Hostname: page-component-5c6d5d7d68-txr5j Total loading time: 0 Render date: 2024-08-15T17:45:36.922Z Has data issue: false hasContentIssue false

The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host

Published online by Cambridge University Press:  12 April 2024

K. Knopf*
Affiliation:
Department of Inland Fisheries, Leibniz-Institute for Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany
*
* Fax: +49 30 64181799, klaus.knopf@igb-berlin.de

Abstract

The swimbladder nematode Anguillicola crassus originates from Asia where it is a parasite of the Japanese eel Anguilla japonica. After its introduction to Europe about 25 years ago, the parasite spread rapidly within the indigenous populations of the European eel Anguilla anguilla and subsequently the prevalence and mean intensity appeared to stabilize. Under experimental and aquaculture conditions the naïve new host appears to be more susceptible to A. crassus compared to the original host. Both eel species develop a immune response against A. crassus. The antibody response is well characterized for the European eel, but poorly characterized for the Japanese eel. It remains unclear if antibodies have any protective function against A. crassus. Encapsulation of larvae of A. crassus can be observed in naturally infected European eels. However, encapsulation of larvae following experimental infection has not been detected in European eels, but only in Japanese eels. Reinfection experiments and intraperitoneal injection of A. crassus homogenates failed to demonstrate the development of acquired immunity in European eels. Immunization with irradiated third stage larvae provided preliminary evidence for acquired immunity against A. crassus in the Japanese eel, but not in the European eel.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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

