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A Comparative Study of Eubothrium Salvelini and E. crassum (Cestoda: Pseudophyllidea) Parasites of Arctic Charr and Brown Trout in Alpine Lakes

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Abstract

We compared the morphology, morphometry, and some aspects of the biology and ecology of Eubothrium crassum and E. salvelini, two pseudophyllidean tapeworms in brown trout, Salmo trutta m. lacustris, and Arctic charr, Salvelinus alpinus, in lakes of the western part of the Alps. The taxonomic importance of the apical disc for the discrimination of both taxa was confirmed. The apical disc of E. crassum is rectangular, possessing two deep grooves above the bothriae and 2–16 additional indentations. In E. salvelini, the apical disc is bilobed and bilaterally symmetric. We found new and significant interspecific differences in the length and width of the scolex, the diameter of the apical disc, and the width of the neck, with all measurements being larger in E. crassum. The two species differ in the number and size of the testes (fewer and larger in E. salvelini), the length of the cirrus sac (longer in E. crassum), and the size of vitelline follicles (larger in E. salvelini). Vitelline follicles of E. crassum are always cortical and sometimes enter into the outermost muscle fibres, whereas follicles of E. salvelini are situated largely medullary with few follicles entering between the innermost bundles of muscles. The eggs and the oncospheres of E. salvelini are larger. The embryonic hooks of E. crassum measure 14–18 μm whilst those of E. salvelini are 18–26 μm. For both taxa, the intraspecific variability in morphometric characters was fairly low. The prevalence and intensity of infection of E. crassum and E. salvelini in their respective fish hosts were very high (prevalence 90–94% mean intensity 36.3 and 6.6, maximums of 172 and 63 tapeworms per fish, respectively). E. salvelini eggs were spontaneously released throughout the year except for winter months; E. crassum laid eggs only in summer (June–August). Natural infection of copepods with Eubothrium procercoids was very low (prevalence 0.002%). The morphogenesis of Eubothrium procercoids was studied in an intermediate host, the copepod Cyclops prealpinus, that had been simultaneously infected with both species.

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References cited

  • Akhmerov, A.C. 1962. On the biology of cestode Eubothrium crassum. Trudy Parasit. 12: 5–8 (in Russian).

    Google Scholar 

  • Amin, D.M. 1977. Helminth parasites of some south-western Lake Michigan fishes. Proc. Helminthol. Soc. Wash. 44: 210–217.

    Google Scholar 

  • Andersen, K.I. 1979. Studies on the scolex morphology of Eubothrium spp. with emphasis on characters usable in species discrimination and with brief references on the scolices of Bothriocephalus sp. and Triaenophorus spp. (Cestoda, Pseudophyllidea). Z. Parasitenk. 60: 147–156.

    Google Scholar 

  • Andersen, K.I. & C.R. Kennedy. 1983. Systematics of the genus Eubothrium Nybelin (Cestoda, Pseudophyllidea), with partial re-description of the species. Zool. Scr. 12: 95–105.

    Google Scholar 

  • Boyce, N.P. 1974. Biology of Eubothrium salvelini (Cestoda: Pseudophyllidea), a parasite of juvenile sockeye salmon (Oncorhynchus nerka) of Babine Lake, British Lake, British Columbia. J. Fish. Res. Board Can. 31: 1735–1742.

    Google Scholar 

  • Bristow, G.A. & B. Berland. 1991. The effect of long term, low level Eubothrium sp. infection on growth in farmed salmon (Salmo salar L.). Aquaculture 98: 325–330.

    Google Scholar 

  • Bush, A.O., K.D. Lafferty, J.M. Lotz & A.W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revised. J. Parasitol. 83: 575–583.

    Google Scholar 

  • Buchmann, K. & J. Bresciani. 1997. Parasitic infections in pondreared rainbow trout Oncorhynchus mykiss in Denmark. Dis. Aquat. Org. 28: 125–138.

    Google Scholar 

  • Chubb, J.C., D.W. Pool & C.J. Veltkamp. 1987. A key to the species of cestodes (tapeworms) parasitic in British and Irish freshwater fishes. J. Fish Biol. 31: 517–543.

    Google Scholar 

  • Dubinina, M.N. 1987. Class Cestoda Rudolphi, 1808. pp. 5–76. In: O.N. Bauer (ed.) Key to the Parasites of Freshwater Fishes of the USSR, Volume 3, Nauka, Leningrad (in Russian).

