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Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years

Published online by Cambridge University Press:  28 November 2001

C. R. KENNEDY ,
P. C. SHEARS  and
J. A. SHEARS
C. R. KENNEDY
Affiliation:
School of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS
P. C. SHEARS
Affiliation:
School of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS
J. A. SHEARS
Affiliation:
School of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS
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Abstract

Data are presented on 2 full epizootic cycles and the start of a third of Ligula intestinalis in roach Rutilus rutilus in a small lake, and the relationships of these cycles to the densities of rudd, Scardinius erythrophthalmus, and Great Crested Grebes, Podiceps cristatus, over 31 years. The parasite was introduced to the lake by P. cristatus in 1973 at a time when the roach population had increased in response to eutrophication to a level at which individual fish growth was stunted and the hithero dominant rudd population had declined in numbers as a consequence of inter-specific competition with roach. Ligula prevalence peaked at 28% in only 2 years: thereafter parasite-induced host mortality caused a decline in the roach population, releasing fish from stunting and allowing the rudd population to recover. The consequent improved growth of roach individuals and their short life-span reduced Ligula transmission rates and prevalence levels declined to approximately 1% although Ligula nevertheless persisted for a further 10 years. Following a massive winter-kill of the fish populations in 1984–1985, fish and Ligula numbers declined to barely detectable levels and the parasite disappeared from samples. Rudd recovered first, then roach and interspecific competition again led to a decline in rudd numbers. This increase in roach numbers led to a decrease in roach growth rates, which coincided with the re-colonization of the lake by Ligula. This second epizootic of Ligula peaked within 2 years in 1991–1992, when up to 78% of roach were infected with a maximum abundance of 2.2 parasites and intensity of 21 parasites. Heavy parasite-induced mortality of roach led to a decline in numbers, an improvement in individual growth rate and a reduction of Ligula transmission rates such that the epizootic died out in 1996. Similar conditions of roach numbers and growth prevailed at the start of a third cycle in 1998. The course of events over the second cycle was so similar to that of the first that it confirms the interpretations of that cycle. Comparison with other localities shows that epizootics of Ligula always coincide with rapid increases in roach numbers, for whatever cause, and stunted growth, which together attract piscivorous birds. At the start of a cycle Ligula is a major determinant of the population dynamics of the roach, but at the end of the cycle the fish population dynamics determine those of the parasite. The cycles are not regulated and the roach–Ligula system is inherently unstable.

Keywords

Ligulapopulation cycleshost–parasite systemslong-term dynamicsepizooticsinstability
Type
Research Article
Information
Parasitology , Volume 123 , Issue 3 , March 2001 , pp. 257 - 269
Copyright
© 2002 Cambridge University Press

