Metazoan Parasites and Health State of European Eel, Anguilla Anguilla (Anguilliformes, Anguillidae), From Tonga Lake and El Mellah Lagoon in the Northeast of Algeria

Open access


The aim of the study was to examine metazoans parasite communities of European eels (Anguilla anguilla) in freshwater (Tonga Lake) and brackish water (El Mellah lagoon) in the northeast of Algeria. Six parasite taxa were collected: one monogenean, Pseudodactylogyrus sp.; two crustaceans, Ergasilus sp. and Argulus foliaceus; two nematodes, Cucullanus sp. and Anguillicola crassus; one cestode, Bothriocephalus claviceps. Th e most prevalent parasite taxa in freshwater were Pseudodactylogyrus sp., A. crassus and Bothriocephalus claviceps; whereas in the brackish water, eels were infected mainly with A. crassus. Th e characteristics of the parasite component community structure revealed low parasite species diversity and high dominance values in eels from the two localities. Both communities were dominated by a single parasite species: Tonga eels by the monogenean Pseudodactylogyrus sp. and El Mellah lagoon eels by the nematode A. crassus, verified by high Berger-Parker dominance values of 0.76 and 0.87 respectively.

Abdelmonem, A. A., Metwally, M. M., Hussein, H. S., Elsheikha, H. M. 2010. Gross and microscopic pathological changes associated with parasite infection in European eel (Anguilla anguilla, Linnaeus 1758). Parasitology Research, 106, 463-469.

Baltazar-Soares, M., Biastoch, A., Harrod, C., Hanel, R., Marohn, L., Prigge, E., Evans, D., Bodles, K., Behrens, E., Boning, C. W., Eizaguirre, C. 2014. Recruitment collapse and population structure of the European eel shaped by local ocean current dynamics. Current Biology, 24, 104-108.

Banning, P., Haenen, O. L. M. 1990. Eff ects of the swimbladder nematode Anguillicola crassusin wild and farmed eel, Anguilla anguilla. In: Perkins, F. O., Cheng, T. C., eds. Pathology in Marine Science. Academic Press, 317-330.

Barry, J., McLeish, J., Dodd, J. A., Turnbull, J. F., Boylan, P., Adams, C. E. 2014. Introduced parasite Anguillicola crassus infection signifi cantly impedes swim bladder function in the European eel Anguilla Anguilla (L.). Journal of Fish Diseases, 37, 21-924.

Boudjadi, Z., Tahri, M., Djebarri, N., Bensouilah, M. 2008. Etude de l’infestation des anguilles (Anguilla anguilla) par le nematode (Anguillicola crassus) dans l’estuaire du Mafrag (Nord Est algerien). Mésogée, 64, 41-48.

Buchmann, K. 2012. Pseudodactylogyrus anguillae and Pseudodactylogyrus bini. In: Woo, T. K., Buchmann, K., eds. Fish Parasites: Pathology and Protection. CABI International, Wallingford, 209-224.

Bush, A. O., Laff erty, 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.

Britton, J. R., Pegg, J., Williams, C. F. 2011. Pathological and ecological host consequences of infection by an introduced fi sh parasite. PLoS One, 6, e26363.

Brusle, J. 1994. L’anguille europeenne Anguilla anguilla, un poisson sensible aux stress environnementaux et vulnerable a diverses atteintes pathogenes. Bulletin Français de la Peche et de la Pisciculture, 335, 237-260.

Chan, B. Z.; Wu, B. W. 1984. Studies on the pathogenicity, biology and treatment of Pseudodactylogyrus for eels in fi sh farms. Acta Zoologica Sinica, 30, 173-180.

Dezfuli, B. S., Giari, L., Castaldelli, G., Lanzoni, M., Rossi, R.; Lorenzoni M., Kennedy, C. R. 2014.Temporal and spatial changes in the composition and structure of helminth component communities in European eels Anguilla anguilla in an Adriatic coastal lagoon and some freshwaters in Italy. Parasitol. Res., 113, 113-120.

Dhaouadi, R., Sghaier, A., Aloui, N., Rejeb, A., Tarhouni, D., Dargouth, M. A. 2014. Etude de l’infestation de l’anguille europeenne, Anguilla anguilla, par le nematode Anguillicoloides crassus dans la lagune de Ghar El Melh (Nord de la Tunisie). Mar. Life, 18, 17-24.

Djebbari, N., Boudjadi, Z., Bensouilah, M. 2009. L’infestation de l’anguille Anguilla anguilla L., 1758 par le parasite Anguillicola crassus (Kuwahara, Niimi & Itagaki,1974) dans le complexe de zones humides d’El Kala (Nord-Est algerien).Bulletin de l’institut Scientifi que, Rabat, section Sciences de la vie, 31 (1), 45-50.

