Folia Parasitologica 48[1] 37-46 (2001) | DOI: 10.14411/fp.2001.007
Colonisation and extinction in relation to competition and resource partitioning in acanthocephalans of freshwater fishes of the British Isles
- 1 Department of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter, EX4 4PS, UK
- 2 Department of Biological Sciences, Heriot-Watt University, Edinburgh, EH14 4AS, UK
This paper challenges two paradigms long held in relation to the ecology of parasites in freshwater systems: (1) autogenic species are poorer colonisers than allogenic ones; and (2) parasites with direct life cycles are more successful colonisers than those with complex life cycles. Using new and existing data for Acanthocephala in freshwater fish from the British Isles, it is suggested that all six species present have been able to colonise and persist successfully, in spite of the supposed limitations of their autogenic life-style. It is proposed that these parasites have overcome these limitations by a variety of means, which apply equally to all species considered. Foremost among these is the utilisation of a migratory fish host as either a preferred or a suitable host in their life cycle, allowing colonisation of new areas and rescue effects in established areas, whilst equally important is the use of a common and widespread crustacean as the intermediate host. In addition, all six species appear to exhibit resource partitioning by host at either or both the larval and adult stages, thus reducing the potential for competition and further facilitating colonisation and survival. This hypothesis is supported by data from previous studies both on acanthocephalans from Europe and North America and on other autogenic parasites. It also provides an explanation for the apparently atypical host utilisation patterns of some acanthocephalan species in areas on the edge of their distributions, notably in Ireland.
Keywords: Acanthocephala, colonisation, extinction, fish, persistence, resource partitioning
Received: December 3, 1998; Accepted: June 22, 2000; Published: March 1, 2001 Show citation
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References
- AMANTE L.C., FRESI E., LANERI U. 1967: Dati preliminari sul rapporto-sessi di un Acanthocefalo parassita di Asellus (Proasellus) coxalis Dollfus (Crustacea, Isopoda). Ric. Sci. 37: 446-451
- ARAI H.P. 1989: Acanthocephala. In: L. Margolis and Z. Kabata (Eds.), Guide to the Parasites of Fishes of Canada. Part III. Can. Spec. Publ. Fish. Aquat. Sci. 107: 1-90
- 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
Go to original source...
Go to PubMed... - BATES R.M., KENNEDY C.R. 1991: Potential interactions between Acanthocephalus anguillae and Pomphorhynchus laevis in their natural hosts chub, Leucisus cephalus and the European eel, Anguilla anguilla. Parasitology 102: 289-297
Go to original source...
Go to PubMed... - BROWN A.F., CHUBB J.C., VELTKAMP C.J. 1986: A key to the species of Acanthocephala parasitic in British freshwater fishes. J. Fish Biol. 28: 327-334
Go to original source... - BUSH A.O., LAFFERTY K.D., LOTZ J.M., SHOSTAK A.W. 1997: Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83: 575-583.
Go to original source...
Go to PubMed... - CHUBB J.C. 1967: Host specificity of some acanthocephalans of freshwater fishes. Helminthologia 8: 63-70
- CORDONNIER L.M., WARD H.L. 1967: Pomphorhynchus rocci sp. n. (Acanthocephala) from the rock bass Roccus saxatilis. J. Parasitol. 53: 1295-1297
Go to original source...
Go to PubMed... - DEZFULI B.S. 1996: Cypria reptans (Crustacea: Ostracoda) as an intermediate host of Neoechinorhynchus rutili (Acanthocephala: Eoacanthocephala) in Italy. J. Parasitol. 82: 503-505
Go to original source...
