, C. R. (1976). Reproduction and dispersal. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.), pp. 143160. North Holland Publishing Company, Amsterdam, The Netherlands.Google Scholar
Kennedy, C. R. (1990). Helminth communities in freshwater fish: structured communities or stochastic assemblages? In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 131156. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Kennedy, C. R. (1993). The dynamics of helminth communities in eels Anguilla anguilla in a small stream: long term changes in richness and structure. Parasitology 107, 7178.CrossRefGoogle Scholar
Kennedy, C. R. (1994). The ecology of introductions. In Parasitic Diseases of Fish (ed. Pike, A. W. and Lewis, J. W.), pp. 189208. Samara Publishing Ltd, Tresaith, UK.Google Scholar
Kennedy, C. R. (1995). Richness and diversity of macroparasite communities in tropical eels Anguilla reinhardtii in Queensland, Australia. Parasitology 111, 233245.CrossRefGoogle Scholar
Kennedy, C. R. (1996). Establishment, survival and site selection of the cestode Eubothrium crassum in brown trout Salmo trutta. Parasitology 112, 347355.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (1997). Long-term and seasonal changes in composition and richness of intestinal helminth communities in eels Anguilla anguilla of an isolated English river. Folia Parasitologica 44, 267273.Google ScholarPubMed
Kennedy, C. R. (2001 a). Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis. Parasitology 122, S13S22.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (2001 b). Metapopulation and community dynamics of helminth parasites of eels Anguilla anguilla in the River Exe system. Parasitology 122, 689698.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Bush, A. O. (1992). Species richness in helminth communities: the importance of multiple congeners. Parasitology 104, 189197.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Bush, A. O. (1994). The relationship between pattern and scale in parasite communities: a stranger in an strange land. Parasitology 109, 187196.CrossRefGoogle Scholar
Kennedy, C. R. and Guégan, J.-F. (1994). Regional versus local helminth parasite species richness in British freshwater fish: saturated or unsaturated parasite communities? Parasitology 109, 187196.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Guégan, J.-F. (1996). The number of niches in intestinal communities of Anguilla anguilla: are there enough spaces for parasites? Parasitology 113, 293302.CrossRefGoogle Scholar
Kennedy, C. R. and Moriarty, C. (2002). Long-term stability in the richness and structure of helminth communities in eels, Anguilla anguilla, in Lough Derg, River Shannon, Ireland. Journal of Helminthology 76, 315322.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Rumpus, A. (1977). Long term changes in the size of the Pomphorhynchus laevis (Acanthocephala) population in the River Avon. Journal of Fish Biology 10, 3542.CrossRefGoogle Scholar
Kennedy, C. R., Bush, A. O. and Aho, J. M. (1986). Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205215.CrossRefGoogle ScholarPubMed
Kennedy, C. R., Shears, P. C. and Shears, J. A. (2001). Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizooitc cycles over thirty one years. Parasitology 123, 257269.CrossRefGoogle ScholarPubMed
Kikkawa, J. and Anderson, D. J. (1986). Community Ecology. Blackwell Scientific Publications, Carlton, Victoria, Australia.Google Scholar
Lawton, J. H. (1999). Are there general laws in ecology? Oikos 84, 177192.CrossRefGoogle Scholar
MacArthur, R. H. (1972). Geographical Ecology: Patterns in the Distribution of Species. Harper and Row, New York, USA.Google Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, USA.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1998). Comparison of richness and diversity of macroparasite communities among eels from Nova Scotia, the United Kingdom and Australia. Parasitology 116, 7383.CrossRefGoogle ScholarPubMed
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite interactions: II Destabilising processes. Journal of Animal Ecology 47, 249268.CrossRefGoogle Scholar
Mouillot, D., George-Nascimento, M. and Poulin, R. (2003). How parasites divide resources: a test of the niche apportionment hypothesis. Journal of Animal Ecology 72, 757764.CrossRefGoogle Scholar
Mouillot, D., George-Nascimento, M. and Poulin, R. (2005). Richness, structure and functioning in metazoan parasite communities. Oikos 109, 447460.CrossRefGoogle Scholar
Munoz, S. A. and George-Nascimento, M. (2008). The effects of Anonchocephalus chilensis Riggenbach (Eucestoda: Bothriocephalidae) on infracommunity patterns in Genypterus maculatus Tschudi (Osteichthyes: Ophidiidae). Journal of Helminthology 82, 221226.CrossRefGoogle Scholar
Norton, J., Lewis, J. W. and Rollinson, D. (2004 a). Temporal and spatial patterns of nestedness in eel macroparasite communities. Parasitology 129, 203211.CrossRefGoogle ScholarPubMed
Norton, J., Rollinson, D. and Lewis, J. W. (2004 b). Patterns of infracommunity richness in eels, Anguilla anguilla. Journal of Helminthology 78, 141146.CrossRefGoogle ScholarPubMed
