Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-18T13:45:50.416Z Has data issue: false hasContentIssue false

Interspecific interactions between Acanthocephala in the intestine of brown trout: are they more frequent in Ireland?

Published online by Cambridge University Press:  17 October 2003

C. J. BYRNE
Affiliation:
Department of Zoology, University of Dublin Trinity College, Dublin 2, Ireland
C. V. HOLLAND
Affiliation:
Department of Zoology, University of Dublin Trinity College, Dublin 2, Ireland
C. R. KENNEDY
Affiliation:
Department of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS, UK
W. R. POOLE
Affiliation:
Marine Institute, Salmon Management Service Division, Newport, Co. Mayo, Ireland

Abstract

The aim of this paper was to test the hypothesis that when the 2 species of Acanthocephalan Pomphorhynchus laevis and Acanthocephalus clavula are found concurrently within the intestine of brown trout under field conditions, they have the potential to interact negatively. Evidence has shown that Acanthocephala are more likely to exhibit negative interactions with their own and other species, under both field and experimental conditions. Furthermore, the likelihood of these interactions is increased in Ireland because of the absence of certain definitive hosts and the fact that concurrent infections by two or more species of Acanthocephala are more commonly observed in fish. Data collected from wild and stocked brown trout and from 2 lakes provided an opportunity to compare the 2 potentially interacting helminth species in their fundamental and realized niche and several pieces of convincing evidence are provided here to support the hypothesis. A significant negative association between the numbers of each species found in individual fish was reported and this was consistent for both wild and stocked trout. Furthermore, an analysis of the proportions of low, moderate and high intensity infections in single and concurrent infections revealed a significant reduction in increasing intensities in concurrent infections compared to single infections. Finally, strikingly different patterns of niche inhabitation were observed, particularly for P. laevis in the presence of A. clavula in wild trout. Results from the niche width analysis also support the observations on average position in single and concurrent infections. The niche width of P. laevis when it co-occurred with A. clavula decreased markedly in high intensity infections compared to low intensity infections.

Type
Research Article
Copyright
2003 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