Go to PubMed... - DEZFULI B.S., ROSSETTI E., BELLETTATO C.M., MAYNARD B.J. 1999: Pomphorhynchus laevis in its intermediate host Echinogammarus stammeri in the River Brenta, Italy. J. Helminthol. 73: 95-102
Go to original source... - DEZFULI B.S., ROSETTI E., FANO E.A., ROSSI R. 1994: Occurrence of larval Acanthocephalus anguillae (Acanthocephala) in the Asellus aquaticus (Crustacea, Isopoda) from the River Brenta. Boll. Zool. 61: 77-81
Go to original source... - DEZFULI B.S., ROSSETTI E., ZANINI N., ROSSI R. 1991a: Occurrence of Acanthocephalus clavula (Acanthocephala) in Echinogammarus pungens (Amphipoda) from the River Adige. Parassitologia 33: 121-126
Go to PubMed... - DEZFULI B.S., ZANINI N., REGGIANI G., ROSSI R. 1991b: Echinogammarus stammeri (Amphipoda) as an intermediate host for Pomphorhynchus laevis (Acanthocephala) parasite of fishes from the River Brenta. Boll. Zool. 58: 267-271
Go to original source... - DORUCU M., CROMPTON D.W.T., HUNTINGFORD F.A., WALTERS D.E. 1995: The ecology of endoparasitic helminth infections of brown trout (Salmo trutta) and rainbow trout (Oncorhynchus mykiss) in Scotland. Folia Parasitol. 42: 29-35
Go to PubMed... - ESCH G.W., KENNEDY C.R., BUSH A.O., AHO J.M. 1988: Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96: 519-532
Go to original source...
Go to PubMed... - FITZGERALD R.D., MULCAHY M.F. 1983: Parasites of salmon, Salmo salar L., and trout, Salmo trutta L., in the River Shournagh. Irish Fish. Inv. Series A 23:24-31
- GLEASON L.N. 1987: Population dynamics of Pomphorhynchus bulbocolli in Gammarus pseudolimnaeus. J. Parasitol. 73: 1099-1101
Go to original source...
Go to PubMed... - GLEDHILL T., SUTCLIFFE D.W., WILLIAMS W.D. 1993: British freshwater Crustacea Malacostraca: a key with ecological notes. Freshwater Biological Association Scientific Publication 52: 1-173
- GRIFFITHS D. 1997: The status of the Irish freshwater fish fauna: a review. J. Appl. Ichthyol. 13: 9-13
Go to original source... - HINE P.M., KENNEDY C.R. 1974: Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Mueller). J. Fish Biol. 6: 521-535
Go to original source... - HOLLAND C., KENNEDY C.R. 1997: A checklist of parasitic helminth and crustacean species recorded in freshwater fish from Ireland. Biol. Env. Proc. R. Irish Acad. 97B: 225-243
- KANE M.B. 1966: Parasites of Irish fishes. Sci. Proc. R. Dublin Soc. B 18: 205-220
- KENNEDY C.R. 1974: A checklist of British and Irish freshwater fish parasites with notes on their distribution. J. Fish Biol. 6: 613-644
Go to original source... - KENNEDY C.R. 1975: Ecological Animal Parasitology. Blackwell, Oxford, 163 pp
- KENNEDY C.R. 1984a: The status of flounders, Platichthys flesus L., as hosts of the acanthocephalan Pomphorhynchus laevis (Mueller) and its survival in marine conditions. J. Fish Biol. 24: 135-149
Go to original source... - KENNEDY C.R. 1984b: The dynamics of a declining population of the acanthocephalan Acanthocephalus clavula in eels Anguilla anguilla in a small river. J. Fish Biol. 25: 665-677
Go to original source... - KENNEDY C.R. 1985: Interactions of fish and parasite populations: to perpetuate or pioneer? In: D. Rollinson and R.M. Anderson (Eds.), Ecology and Genetics of HostParasite Interactions. Academic Press, London, pp. 1-20
- KENNEDY C.R. 1990: Helminth communities in freshwater fish: structured communities or stochastic assemblages? In: G.W. Esch, A.O. Bush and J.M. Aho (Eds.), Parasite Communities: Patterns and Processes. Chapman and Hall, London, pp. 131-156
Go to original source... - KENNEDY C.R. 1992: Field evidence for interactions between the acanthocephalans Acanthocephalus anguillae and A. lucii in eels, Anguilla anguilla. Ecol. Parasitol. 1: 122-134
- 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. J. Fish Biol. 43: 287-301
Go to original source... - KENNEDY C.R. 1994: The ecology of introductions. In: A.W. Pike and J.W. Lewis (Eds.), Parasitic Diseases of Fish. Samara Publishing Ltd., Tresaith, Wales, pp. 189208
- KENNEDY C.R. 1996: Colonization and establishment of Pomphorhynchus laevis (Acanthocephala) in an isolated English river. J. Helminthol. 70: 27-31
Go to original source...
