Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-08T07:19:45.176Z Has data issue: false hasContentIssue false

Epidemiology of Anguillicola crassus in the European eel (Anguilla anguilla) from two rivers in southern England

Published online by Cambridge University Press:  17 February 2005

J. NORTON
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD
D. ROLLINSON
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD
J. W. LEWIS
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX

Abstract

European eels Anguilla anguilla from the rivers Thames and Test, in the south of England, were examined between 2000 and 2003 for infection with the swim-bladder nematode Anguillicola crassus. Since its introduction to Thames eels at tidal estuarine locations circa 1987, A. crassus has become established in non-tidal freshwater stretches upriver and data from these locations are reported for the first time. The prevalence of infection at Thames estuary locations was higher during 2000–2003 than for the period 1987–1992. By 2003, similar prevalences were observed at freshwater and estuarine locations, but infection intensities were significantly higher in freshwater. Eels from the river Test appear to have been recently colonized by A. crassus (circa 2000). Parasite population establishment within these eels was uncharacteristically slow during 2000–2001, with low prevalence and intensity of infection, and few gravid females during this period. By 2003, infection levels in Test eels were similar to those in Thames eels. The expansion of the A. crassus population in Test eels has occurred in the absence of the paratenic host ruffe Gymnocephalus cernuus, and at suboptimal pH for the survival and infectivity of free-living larvae. The epidemiology of A. crassus in Test eels demonstrates that transmission of A. crassus by ruffe is not required for high prevalence and intensity of infection in eels. However, the consistently low and atypical levels of infection in Test eels during 2000 and 2001 suggests that paratenic transmission by ruffe may provide a substantial contribution to the dynamics of A. crassus in eels in the early years following introduction, by facilitating the rapid increase in prevalence and intensity of A. crassus infection that typically occurs during this time.

Type
Research Article
Copyright
© 2005 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