O' Mahony, E. M., Bradley, D. G., Kennedy, C. R. and Holland, C. V. (2004). Evidence for the hypothesis of strain formation in Pomphorhynchus laevis (Acanthocephala): an investigation using DNA sequences. Parasitology 129, 341347.CrossRefGoogle ScholarPubMed
Poulin, R. (2001 a). Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.CrossRefGoogle ScholarPubMed
Poulin, R. (2001 b). Another look at the richness of helminth communities in tropical freshwater fish. Journal of Biogeography 28, 737743.CrossRefGoogle Scholar
Poulin, R. (2007 a). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Poulin, R. (2007 b). Are there general laws in parasite ecology? Parasitology 134, 763776.CrossRefGoogle ScholarPubMed
Poulin, R. and Guégan, J.-F. (2000). Nestedness, anti-nestedness and the relationship between prevalence and intensity in ectoparasite assemblages of marine fish: a spatial model of species coexistence. International Journal for Parasitology 30, 11471152.CrossRefGoogle Scholar
Poulin, R. and Luque, J. L. (2003). A general test of the interactive-isolationist continuum in gastrointestinal parasite communities of fish. International Journal for Parasitology 33, 16231630.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (1999). Geographical distances and the similarity amongst parasite communities of conspecific host populations. Parasitology 119, 369374.CrossRefGoogle Scholar
Poulin, R. and Morand, S. (2000). The diversity of parasites. Quarterly Review of Biology 75, 277293.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. T. (2001). Nested assemblages resulting from host size variation: the case of endoparasitic communities in fish hosts. International Journal for Parasitology 31, 11941204.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. T. (2002). The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. International Journal for Parasitology 32, 12351243.CrossRefGoogle ScholarPubMed
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, USA.Google ScholarPubMed
Price, P. W. (1984). Communities of specialists: vacant niches in ecological and evolutionary time. In Ecological Communities (ed. Strong, D. R., Simberloff, D., Abele, L. G. and Thistle, A. B.), pp. 510523. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Rohde, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648671.CrossRefGoogle Scholar
Rohde, K. (1994). Niche restriction in parasites: proximate and ultimate causes. Parasitology 109, 569584.CrossRefGoogle ScholarPubMed
Rohde, K. (2005). Nonequilibrium Ecology. Cambridge University Press, Cambridge, UK.Google Scholar
Salgado-Maldonado, G. and Kennedy, C. R. (1997). Richness and diversity of helminth communities in a tropical cichlid fish in Mexico. Parasitology 114, 581590.Google Scholar
Šimková, A., Sasal, P., Kadlec, D. and Gelnar, M. (2001). Water temperature influencing dactylogyrid species communities in roach, Rutilus rutilus, in the Czech Republic. Journal of Helminthology 75, 373383.CrossRefGoogle ScholarPubMed
Smith, H. D. (1973). Observations on the cestode Eubothrium salvelini in juvenile sockeye salmon (Onchorhynchus nerka) at Babine Lake, British Columbia. Journal of the Fisheries Research Board of Canada 30, 947964.CrossRefGoogle Scholar
Sures, B. and Streit, B. (2001). Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123, 185191.CrossRefGoogle ScholarPubMed
Sures, B., Knopf, K., Wurtz, J. and Hirt, J. (1999). Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 119, 323330.CrossRefGoogle ScholarPubMed
Takemoto, S., Pavanelli, G. C., Lizana, M. A. P., Luque, J. L. and Poulin, R. (2005). Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil. (2005). Journal of Helminthology 79, 7583.CrossRefGoogle Scholar
Taraschewski, H., Moravec, F., Lamah, T. and Anders, K. (1987). Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nematoda; Dracunculidae) and Paratenuisentis ambiguus (Acanthocephala; Teunuisentidae). Diseases of Aquatic Organisms 3, 167176.CrossRefGoogle Scholar
Timi, J. T. and Poulin, R. (2008). Different methods, different results: temporal trends in the study of nested subset patterns in parasite communities. Parasitology 135, 131138.CrossRefGoogle Scholar
Townsend, C. R., Harper, J. L. and Begon, M. (2000). Essentials of Ecology. Blackwell Science Inc., Malsen, MA, USA.Google Scholar
Uznanski, R. L. and Nickol, B. B. (1982). Site selection, growth and survival of Leptorhynchoides thecatus (Acanthocephala) during the prepatent period in Lepomis cyanellus. Journal of Parasitology 68, 686690.CrossRefGoogle Scholar
Vidal-Martinez, V. M. and Kennedy, C. R. (2000). Potential interactions between the intestinal helminths of the cichlid fish Cichlasoma synspilum from southeastern Mexico. Journal of Parasitology 86, 691695.CrossRefGoogle ScholarPubMed
Vidal-Martinez, V. M. and Poulin, R. (2003). Spatial and temporal repeatability in parasite community structure of tropical fish hosts. Parasitology 127, 387398.CrossRefGoogle ScholarPubMed