Go to PubMed... - 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 Parasitol. 44: 267-273
Go to PubMed... - 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. J. Fish Biol. 34:607619
Go to original source... - KENNEDY C.R., HARTVIGSEN R., HALVORSEN O. 1991: The importance of fish stocking in the dissemination of parasites throughout a group of reservoirs. J. Fish Biol. 38: 541-552
Go to original source... - 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: 301-310
Go to original source...
Go to PubMed... - KENNEDY C.R., NIE P., KASPERS J., PAULISSE J. 1992: Are eels (Anguilla anguilla L.) planktonic feeders? Evidence from parasitic communities. J. Fish Biol. 41: 567-580
Go to original source... - LASSIERE O.L. 1988: Host-parasite relationships between larval Sialis lutaria (Megaloptera) and Neoechinorhynchus rutili (Acanthocephala). Parasitology 97: 331-338
Go to original source...
Go to PubMed... - LUNDSTROM A. 1942: Die Acanthocephalan Schwedens. Doctoral thesis, University of Lund, Sweden, 242 pp.
- LYNDON A.R. 1996: The role of acanthocephalan parasites in the predation of freshwater isopods by fish. In: S.P.R. Greenstreet and M.L. Tasker (Eds.), Aquatic Predators and Their Prey. Fishing News Books, Oxford, pp. 26-32
- MARCOGLIESE D.J., CONE D. 1996: On the distribution and abundance of eel parasites in Nova Scotia: influences of pH. J. Parasitol. 82: 389-399
Go to original source...
Go to PubMed... - MUNRO M.A., WHITFIELD P.J., DIFFLEY R. 1989: Pomphorhynchus laevis (Mueller) in flounder, Platichthys flesus L., in the tidal River Thames: population structure, microhabitat utilization and reproductive status in the field and under conditions of controlled salinity. J. Fish Biol. 35:719-735
Go to original source... - PRICE P.W. 1980: Evolutionary Biology of Parasites. Princeton University Press, New Jersey, 237 pp
- VAN MAREN M.J. 1979a: The amphipod Gammarus fossarum Koch (Crustacea) as intermediate host for some helminth parasites, with notes on their occurrence in the final host. Bijdr. Dierk. 42: 97-110
Go to original source... - VAN MAREN M.J. 1979b: Structure and dynamics of the French upper Rhone ecosystems XII. An inventory of helminth fish parasites from the upper Rhone river (France). Bull. Zool. Mus. Amsterdam 6: 189-199
- VARLEY M.E. 1967: British Freshwater Fishes: Factors Affecting Their Distribution. Fishing News Books, London, 148 pp
- WALKEY M. 1967: The ecology of Neoechinorhynchus rutili (Mueller). J. Parasitol. 53: 795-804
Go to original source...
Go to PubMed... - WHEELER A. 1977: The origin and distribution of the freshwater fishes of the British Isles. J. Biogeography 4: 124
Go to original source... - WILLIAMS W.D. 1963: The ecological relationships of isopod crustaceans Asellus aquaticus (L.) and A. meridianus Rac. Proc. Zool. Soc. Lond. 140: 661-679
Go to original source... - YEOMANS W.E., CHUBB J.C., SWEETING R.A. 1997: Khawia sinensis (Cestoda: Caryophyllidea) - an indicator of legislative failure to protect freshwater habitats in the British Isles? J. Fish Biol. 51: 880-885
Go to original source...