ASHWORTH, S. T. ( 1994). Possible regulation in the Anguillicola crassus host–parasite system. In Parasitic Diseases of Fish ( ed. Pike, A. W. & Lewis, J. W.), pp. 141150. Samara Publishing, Tresaith, Dyfed.
ASHWORTH, S. T. & BLANC, G. ( 1997). Anguillicola crassus, un colonisateur agressif récemment introduit dans les stocks Européens d'anguilles. Bulletin Francais de la Pêche et de la Pisciculture 344/345, 335342.CrossRefGoogle Scholar
ASHWORTH, S. T. & KENNEDY, C. R. ( 1999). Density dependent effects on Anguillicola crassus (Nematoda) within its European eel definitive host. Parasitology 118, 289296.CrossRefGoogle Scholar
AUDENAERT, V., HUYSE, T., GOEMANS, G., BELPAIRE, C. & VOLCKAERT, F. A. M. ( 2003). Spatio-temporal dynamics of the parasitic nematode Anguillicola crassus in Flanders, Belgium. Diseases of Aquatic Organisms 55, 223233.CrossRefGoogle Scholar
BARUš, V., MORAVEC, F. & PROKEš, M. ( 1999). Anguillicolosis of the European eel (Anguilla anguilla) in the Czech Republic. Czech Journal of Animal Science 44, 423431.Google Scholar
BELPAIRE, C., DE CHARLEROY, D., THOMAS, K., VAN DAMME, P. & OLLEVIER, F. ( 1989). Effects of restocking on the distribution of the swimbladder nematode Anguillicola crassus in Flanders, Belgium. Journal of Applied Ichthyology 5, 151153.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, 575583.CrossRefGoogle Scholar
DE CHARLEROY, D., THOMAS, K., BELPAIRE, C. & OLLEVIER, F. ( 1989). The viability of the free-living larvae of Anguillicola crassus. Journal of Applied Ichthyology 5, 154156.CrossRefGoogle Scholar
DE CHARLEROY, D., GRISEZ, L., THOMAS, K., BELPAIRE, C. & OLLEVIER, F. ( 1990). The life cycle of Anguillicola crassus. Diseases of Aquatic Organisms 8, 7784.CrossRefGoogle Scholar
DEKKER, W. & VAN WILLIGEN, J. ( 1989). Short note on the distribution and abundance of Anguillicola in the Netherlands. Journal of Applied Ichthyology 1, 4647.CrossRefGoogle Scholar
EVANS, D. W. & MATTHEWS, M. A. ( 1999). Anguillicola crassus (Nematoda: Dracunculoidea); first documented record of this swimbladder parasite of eels in Ireland. Journal of Fish Biology 55, 665668.CrossRefGoogle Scholar
EVANS, D. W., MATTHEWS, M. A. & McCLINTOCK, C. A. ( 2001). The spread of the eel swimbladder nematode Anguillicola crassus through the Erne system, Ireland. Journal of Fish Biology 59, 14161420.CrossRefGoogle Scholar
FRIES, L. T., WILLIAMS, D. J. & JOHNSON, S. K. ( 1996). Occurrence of Anguillicola crassus, an exotic parasitic swim bladder nematode of eels, the southeastern United States. Transactions of the American Fisheries Society 125, 794797.2.3.CO;2>CrossRefGoogle Scholar
HAENEN, O. L. M., GRISEZ, L., DE CHARLEROY, D., BELPAIRE, C. & OLLEVIER, F. ( 1989). Experimentally induced infections of European eel Anguilla anguilla with Anguillicola crassus (Nematoda, Dracunculoidea) and subsequent migration of larvae. Diseases of Aquatic Organisms 7, 97101.CrossRefGoogle Scholar
HAENEN, O. L. M. & VAN BANNING, P. ( 1991). Experimental transmission of Anguillicola crassus (Nematoda, Dracunculoidea) larvae from infected prey fish to the eel Anguilla anguilla. Aquaculture 92, 115119.CrossRefGoogle Scholar
HAENEN, O. L. M., VAN BANNING, P. & DEKKER, W. ( 1994). Infection of eel Anguilla anguilla (L.) and smelt Osmerus eperlanus (L.) with Anguillicola crassus (Nematoda, Dracunculoidea) in the Netherlands from 1986 to 1992. Aquaculture 126, 219229.Google Scholar
EL HILALI, M., YAHYAOUI, A., SADAK, A., MAACHI, M. & TAGHY, Z. ( 1996) Premières données épidémiologies sur l'anguillicolose au Maroc. Bulletin Francais de la Pêche et de la Pisciculture 340, 5760.CrossRefGoogle Scholar
HÖGLUND, J. & THOMAS, K. ( 1992). The black goby Gobius niger as a potential paratenic host for the parasitic nematode Anguillicola crassus in a thermal effluent of the Baltic. Diseases of Aquatic Organisms 13, 175180.CrossRefGoogle Scholar
KENNEDY, C. R. & FITCH, D. J. ( 1990). Colonisation, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel Anguilla anguilla, in Britain. Journal of Fish Biology 36, 117131.CrossRefGoogle Scholar
KIRK, R. S. ( 2003). The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology 10, 385394.CrossRefGoogle Scholar
KIRK, R. S., KENNEDY, C. R. & LEWIS, J. W. ( 2000 a). Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Diseases of Aquatic Organisms 40, 211218.Google Scholar
KIRK, R. S., LEWIS, J. W. & KENNEDY, C. R. ( 2000 b). Survival and transmission of Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 (Nematoda) in seawater eels. Parasitology 120, 289295.Google Scholar
KUWAHARA, A., NIIMI, A. & ITAGAKI, H. ( 1974). Studies on a nematode parasitic in the air bladder of the eel. I. Description of Anguillicola crassa n. sp. (Philometridea, Anguillicolidae). Japanese Journal of Parasitology 23, 275279.Google Scholar