Djebbari, N., Hamza, I., Ladjama, I., Kaouachi, N., Barour, C., Bensouilah, M. 2015. Environmental Parameters and Temporal Dynamics of Anguillicoides crassus in Tonga Lake and Mafragestuary (North-East of Algeria). Research Journal of Fisheries and Hydrobiology, 10 (14), 147-156.

FAO 1987. Aménagement du chenal du lac Mellah. FAO et Ministere de l’hydraulique, de l’environnement et des forets, division de developpement des activites hydrauliques et agricoles, 1-25.

Fazio, G., Lecomte-Finiger, R., Bartrina, J., Mone, H., Sasal, P. 2005. Macroparasite community and asymmetry of the yellow eel Anguilla anguilla in Salses-Leucate lagoon, Southern France. Bulletin Français de la Peche et de la Pisciculture, 378-379

Fang, J., Shirakashi, S., Ogawa, K. 2008. Comparative susceptibility of Japanese and European eels to infections with Pseudodactylogyrus spp. Fish Pathology, 43, 144-151.

Feunteun, E. 2002. Management and restoration of European eel population (Anguilla anguilla): an impossible bargain? Ecological Engineering, 18, 575-591.

Ginneken, V., Ballieux, B., Willemze, R., Coldenhoff , K., Lentjes, E., Antonissen, E., Haenen, O., van den Th illlart, G. 2005. Haematology patterns of migrating European eels and the role of the EVEX virus. Comparative Biochemistry and Physiology, 140, 97-102.

Haenen, O. L. M., Lehmann, J., Engelsma, M. Y., Sturenberg, F. J., Roozenburg, I. 2010. Th e health status of European silver eels, Anguilla anguilla, in the Dutch River Rhine watershed and Lake Ijsselmeer. Aquaculture, 309, 15-24.

ICES, 2013. Report of the Joint EIFAAC/ICES Working Group on Eels (WGEEL). ICES CM.2013/AC0M:18. Available at: acom/2013/WGEEL/wgeel_2013.pdf/ (last accessed 4June 2014).

Jakob, E., Walter, T., Hanel, R. 2009. A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites. Journal of Applied Ichthyology, 1-49.

Kania, P. W., Taraschewski, H., Han, Y. S., Cone, D. K., Buchmann, K. 2010. Divergence between Asian, European and Canadian populations of the monogeneanPseudodactylogyrus bini indicated by ribosomal DNA patterns. Journal of Helminthology, 84, 404-409.

Kennedy, C. R. 1994. Th e distribution and abundance of the nematode Anguillicola australiensis in eels Anguilla reinhardtii in Queensland, Australia. Folia Parasitologica, 41, 279-285.

Kennedy, C. R. 2007. Th e pathogenic helminth parasites of eels. Journal of Fish Diseases, 30, 319-334.

Kennedy, C. R., Di Cave, D., Berrilli, F., Orecchia, P. 1997. Composition and structure of helminth communities in eels Anguilla anguilla from Italian coastal lagoons. Journal of Helminthology, 71, 35-40.

Kettle, A. J, Vollestad, L. A., Wibig, J. 2011. Where once the eel and the elephant were together: decline of the European eel because of changing hydrology in southwest Europe and northwest Africa? Fish and Fisheries, 12, 380-411.

Kirk, R. S., Kennedy, C. R., Lewis, J. W. 2000. Eff ect of salinity on hatching, survival an infectivity of Anguillicola crassus (Nematoda: Dracunculoiea) larvae. Dis. Aquat.Organ. 40, 211-218.

Knopf, K., Madriles Helm, A., Lucius, R., Bleiss, W., Taraschewski, H. 2008. Migratory response of European eel (Anguilla anguilla) phagocytes to the eel swimbladder nematode Anguillicola crassus. Parasitol. Res., 102, 1311-1316.

Koie, M. 1988. Parasites in eels, Anguilla Anguilla (L.), from eutrophic lake Esrum (Denmark). Acta Parasitol Pol. 33, 89-100.

Koie, M. 1991. Swimbladder nematodes (Anguilla spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the European eel (Anguilla anguilla). Journal du Conseil International Pour l’Exploration de la Mer, 47, 391-398.

Kristmundsson, A., Helgason, S. 2007. Parasite communities of eels Anguilla anguilla in freshwater and marine habitats in Iceland in comparison with other parasite communities of eels in Europe. Folia Parasitologica, 54, 141-153.

Lefebvre, F., Fazio, G., Crivelli, A. J. 2012. Anguillicoloides crassus. In: Woo, P. T. K., Buchmann, K., eds. Fish Parasites: Pathobiology and Protection. CABI, Wallingford, 320-336.

Lefebvre, F., Contournet, P, Crivelli, A. J. 2002. Th e health state of the eel swim bladder as a measure of parasite pressure by Anguillicola crassus. Parasitology, 124, 457-463.