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References

ANDERSON, R. M. & MAY, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
ARME, C. (1975). Tapeworm–host interactions. Symposia of the Society for Experimental Biology 29, 505–532.Google Scholar
ARME, C. (1997). Ligula intestinalis: interactions with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 83–84.CrossRefGoogle Scholar
ARME, C. & OWEN, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fishes. Journal of Parasitology 54, 272–280.CrossRefGoogle Scholar
BAUER, O. N. & STOLYAROV, V. P. (1961). Formation of the parasite fauna and parasitic diseases of fish in hydro-electric reservoirs. In Parasitology of Fishes (ed. DOGIEL, V. A. PETRUSHEVSKI, G. K. & POLYANSKI, Y. I.), pp. 246–254. Oliver and Boyd, London.
BEAN, C. W. & WINFIELD, I. J. (1992). Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Netherlands Journal of Zoology 42, 416–429.Google Scholar
BLACK, G. A. & FRASER, J. M. (1984). Dynamics of Ligula intestinalis (L.) in Catastomus commersoni (Lacépède). Journal of Fish Biology 25, 139–146.Google Scholar
BURROUGH, R. J. & KENNEDY, C. R. (1979). The occurrence and natural alleviation of stunting in a population of roach, Rutilus rutilus (L.). Journal of Fish Biology 15, 93–109.CrossRefGoogle Scholar
BURROUGH, R. J., BREGAZZI, P. R. & KENNEDY, C. R. (1979). Interspecific dominance amongst three species of coarse fish in Slapton Ley, Devon. Journal of Fish Biology 15, 535–544.CrossRefGoogle Scholar
BURT, T. P. & HEATHWAITE, A. L. (1996). The hydrology of the Slapton catchments. Field Studies 8, 543–557.Google Scholar
BUSH, A. O., LAFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
DIAMOND, J. M. (1975). Assembly of species communities. In Ecology and Evolution of Communities (ed. CODY, M. L. & DIAMOND, J. M.), pp. 342–444. Belknap Press of Harvard University Press, Cambridge, Massachusetts and, London.
DOBSON, A. P. (1988). The population biology of parasite-induced changes in host behaviour. Quarterly Review of Biology 63, 139–165.CrossRefGoogle Scholar
DUBININA, M. N. (1980). Tapeworms, (Cestoda, Ligulidae) of the Fauna of the USSR. Amerind Publishing Co. Ltd, New Delhi.
ELPHICK, D. (1996). A review of 35 years of bird-ringing at Slapton Ley (1961–1995) together with a brief historical review of ornithological observations. Field Studies 8, 699–725.Google Scholar
ESCH, G. W., HAZEN, T. C., MARCOGLIESE, D. J., GOATER, T. M. & CREWS, A. E. (1986). A long term study on the population biology of Crepidostomum cooperi (Trematoda: Allocreadidae) in the burrowing mayfly Hexagenia limbata (Ephemeroptera). American Midland Naturalist 116, 304–314.CrossRefGoogle Scholar
HARRIS, M. T. & WHEELER, A. (1974). Ligula infection of bleak Alburnus alburnus (L.) in the Tidal Thames. Journal of Fish Biology 6, 181–188.CrossRefGoogle Scholar
HOLMES, J. C. & BETHEL, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. W. & Wright, C. A.). Journal of the Linnean Society 51, Suppl. 1, 123–149.Google Scholar
HOOLE, D. (1994). Tapeworm infections in fish: past and future problems. In Parasitic Diseases of Fish (ed. PIKE, A. W. & LEWIS, J. W.), pp. 119–140. Samara Publishing Ltd, Tresaith, Dyfed.
IZYUMOVA, N. A. (1987). Parasitic Fauna of Reservoir Fishes of the USSR and its Evolution. Amerind Publishing Co. Pvt. Ltd, New Delhi.
KEMPE, E. O. (1962). The growth of the roach (Leuciscus rutilus L.) in some Swedish lakes. Report of the Institute of Freshwater Research, Drottnigholm 44, 42–104.Google Scholar
KENNEDY, C. R. (1985). Interactions of fish and parasite populations: to perpetuate or pioneer? In Ecology and Genetics of Host–Parasite Interactions (ed. ROLLINSON, D. & ANDERSON, R. M.), pp. 1–20. Linnean Society Symposium Series 11. Academic Press, London.
KENNEDY, C. R. (1993). The dynamics of intestinal helminth communities in eels Anguilla anguilla in a small stream: long-term changes in richness and structure. Parasitology 107, 71–78.CrossRefGoogle Scholar
KENNEDY, C. R. (1996). The fish of Slapton Ley. Field Studies 8, 685–697.Google Scholar
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, 267–273.Google Scholar
