Hostname: page-component-7479d7b7d-q6k6v Total loading time: 0 Render date: 2024-07-11T18:57:15.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis

Published online by Cambridge University Press:  24 October 2011

C. R. KENNEDY
C. R. KENNEDY
Affiliation:
School of Biological Sciences, University of Exeter, Exeter EX4 4PS, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

The changes in prevalence and abundance of the three species of metacercariae in the humour of the eyes of perch Perca fluviatilis in Slapton Ley, Devon, have been monitored over a period of 29 years. Earlier studies had revealed that Diplostomum gasterostei was originally the sole occupant of this niche, but Tylodelphys clavata colonised in 1973 and T. podicipina in 1976. A decline in the number of perch with heavy infections of D. gasterostei was significantly negatively correlated with population abundance of T. clavata and a decline in recruitment rate of D. gasterostei coincided with the population increase in T. podicipina over the period 1976–1979. It was suggested that the decline in population size of D. gasterostei was due to inter-specific competition, but this hypothesis could not be tested experimentally. Subsequent investigations, reported here, confirmed the decline when the data set was extended to 1985. A severe decline in the perch population over the winter of 1984/1985 resulted in the disappearance of D. gasterostei and T. podicipina and this was followed by a slow recovery from 1990 onwards. This natural experiment provided an opportunity to test the hypothesis. Only T. clavata survived throughout the perch crash and the population continued at pre-crash levels up to 1999. Its congener T. podicipina did not re-appear until 1994 and was probably a re-introduction: it did not attain pre-crash levels until 1999. It is likely that D. gasterostei survived the crash as it re-appeared in 1991, but was confined to young of the year fish and barely approached pre-crash levels even in 1999. Its continual low levels cannot be explained by changes in the lake or in densities of snail intermediate or bird definitive hosts. New data revealed that the suspensory ligaments of the eye were the preferred site of all three species and that the eye was partitioned out between them. The data from the post-crash period do not refute but rather confirm earlier conclusions that inter-specific competition is responsible for the decline in D. gasterostei and this remains the preferred hypothesis.

Keywords

Metacercariaeinterspecific competitionpopulation dynamicsnicheresource partitioningnegative interactions
Type
Research Article
Information
Parasitology , Volume 122 , Supplement S1 , March 2001 , pp. S13 - S22
Copyright
© 2002 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