Ashworth, S.T. & Kennedy, C. R. (1999) Density-dependent effects on Anguillicola crassus (Nematoda) within its European eel definitive host. Parasitology 118, 289296.CrossRefGoogle ScholarPubMed
Ashworth, S.T., Kennedy, C.R. & Blanc, G. (1996) Density-dependent effects of Anguillicola crassus (Nematoda) within and on its copepod intermediate hosts. Parasitology 113, 303309.CrossRefGoogle ScholarPubMed
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 56, 223233.CrossRefGoogle ScholarPubMed
Boon, J.H., Cannaerts, V.M.H., Augustijn, H., Machiels, M.A.M., De Charleroy, D. & Ollevier, F. (1990a) The effect of different infection levels with infective larvae of Anguillicola crassus on haematological parameters of European eel (Anguilla anguilla). Aquaculture 87, 243253.CrossRefGoogle Scholar
Boon, J.H., Zuxu, Y. & Booms, G.H.R. (1990b) Effects on Anguillicola crassus and Trypanosoma granulosum infections on peripheral blood cells of European eel (Anguilla anguilla, L.). Bulletin of the European Association of Fish Pathologists 10, 143145.Google Scholar
Buchmann, K., Pedersen, L.Ø. & Glamann, J. (1991) Humoral immune response of European eel Anguilla anguilla to a major antigen in Anguillicola crassus . Diseases of Aquatic Organisms 12, 5557.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
Egusa, S. (1979) Notes on the culture of the European eel (Anguilla anguilla, L.) in Japanese eel-farming ponds. Rapports et Proces-Verbaux des Réunions. Conseil International pour l'Éxploration de la Mer 174, 5158.Google Scholar
El Hilali, M., Yahyaoui, A., Sadak, A., Maachi, M. & Taghy, Z. (1996) Premières données épidémiologiques sur l’ anguillicolose au Maroc. Bulletin Français de la Pêche et de Pisciculture 340, 5760.CrossRefGoogle Scholar
Fries, L.T. & Williams, D.J. (1996) Occurrence of Anguillicola crassus, an exotic parasitic swim bladder nematode of eels, in 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. & 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.CrossRefGoogle Scholar
Haenen, O.L.M., van Wijngaarden, T.A.M., van der Heijden, M.H.T., Höglund, J., Cornelissen, J.B.W.J., van Leengoed, L.A.M.G. (1996) Effects of experimental infections with different doses of Anguillicola crassus (Nematoda, Dracunculoidea) on European eel (Anguilla anguilla). Aquaculture 141, 4157.CrossRefGoogle Scholar
Hartmann, F. (1991) Neue Untersuchungen über den Aalparasiten Anguillicola crassus. pp. 112 in Koops, H. (Ed.) Arbeiten des Deutschen Fischerei-Verbandes. Hamburg, Deutscher Fischerei-Verband.Google Scholar
Höglund, J., Pilström, L. (1994) Purification of adult Anguillicola crassus whole-worm extract antigens for detection of specific antibodies in serum from the European eel (Anguilla anguilla) by ELISA. Fish and Shellfish Immunology 4, 311319.CrossRefGoogle Scholar
Höglund, J., Pilström, L. (1995) Mechanical isolation and characterization of antigens from adult Anguillicola crassus . Fish and Shellfish Immunology 5, 5160.CrossRefGoogle Scholar
Höglund, J., Andersson, J., Härdig, J. (1992a) Haematological responses in the European eel, Anguilla anguilla, L., to sublethal infestation by Anguillicola crassus in a thermal effluent of the Swedish Baltic. Journal of Fish Diseases 15, 507514.CrossRefGoogle Scholar
Höglund, J., Andersson, J., Wickström, H. & Reizenstein, M. (1992b) The distribution of Anguillicola in Sweden and its association with thermal discharge areas. Irish Fisheries Investigations Series A (Freshwater) 36, 143150.Google 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) Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Diseases of Aquatic Organisms 40, 211218.CrossRefGoogle ScholarPubMed
Knopf, K. (1999) Untersuchungen zur Immunantwort des Europäischen Aals ( Anguilla anguilla ) auf den Schwimmblasen-Nematoden Anguillicola crassus. PhD thesis, 141 pp. University of Karlsruhe.Google Scholar
Knopf, K. & Mahnke, M. (2004) Differences in susceptibility of the European eel (Anguilla anguilla) and the Japanese eel (Anguilla japonica) to the swimbladder nematode Anguillicola crassus . Parasitology 129, 491496.CrossRefGoogle Scholar
Knopf, K., Würtz, J., Sures, B. & Taraschewski, H. (1998) Impact of low water temperature on the development of Anguillicola crassus in the final host Anguilla anguilla . Diseases of Aquatic Organisms 33, 143149.CrossRefGoogle ScholarPubMed
Knopf, K., Naser, K., van der Heijden, M.H.T. & Taraschewski, H. (2000a) Humoral immune response of European eel Anguilla anguilla experimentally infected with Anguillicola crassus . Diseases of Aquatic Organisms 42, 6169.CrossRefGoogle ScholarPubMed
Knopf, K., Naser, K., van der Heijden, M.H.T. & Taraschewski, H. (2000b) Evaluation of an ELISA and immunoblotting for studying the humoral immune response in Anguillicola crassus infected European eel Anguilla anguilla . Diseases of Aquatic Organisms 43, 3948.CrossRefGoogle ScholarPubMed
Køie, M. (1988) Parasites in European eel Anguilla anguilla (L.) from Danish freshwater, brackish and marine localities. Ophelia 29, 93118.CrossRefGoogle Scholar