KENNEDY, C. R. (1998). Aquatic birds as agents of parasite dispersal: a field test of the effectiveness of helminth colonisation strategies. Bulletin of the Scandinavian Society for Parasitology 8, 23–28.Google Scholar
KENNEDY, C. R. (2001). Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis. Parasitology 122, Suppl. 1 S13–S22.CrossRefGoogle Scholar
KENNEDY, C. R. & BURROUGH, R. J. (1981). The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilus rutilus (L.). Journal of Fish Biology 19, 105–126.CrossRefGoogle Scholar
KENNEDY, C. R. & RUMPUS, A. (1977). Long term changes in the size of the Pomphorhynchus laevis (Acanthocephala) population in the River Avon. Journal of Fish Biology 10, 35–42.CrossRefGoogle Scholar
KENNEDY, C. R., WYATT, R. J. & STARR, K. (1994). The decline and natural recovery of an unmanaged coarse fishery in relation to changes in land use and attendant eutrophication. In Rehabilitation of Freshwater Fisheries (ed. COWX, I. G.), pp. 366–375. Fishing News Books, Oxford.
KERR, T. (1948). The pituitary in normal and parasitised roach (Leuciscus rutilus Flemm.). Quarterly Journal of Microscopical Science 89, 129–137.Google Scholar
MAY, R. M. & ANDERSON, R. M. (1978). Regulation and stability of host-parasite population interactions, II. Destabilizing processes. Journal of Animal Ecology 47, 249–267.CrossRefGoogle Scholar
MOORE, D. E. & BROWN, D. J. A. (1975). The decline in populations of bleak (A. alburnus) in some fenland rivers. Proceedings of the 7th British Coarse Fish Conference, 43–49.Google Scholar
MORRISON, B. R. S. (1977). Observations on the tapeworm (Ligula intestinalis) a parasite of roach (Rutilus rutilus) in the Lake of Menteith, Perthshire. Proceedings of the 8th British Coarse Fish Conference, 101–107.Google Scholar
ORR, T. S. C. (1966). Spawning behaviour of rudd Scardinius erythophthalmus infested with plerocercoids of Ligula intestinalis. Nature, London 212, 736.CrossRefGoogle Scholar
SMITH, H. D. (1973). Observations on the cestode Eubothrium salvelini in juvenile sockeye salmon (Onchorhynchus nerka) at Babine of Lake, British Columbia. Journal of the Fisheries Research Board of Canada 30, 947–964.CrossRefGoogle Scholar
SWEETING, R. A. (1976). Studies on Ligula intestinalis. Effects on a roach population in a gravel pit. Journal of Fish Biology 9, 515–522.Google Scholar
SWEETING, R. A. (1977). Studies on Ligula intestinalis. Some aspects of the pathology in the second intermediate host. Journal of Fish Biology 10, 43–50.Google Scholar
TAYLOR, N. & HOOLE, D. (1989). Ligula intestinalis (L.) (Cestoda: Pseudophyllidea): pleroceroid-induced changes in the spleen and pronephros of roach, Rutilus rutilus (L.) and gudgeon Gobio gobio (L.). Journal of Fish Biology 34, 583–596.Google Scholar
TINSLEY, R. C. (1999). Parasite adaptation to extreme conditions in a desert environment. Parasitology 119 (Suppl.), S31–S56.Google Scholar
TOBIN, C. (1986). A record of Ligula intestinalis (L.) (Cestoda) from roach (Rutilus rutilus (L.)) in Lough Neagh. Irish Naturalists' Journal 22, 78.Google Scholar
VAN DOBBEN, W. H. (1952). The food of the cormorant in the Netherlands. Ardea 40, 1–63.Google Scholar
WILSON, R. S. (1971). The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129–137.Google Scholar
WINFIELD, I. J., WINFIELD, D. K. & TOBIN, C. M. (1992). Interactions between the roach, Rutilus rutilus, and waterfowl populations of Lough Neagh, Northern Ireland. Environmental Biology of Fishes 33, 207–214.CrossRefGoogle Scholar
WYATT, R. J. (1988). The cause of extreme year class variation in a population of roach, Rutilus rutilus (L.), from a eutrophic lake in southern England. Journal of Fish Biology 32, 409–421.Google Scholar
WYATT, R. J. & KENNEDY, C. R. (1988). The effects of a change in the growth rate of roach, Rutilus rutilus (L.) on the population biology of the fish tapeworm Ligula intestinalis (L.). Journal of Fish Biology 33, 45–57.Google Scholar
WYATT, J. & KENNEDY, C. R. (1989). Host-constrained epidemiology of the fish tapeworm Ligula intestinalis (L.). Journal of Fish Biology 35, 215–227.CrossRefGoogle Scholar