Lefebvre, F., Fazio, G., Palstra, AP., Szekely, C., Crivelli, A. J. 2011. An evaluation of indices of gross pathology associated with the nematode Anguillicoloides crassus in eels. Journal of Fish Diseases, 34, 31-45.

Loucif, N., Meddour, A., Samraoui, B. 2009. Biodiversite des Parasites chez Anguilla anguilla Linnaeus, 1758 dans le Parc National d’El Kala - Algerie. European Journal of Scientifi cResearch, 2, 300-309.

Lymbery, A. J., Morine, M., Kanani, H. G., Beatty, S. J., Morgan, D. L. 2014. Co-invaders: the eff ects of alien parasites on native hosts. International Journal for Parasitology: Parasitesand Wildlife, 3, 171-177.

Magurran, A. E. 1988. Ecological Diversity and its Measurement. Croom Helm, London, 1-179.

Mayo-Hernandez, E., Penalver, J., Garcıa-Ayala, A., Serrano, E., Munoz, P., Ruiz de Ybanez, R. 2015. Richness and diversity of helminth species in eels from a hypersaline coastal lagoon, Mar Menor, south-east Spain. Journal of Helminthology, 89, 345-351.

Meeus, I., Brown, M. J., De Graaf, D. C., Smagghe, G. 2011. Eff ects of invasive parasites on bumble bee declines. Conservation Biology, 25, 662-671.

Molnar, K., Baska, F., Csaba, G., Glavits, R., Szekely, C. 1993. Pathological and histopathological studies o the swimbladder of eels Anguilla anguilla infected by Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms, 15, 41-50.

Moravec, F. 1992. Spreading of the nematode Anguillicola crassus (Dracunculoidea) among eel populations in Europe. Folia Parasitologica, 39, 247-248.

Moriarty, C., Dekker, W. 1997. Management of European eel. Irish Fisheries Bulletin (Dublin), 15.

Newbold, L. R., Hockley, F. A., Williams, C. F., Cable, J., Reading, A. J., Auchterlonie, N., Kemp, P. S. 2015. Relationship between European eel Anguilla anguilla infection with non-native parasites and swimming

behaviour on encountering accelerating fl ow. Journal of Fish Biology, 86 (5), 1519-1533.

Nielsen, M. E. 1997. Infection status of the swimbladder worm, Anguillicola crassus in silver stage European eel, Anguilla anguilla, from three diff erent habitats in Danish waters. J. Appl. Ichthyol., 13, 195−196.

Palstra, A. P., Heppener, D. F. M., Van Ginneken, V. J. T., Szekely, C., Van den Th illart, G. E. E. J. M. 2007. Swimming performance of silver eels is severely impaired by the swimbladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology, 352, 244-256.

Raibaut, A., Altunel, F. N. 1976. Redescription de Ergasilus gibbus Nordmann, 1832, Copepode parasite branchial de l’Anguille et remarques sur sa repartition geographique. B. Soc. Sci. Nat.Tunisie, 11, 75-80.

Robinet, T., Feunteun, E. 2002. Sublethal eff ects of exposure to chemical compounds: a cause for the decline in Atlantic eels? Ecotoxicology. 11, 265-277.

Sprengel, G., Luchtenberg, H. 1991. Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Diseases of Aquatic Organisms, 11, 31-35.

Tahri, M., Crivelli , A. J., Panfi li, J., Bensouilah, M. 2016. Health status of the swim bladder of the European eel Anguilla anguilla in northeastern Algeria’s lakeOubeira. International Journal of Fisheries and aquatic

Studies, 4 (1), 364-369.

Taraschewski, H. 2006. Hosts and parasites as aliens. Journal of Helminthology. 80, 99-128.

Terech-Majewska, E., Schulz, P., Siwicki, A. K. 2015. Infl uence of nematode Anguillicoloides crassus infestation on the cellular and humoral innateimmunity in European eel (Anguilla anguilla L.). Centr. Eur. J. Immunol., 40 (2), 127-131.

Winter, H. V., Jansen, H. M., Brujis, M. C. M. 2006. Assessing the impact of hydropower and fi sheries on downstream migrating silver eel, Anguilla anguilla, by telemetry in the River Meuse. Ecology of Freshwater Fish.,15, 221-228.

Wurtz, J., Taraschewski, H. 2000. Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Dis.Aquat. Org., 39,121-134.

Wurtz, J., Taraschewski, H., Pelster, B. 1996. Changes in gas composition in the swim bladder of the European eel (Anguilla anguilla) infected with Anguillicola crassus (Nematoda). Parasitology, 112, 233-238.

Vestnik Zoologii

The Journal of National Academy of Sciences of Ukraine, Schmalhauzen Institute of Zoology

Journal Information

Cite Score 2017: 0.39

SCImago Journal Rank (SJR) 2017: 0.268
Source Normalized Impact per Paper (SNIP) 2017: 0.485


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 120 120 16
PDF Downloads 113 113 9