BATES, R. M. & KENNEDY, C. R. (1990). Interactions between the acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae in rainbow trout: testing an exclusion hypothesis. Parasitology 100, 435–444.CrossRefGoogle Scholar
BATES, R. M. & KENNEDY, C. R. (1991). Potential interactions between Acanthocephalus anguillae and Pomphorhynchus laevis in their natural hosts chub, Leuciscus cephalus and the European eel, Anguilla anguilla. Parasitology 102, 289–297.CrossRefGoogle Scholar
BUCHMANN, K. (1988). Spatial distribution of Pseudodactylogyrus anguillae and P. bini (Monogenea) on the gills of the European eel, Anguilla anguilla. Journal of Fish Biology 32, 801–802.Google Scholar
BURT, T. P. & HEATHWAITE, A. L. (1996). The hydrology of the Slapton catchments. Field Studies 8, 543–557.Google Scholar
BUSH, A. O. & HOLMES, J. C. (1986). Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 142–152.CrossRefGoogle Scholar
BUSH, A. O., LAFFERTY, 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
CANNING, E. U., COX, F. E. G., CROLL, N. A. & LYONS, K. M. (1973). The natural history of Slapton Ley Nature Reserve: VI. Studies on the parasites. Field Studies 3, 681–718.Google Scholar
CHAPPELL, L. H. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775–778.CrossRefGoogle Scholar
DOBSON, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317–347.CrossRefGoogle Scholar
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
GREY, A. J. & HAYUNGA, E. G. (1980). Evidence for alternative site selection by Glaridacris laruei (Cestoida: Caryophyllidea) as a result of interspecific competition. Journal of Parasitology 66, 371–372.CrossRefGoogle Scholar
HALVORSEN, O. & MACDONALD, S. (1972). Studies on the helminth fauna of Norway XXVI: the distribution of Cyathocephalus truncatus (Pallas) in the intestine of brown trout (Salmo trutta L.). Norwegian Journal of Zoology 20, 265–272.Google Scholar
HOLLAND, C. (1984). Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303–315.Google Scholar
HOLLAND, C. (1987). Interspecific effects between Moniliformis (Acanthocephala), Hymenolepis (Cestoda) and Nippostrongylus (Nematoda) in the laboratory rat. Parasitology 94, 567–581.CrossRefGoogle Scholar
HOLMES, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–347.CrossRefGoogle Scholar
JOHNES, P. J. & WILSON, H. M. (1996). The limnology of Slapton Ley. Field Studies 8, 585–612.Google Scholar
KENNEDY, C. R. (1975). The natural history of Slapton Ley Nature Reserve VIII. The parasites of fish, with special reference to their use as a source of information about the aquatic community. Field Studies 4, 177–189.Google Scholar
KENNEDY, C. R. (1981a). The establishment and population biology of the eyefluke Tylodelphys podicipina (Digenea: Diplostomatidae) in perch. Parasitology 82, 245–255.Google Scholar
KENNEDY, C. R. (1981b). Long term studies on the population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata (Digenea: Diplostomatidae), concurrently infecting the eyes of perch, Perca fluviatilis. Journal of Fish Biology 19, 221–236.Google Scholar
KENNEDY, C. R. (1987). Long term stability in the population levels of the eyefluke Tylodelphys podicipina (Digenea: Diplostomatidae) from perch. Journal of Fish Biology 31, 571–581.CrossRefGoogle Scholar
KENNEDY, C. R. (1992). Field evidence for interactions between the acanthocephalans Acanthocephalus anguillae and A. lucii in eels, Anguilla anguilla. Ecological Parasitology 1, 122–134.Google Scholar
KENNEDY, C. R. (1993). Introductions, spread and colonization of new localities by fish helminth and crustacean parasites in the British Isles: a perspective and appraisal. Journal of Fish Biology 43, 287–301.CrossRefGoogle Scholar
KENNEDY, C. R. (1994). The ecology of introductions. In Parasitic Diseases of Fish (ed. PIKE, A. W. & LEWIS, J. W.), pp. 189–208. Tresaith, Dyfed, Samara Publishing Ltd.
KENNEDY, C. R. (1996). The fish of Slapton Ley. Field Studies 8, 685–697.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., BATES, R. M. & BROWN, A. F. (1989). Discontinuous distributions of the fish acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae in Britain and Ireland: an hypothesis. Journal of Fish Biology 34, 607–619.CrossRefGoogle Scholar
KENNEDY, C. R. & BURROUGH, R. (1977). The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch. Journal of Fish Biology 11, 619–633.CrossRefGoogle Scholar
KENNEDY, C. R. & DI CAVE, D. (1998). Gyrodactylus anguillae (Monogenea): the story of an appearance and a disappearance. Folia Parasitologica 45, 77–78.Google Scholar
KENNEDY, C. R. & GUÉGAN, J.-F. (1996). The number of niches in intestinal helminth communities of Anguilla anguilla: are there enough spaces for parasites? Parasitology 113, 293–302.Google Scholar
KENNEDY, C. R & HARTVIGSEN, R. A. (2000). Richness and diversity of intestinal metazoan communities in brown trout Salmo trutta compared to those of eels Anguilla anguilla in their European heartlands. Parasitology 121, 55–64.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. Oxford, Fishing News Books.
ROHDE, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648–671.CrossRefGoogle Scholar
ROHDE, K. (1991). Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91–104.CrossRefGoogle Scholar
ROHDE, K. (1998). Is there a fixed number of niches for endoparasites of fish? International Journal for Parasitology 28, 1861–1865.Google Scholar
STOCK, T. M. & HOLMES, J. C. (1987). Dioecocestus asper (Cestoda: Dioecocestidae): an interference competitor in an enteric helminth community. Journal of Parasitology 73, 1116–1123.CrossRefGoogle Scholar
STOCK, T. M. & HOLMES, J. C. (1988). Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. Journal of Parasitology 74, 214–227.CrossRefGoogle Scholar