Lefebvre, F.S. & Crivelli, A.J. (2004) Anguillicolosis: dynamics of the infection over two decades. Diseases of Aquatic Organisms 62, 227232.CrossRefGoogle ScholarPubMed
Lefebvre, F., Mounaix, B., Poizat, G. & Crivelli, A.J. (2004) Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses. Journal of Fish Biology 64, 435447.CrossRefGoogle Scholar
Molnár, K. (1994) Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicola crassus . Diseases of Aquatic Organisms 20, 163170.CrossRefGoogle Scholar
Molnár, K., Baska, F., Csaba, G. & Székely, C. (1993) Pathological and histopathological studies of the swimbladder of eels Anguilla anguilla infected by Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15, 4150.CrossRefGoogle Scholar
Molnár, K., Szakolczai, J. & Vetési, F. (1995) Histological changes in the swimbladder wall of eels due to abnormal location of adults and second stage larvae of Anguillicola crassus . Acta Veterinaria Hungarica 43, 125137.Google ScholarPubMed
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 aquatic insects as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea), a swimbladder parasite of eels. Diseases of Aquatic Organisms 34, 217222.CrossRefGoogle ScholarPubMed
Moravec, F. & Taraschewski, H. (1988) Revision of the genus Anguillicola Yamaguti, 1935 (Nematoda: Anguillicolidae) of the swimbladder of eels, including descriptions of two new species, A. novaezelandiae sp.n. and A. papernai sp.n. Folia Parasitologica 35, 125146.Google Scholar
Nagasawa, K., Kim, Y.-G. & Hirose, H. (1994) Anguillicola crassus and A. globiceps (Nematoda: Dracunculoidea) parasitic in the swimbladder of eels (Anguilla japonica and A. anguilla) in East Asia: a review. Folia Parasitologica 41, 127137.Google Scholar
Neumann, W. (1985) Schwimmblasenparasit Anguillicola bei Aalen. Fischer and Teichwirt 11, 322.Google Scholar
Nielsen, M.E. (1997) Infection status of the swimbladder worm, Anguillicola crassus in silver stage European eel, Anguilla anguilla, from 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.CrossRefGoogle ScholarPubMed
Nielsen, M.E. & Buchmann, K. (1997) Glutathione-s-transferase is an important antigen in the eel nematode Anguillicola crassus . Journal of Helminthology 71, 319324.CrossRefGoogle Scholar
Nimeth, K., Zwerger, P., Würtz, J., Savenmoser, W. & Pelster, B. (2000) Infection of the glass-eel swimbladder with the nematode Anguillicola crassus . Parasitology 121, 7583.CrossRefGoogle ScholarPubMed
Palíková, M., Navrátil, S. (2001) Occurrence of Anguillicola crassus in the water reservoir Koryèany (Czech Republic) and its influence on the health condition and haematological indices of eels. Acta Veterinaria Brno 70, 443449.CrossRefGoogle Scholar
Schabuss, M., Kennedy, C.R., Konecny, R., Grillitsch, B., Reckendorfer, W., Schiemer, F. & Herzig, A. (2005) Dynamics and predicted decline of Anguillicola crassus infection in European eels, Anguilla anguilla, in Neusiedler See, Austria. Journal of Helminthology 79, 159167.CrossRefGoogle ScholarPubMed
Sures, B. & Knopf, K. (2004) Parasites as a threat to freshwater eels? Science 304, 208209.CrossRefGoogle ScholarPubMed
Székely, C. (1994) Paratenic hosts for the parasitic nematode Anguillicola crassus in Lake Balaton, Hungary. Diseases of Aquatic Organisms 18, 1120.CrossRefGoogle Scholar
Tesch, F.W. (1999) Der Aal. 3rd edn. 397 pp. Berlin, Blackwell Wissenschafts-Verlag.Google Scholar
Ushikoshi, R., Inui, T., Mano, N. & Hirose, H. (1999) A method for specific antibody detection from Japanese eel by indirect ELISA using cuticular antigen of Anguillicola crassus . Fish Pathology 34, 8182.CrossRefGoogle Scholar
Van Banning, P. & Haenen, O.L.M. (1990) Effects of the swimbladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla pp. 317330 in Perkins, F.O. & Cheng, T.C. (Eds) Pathology in marine science. New York, Academic Press.Google Scholar
Van der Heijden, M.H.T., Helders, G.M., Booms, G.H.R., Huisman, E.A., Rombout, J.H.W.M. & Boon, J.H. (1996) Influence of flumequine and oxytetracycline on the resistance of European eel against the parasitic swimbladder nematode Anguillicola crassus . Veterinary Immunology and Immunopathology 52, 127134.CrossRefGoogle ScholarPubMed
Whyte, S.K., Chappell, L.H. & Secombes, C.J. (1989) Cytotoxic reactions of rainbow trout, Salmo gairdneri Richardson, macrophages for larvae of the eye fluke Diplostomum spathaceum (Digenea). Journal of Fish Biology 35, 333345.CrossRefGoogle Scholar
Wickström, H., Clevestam, P., Höglund, J. (1998) The spreading of Anguillicola crassus in freshwater lakes in Sweden. Bulletin Français de la Pêche et de Pisciculture 349, 215221.CrossRefGoogle Scholar
Würtz, J. & Taraschewski, H. (2000) Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus . Diseases of Aquatic Organisms 39, 121134.CrossRefGoogle ScholarPubMed
Würtz, J., Taraschewski, H. & Pelster, B. (1996) Changes in gas composition in the swimbladder of the European eel (Anguilla anguilla) infected with Anguillicola crassus (Nematoda). Parasitology 112, 233238.CrossRefGoogle ScholarPubMed