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Differences in susceptibility of the European eel (Anguilla anguilla) and the Japanese eel (Anguilla japonica) to the swim-bladder nematode Anguillicola crassus

Published online by Cambridge University Press:  14 September 2004

K. KNOPF
Affiliation:
Department of Inland Fisheries, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany
M. MAHNKE
Affiliation:
Department of Inland Fisheries, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany

Abstract

The swim-bladder nematode Anguillicola crassus originates from the Far East where it is a parasite of the Japanese eel (Anguilla japonica). After A. crassus was introduced to Europe, it became a predominant parasite of the European eel (Anguilla anguilla). A study performed with experimentally infected eels (98 days, 23 °C) revealed significant differences in the susceptibility of the two eel species to this parasite. The recovery rate of 30 administered infective A. crassus larvae (L3) from A. japonica was less than half of that from A. anguilla (33·2% and 13·8%, respectively). Almost 60% of the worms recovered from A. japonica were found as dead, encapsulated and necrotic larvae in the swimbladder wall. In contrast, no dead larvae were found in A. anguilla. Additionally, the development of the worms was shown to be significantly slower in A. japonica compared with A. anguilla. The lower survival rate of the worms, together with their slower development, resulted in a significantly lower adult worm burden (11 and 428 mg wet weight, respectively) and in a decreased reproductive success in A. japonica compared with A. anguilla. These results demonstrate that the original host, A. japonica, possesses more effective defence mechanisms against A. crassus than does the non-adapted host, A. anguilla.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

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 Scholar
BUTTERWORTH, A. E. (1984). Cell-mediated damage to helminths. Advances in Parasitology 23, 143235.Google 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
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
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 WIJNGAARDEN, T. A. M. & BORGSTEEDE, F. H. M. (1994). An improved method for the production of infective third-stage juveniles of Anguillicola crassus. Aquaculture 123, 163165.CrossRefGoogle Scholar
HAENEN, O. L. M., VAN WIJNGAARDEN, T. A. M., VAN DER HEIJDEN, M. H. T., HÖGLUND, J., CORNELISSEN, J. B. J. W., VAN LENGOED, L. A. M. G., BORGSTEEDE, F. H. M. & VAN MUISWINKEL, W. B. (1996). Effects of experimental infections with different doses of Anguillicola crassus (Nematoda, Dracunculoidea) on European eel (Anguilla anguilla). Aquaculture 141, 4157.CrossRefGoogle Scholar
HÖGLUND, J., ANDERSSON, J., WICKSTRÖM, H. & REIZENSTEIN, M. (1992). The distribution of Anguillicola in Sweden and its association with thermal discharge areas. Irish Fisheries Investigations Series A (Freshwater) 36, 143150.Google 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. & 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. & FITCH, D. J. (1990). Colonization, 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
KNOPF, K., NASER, K., VAN DER HEIJDEN, M. H. T. & TARASCHEWSKI, H. (2000 a). Humoral immune response of European eel Anguilla anguilla experimentally infected with Anguillicola crassus. Diseases of Aquatic Organisms 42, 6169.Google Scholar
KNOPF, K., NASER, K., VAN DER HEIJDEN, M. H. T. & TARASCHEWSKI, H. (2000 b). Evaluation of an ELISA and immunoblotting for studying the humoral immune response in Anguillicola crassus infested European eel (Anguilla anguilla). Diseases of Aquatic Organisms 43, 3948.Google 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 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. (Philometridae, Anguillicolidae). Japanese Journal of Parasitology 23, 275279.Google 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.Google Scholar
MOLNÁR, K., BASKA, F., CSABA, G. Y., GLÁVITS, R. & SZÉKELY, C. S. (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 Scholar
MORAVEC, F. (1992). Spreading of the nematode Anguillicola crassus (Dracunculoidea) among eel populations in Europe. Folia Parasitologica 39, 247248.Google Scholar
MORAVEC, F. & SKORIKOVA, 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 Scholar
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 Anguillicola globiceps (Nematoda: Dracunculoidea) parasitic in the swimbladder of eels (Anguilla japonica and A. anguilla) in East Asia. Folia Parasitologica 41, 127137.Google 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
SURES, B. & KNOPF, K. (2004). Individual and combined effects of cadmium and 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 128, 445454.CrossRefGoogle Scholar
SURES, B., KNOPF, K., WÜRTZ, J. & TARASCHEWSKI, H. (1999). Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 119, 323330.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. (1999). Der Aal, 3rd Edn. Parey, Berlin.
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. In Pathology in Marine Science (ed. Perkins, F. O. & Cheng, T. C.), pp. 317330. Academic Press, New York.CrossRef
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
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 Scholar