LEFEBVRE, F., CONTOURNET, P., PRIOUR, F., SOULAS, O. & CRIVELLI, A. J. ( 2002). Spatial and temporal variation in Anguillicola crassus counts: results of a 4 year survey of eels in Mediterranean lagoons. Diseases of Aquatic Organisms 50, 181188.CrossRefGoogle Scholar
MOLNÁR, K., SZÉKELY, C. S. & PERÉNYI, M. ( 1994). Dynamics of Anguillicola crassus (Nematoda: Dracunculoidea) infection in eels of Lake Balaton, Hungary. Folia Parasitologica 41, 193202.Google Scholar
MORAVEC, F. ( 1992). Spreading of the nematode Anguillicola crassus (Dracunculoidea) among eel populations in Europe. Folia Parasitologica 39, 247248.Google Scholar
MORAVEC, F. ( 1996). Aquatic invertebrates (snails) as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea) and the role of paratenic hosts in the life cycle of this parasite. Diseases of Aquatic Organisms 27, 237239.CrossRefGoogle Scholar
MORAVEC, F. & KONECNY, R. ( 1994). Some new data on the intermediate and paratenic hosts of the nematode Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974 (Dracunculoidea), a swimbladder parasite of eels. Folia Parasitologica 41, 6570.Google Scholar
MORAVEC, F. & šKORÍKOVÁ, B. ( 1998). Amphibians and larvae of insects as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea), a swimbladder parasite of eels. Diseases of Aquatic Organisms 34, 217222.CrossRefGoogle Scholar
NIELSEN, M. E. ( 1997). Infection status of the swimbladder worm, Anguillicola crassus in silver stage European eel, Anguilla anguilla, from three different habitats in Danish waters. Journal of Applied Ichthyology 13, 195196.CrossRefGoogle Scholar
NIELSEN, M. E. ( 1999). An enhanced humoral immune response against the swimbladder nematode, Anguillicola crassus, in the Japanese eel. Anguilla japonica, compared with the European eel, A. anguilla. Journal of Helminthology 73, 227232.Google Scholar
NIMETH, K., ZWERGER, P., WÜRTZ, J., SALVERMOSER, W. & PELSTER, B. ( 2000). Infection of the glass-eel swimbladder with the nematode Anguillicola crassus. Parasitology 121, 7583.CrossRefGoogle Scholar
NORTON, J., LEWIS, J. W. & ROLLINSON, D. ( 2003). Parasite infracommunity diversity in eels: a reflection of local component community diversity. Parasitology 127, 475482.CrossRefGoogle Scholar
NORTON, J., LEWIS, J. W. & ROLLINSON, D. ( 2004). Temporal and spatial patterns of nestedness in eel-macroparasite communities. Parasitology 129, 203211.CrossRefGoogle Scholar
NORTON, J., ROLLINSON, D. & LEWIS, J. W. ( 2004). Patterns of infracommunity species richness in eels. Journal of Helminthology 78, 141146.CrossRefGoogle Scholar
OGLE, D. H. ( 1998). A synopsis of the biology and life history of ruffe. Journal of Great Lakes Research 24, 170185.CrossRefGoogle Scholar
PAZOOKI, J. & SZÉKELY, C. ( 1994). Survey of the paratenic hosts of Anguillicola crassus in Lake Velece, Hungary. Acta Veterinaria Hungarica 42, 8797.Google Scholar
PIETROCK, M. & MEINELT, T. ( 2002). Dynamics of Anguillicola crassus larval infections in a paratenic host, the ruffe (Gymnocephalus cernuus) from the Oder River on the border of Germany and Poland. Journal of Helminthology 76, 235240.CrossRefGoogle Scholar
PILCHER, M. W. & MOORE, J. F. ( 1993). Distribution and prevalence of Anguillicola crassus in eels from the tidal Thames catchment. Journal of Fish Biology 43, 339344.CrossRefGoogle Scholar
POULIN, R. ( 1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937944.CrossRefGoogle Scholar
REIMER, L. W., HILDEBRAND, A., SCHARBERTH, D. & WALTER, U. ( 1994). Anguillicola crassus in the Baltic Sea: field data supporting transmission in brackish waters. Diseases of Aquatic Organisms 18, 7779.CrossRefGoogle Scholar
ROLBIECKI, L. ( 2002). On the role of the paratenic hosts in the life cycle of the nematode Anguillicola crassus in the Vistula lagoon, Poland. Acta Ichthyologia et Piscatoria 32, 109116.CrossRefGoogle Scholar
RÓSZA, L., REICZIGEL, J. & MAJOROS, G. ( 2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.Google Scholar
SINHA, V. R. P. ( 1969). A note on the feeding of larger eels Anguilla anguilla (L.). Journal of Fish Biology 1, 279283.CrossRefGoogle Scholar
SZÉKELY, C. ( 1994). Paratenic hosts for the parasitic nematode Anguillicola crassus in Lake Balaton, Hungary. Diseases of Aquatic Organisms 18, 1120.CrossRefGoogle Scholar
TARASCHEWSKI, H., MORAVEC, F., LAMAH, T. & ANDERS, K. ( 1987). Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nematoda, Dracunculoidea) and Paratenuisentis ambiguus (Acanthocephala, Tenuisentidae). Diseases of Aquatic Organisms 3, 167176.CrossRefGoogle Scholar
TESCH, F. W. ( 1977). The Eel. Chapman and Hall. London.CrossRef
THOMAS, K. & OLLEVIER, F. ( 1992). Paratenic hosts of the swimbladder nematode Anguillicola crassus. Diseases of Aquatic Organisms 13, 165174.CrossRefGoogle Scholar
WICKSTRÖM, H., CLEVESTAM, P. & HÖGLUND, J. ( 1998). The spreading of Anguillicola crassus in freshwater lakes in Sweden. Bulletin Francais de la Pêche et de la Pisciculture 349, 215221.CrossRefGoogle Scholar