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, 435444.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, 289297.CrossRefGoogle Scholar
BROWN, A. J. (1989). Seasonal dynamics of the Acanthocephalan Pomphorhynchus laevis (Muller, 1776) in its intermediate and preferred definitive hosts. Journal of Fish Biology 34, 183194.CrossRefGoogle Scholar
BYRNE, C. (2000). Helminth parasite communities in wild and stocked trout (Salmo trutta) from the west of Ireland. Ph.D. thesis, Trinity College Dublin.
BYRNE, C., HOLLAND, C., POOLE, W. & KENNEDY, C. R. (2002). Comparison of the macroparasite communities of wild and stocked brown trout (Salmo trutta L.) in the west of Ireland. Parasitology 124, 435445.CrossRefGoogle Scholar
CHAPPELL, L. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775778.CrossRefGoogle Scholar
CONNEELY, J. J. & McCARTHY, T. K. (1984). The metazoan parasites of freshwater fishes in the Corrib catchment area, Ireland. Journal of Fish Biology 24, 363375.CrossRefGoogle Scholar
CONNEELY, J. J. & McCARTHY, T. K. (1986). Ecological factors influencing the composition of the parasite fauna of the European eel, Anguilla anguilla, (L.), in Ireland. Journal of Fish Biology 28, 207219.CrossRefGoogle Scholar
CONNEELY, J. J. & McCARTHY, T. K. (1988). The metazoan parasites of trout (Salmo trutta L.) in Western Ireland. Polish Archives of Hydrobiology 35, 443460.Google Scholar
CULVER, D. C. (1972). A niche analysis of Colorado ants. Ecology 4, 126131.CrossRefGoogle Scholar
DEZFULI, B. S., GIARI, L., De BIAGGI, S. & POULIN, R. (2001). Associations and interactions among intestinal helminths of the brown trout, Salmo trutta, in northern Italy. Journal of Helminthology 75, 331336.Google Scholar
DOBSON, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317347.CrossRefGoogle Scholar
GREY, A. J. & HAYUNGA, E. G. (1980). Evidence for alternative site selection by Glaridacris laruei (Cestoidea: Caryophyllidea) as a result of interspecific competition. Journal of Parasitology 66, 371372.CrossRefGoogle Scholar
GRIFFITHS, D. (1997). The status of Irish freshwater fish fauna: a review. Journal of Applied Ichthyology 13, 913.CrossRefGoogle Scholar
HOLLAND, C. (1984). Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303315.Google Scholar
HOLLAND, C. (1987). Interspecific interactions between Moniliformis (Acanthocephala), Hymenolepis (Cestoda) and Nippostrongylus (Nematoda) in the laboratory rat. Parasitology 94, 567581.CrossRefGoogle Scholar
HOLLAND, C. & KENNEDY, C. R. (1998). A checklist of parasitic helminth and crustacean species recorded in freshwater fish from Ireland. Proceedings of the Royal Irish Academy 97B, 225243.Google Scholar
HOLMES, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I General effects and comparison with crowding. Journal of Parasitology 47, 209216.Google Scholar
HOLMES, J. C. (1962 a). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). II Effects on growth. Journal of Parasitology 48, 8796.Google Scholar
HOLMES, J. C. (1962 b). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). III Effects in hamsters. Journal of Parasitology 48, 97100.Google Scholar
JANOVY, J. (2002). Concurrent infections and the community ecology of helminth parasites. Journal of Parasitology 88, 440445.CrossRefGoogle Scholar
JANOVY, J., CLOPTON, R. B., CLOPTON, D. A., SNYDER, S. D., EFTING, A. & KREBS, L. (1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189196.CrossRefGoogle Scholar
KANE, M. B. (1966). Parasites of Irish fishes. Scientific Proceedings of the Royal Dublin Society B1, 205220.Google Scholar
KENNEDY, C. R. (1966). The helminth parasites of some Irish freshwater fish. Irish Naturalists' Journal 15, 196199.Google Scholar
KENNEDY, C. R. (1972). The effect of temperature and other factors upon the establishment and survival of the acanthocephalan Pomphorhynchus laevis in goldfish. Parasitology 65, 283294.CrossRefGoogle Scholar
KENNEDY, C. R. (1992). Field evidence for interactions between Acanthocephalans Acanthocephalus anguillae and A. lucii in eels, Anguilla anguilla. Ecological Parasitology 1, 122134.Google Scholar
KENNEDY, C. R., BROUGHTON, P. F. & HINE, P. M. (1976). The sites occupied by the acanthocephalan Pomphorhynchus laevis in the alimentary canal of fish. Parasitology 72, 195206.CrossRefGoogle 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, 5564.CrossRefGoogle Scholar
KENNEDY, C. R. & LORD, D. (1982). Habitat specificity of the acanthocephalan Acanthocephalus clavula (Dujardin, 1845) in eels Anguilla anguilla (L). Journal of Helminthology 56, 121129.CrossRefGoogle Scholar
KENNEDY, C. R. & MORIARTY, C. (1987). Co-existence of congeneric species of Acanthocephala: Acanthocephalus lucii and A. anguillae in eels Anguilla anguilla in Ireland. Parasitology 95, 301310.Google Scholar
KENNEDY, C. R. & 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 Scholar
LYNDON, A. R. & KENNEDY, C. R. (2001). Colonisation and extinction in relation to competition and resource partitioning in Acanthocephalans of freshwater fishes of the British Isles. Folia Parasitologica 48, 3746.CrossRefGoogle Scholar
MATTHEWS, M. A., POOLE, W. R., DILLANE, M. G. & WHELAN, K. F. (1997). Juvenile recruitment and smolt output of brown trout (Salmo trutta L.), and Atlantic salmon (Salmo salar L.) from a lacustrine system in western Ireland. Fisheries Research 31, 1937.Google Scholar
MOLLOY, S., HOLLAND, C. & POOLE, W. R. (1993). Helminth parasites of brown and sea trout Salmo trutta L. from the West coast of Ireland. Proceedings of the Royal Irish Academy 93B, 137142.Google Scholar
MOLLOY, S., HOLLAND, C. & POOLE, W. R. (1995). Metazoan parasite community structure in brown trout from two lakes in western Ireland. Journal of Helminthology 69, 237242.CrossRefGoogle Scholar
POOLE, W. R., BYRNE, C. J., DILLANE, M. G., WHELAN, K. F. & GARGAN, P. (2002). The Irish Sea Trout Enhancement Programme: A review of the Broodstock and Ova Production Programmes. Fisheries Management and Ecology 9, 315328.CrossRefGoogle Scholar
POULIN, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.), S1S12.CrossRefGoogle Scholar
PRICE, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey.
VIDAL-MARTINEZ, V. M. & 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 Scholar