    Google Scholar 

  • Dubois, N., D.J. Marcogliese & P. Magnan. 1996. Effects of the introduction of white sucker, Catostomus commersoni, on the parasite fauna of brook trout Salvelinus fontinalis. Can. J. Zool. 74: 1304–1312.

    Google Scholar 

  • Due, T.T. & M.A. Curtis. 1995. Parasites of freshwater resident anadromous Arctic charr (Salvelinus alpinus) in Greenland. J. Fish Biol. 46: 578–592.

    Google Scholar 

  • Gerdeaux, D., M.A. Fillon & L. Van Overmeire. 1995. Arctic charr, Salvelinus alpinus, of Lake Annecy: yield, growth and parasitism by Eubothrium salvelini. Nordic J. Freshwat. Res. 71: 245–251.

    Google Scholar 

  • Hanzelová, V. & R. Žitnan. 1987. The effect of season on embryogenesis of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda). Biológia 42: 105–111.

    Google Scholar 

  • Hanzelová, V., T. Scholz, D. Gerdeaux & A. de Chambrier. 1999. Endoparasitic helminths of fishes in three alpine lakes in France and Switzerland. Rev. Suisse Zool. 106: 581–590.

    Google Scholar 

  • Hernandez, A.D. & P.M. Muzzall. 1998. Seasonal patterns in the biology of Eubothrium salvelini infecting brook trout in a creek in lower Michigan. J. Parasitol. 84: 1119–1123.

    Google Scholar 

  • Hoff, M.H., N.M Pronin & D.R. Baldanova. 1997. Parasites of lake herring (Coregonus artedi) from Lake Superior, with special reference to use of parasites as markers of stock structure. J. Great Lakes Res. 23: 458–467.

    Google Scholar 

  • Hoffmann, R., C.R. Kennedy & J. Meder. 1986. Effects of Eubothrium salvelini Schrank (1790), on Arctic charr, Salvelinus alpinus (L.), in an alpine lake. J. Fish Dis. 9: 153–157.

    Google Scholar 

  • Holland, C.V. & C.R. Kennedy. 1997. A checklist of parasitic helminth and crustacean species recorded in freshwater fish from Ireland. Proceedings of the Royal Irish Academy 97B: 225–243.

    Google Scholar 

  • Ingham, L. & C. Arme. 1973. Intestinal helminths in rainbow trout, Salmo gairdneri (Richardson): absence of effect on nutrient absorption and fish growth. J. Fish Biol. 5: 309–313.

    Google Scholar 

  • Kennedy, C.R. 1978a. Studies on the biology of Eubothrium salvelini and E. crassum in resident and migratory Salvelinus alpinus and Salmo trutta and S. salar in North Norway and the islands of Spitsbergen and Jan Mayen. J. Fish Biol. 12: 147–162.

    Google Scholar 

  • Kennedy, C.R. 1978b. The biology, specificity and habitat of the species of Eubothrium (Cestoda: Pseudophyllidea), with reference to their use as biological tags: a review. J. Fish Biol. 12: 393–410.

    Google Scholar 

  • Kennedy, C.R. 1996. Establishment, survival and site selection of the cestode Eubothrium crassum in brown trout, Salmo trutta. Parasitology 112: 347–355.

    Google Scholar 

  • Král'ová, I., V. Hanzelová, T. Scholz, D. Gerdeaux & M. Špakulová. 2001. A comparison of the internal transcribed spacer of ribosomal DNA for Eubothrium crassum and Eubothrium salvelini (Cestoda: Pseudophyllidea), parasites of salmonid fish. Int. J. Parasitol. 31: 93–96.

    Google Scholar 

  • Kuperman, B.I. 1978. The cestodes Eubothrium salvelini and Eubothrium crassum from salmon of the Kamchatka waters: characteristics of the life cycle and biology. Biologiya Morya 4: 53–60 (in Russian).

    Google Scholar 

  • Lafferty, K.D. 1999. The evolution of trophic transmission. Parasitol. Today 15: 111–115.

    Google Scholar 

  • Margolis, L. & J.R. Arthur. 1979. Synopsis of the parasites of Canada. Bull. Fish. Res. Board Can. 179: 1–269.

    Google Scholar 

  • Margolis, L., G.W. Esch, J.C. Holmes, A.M. Kuris & G.A. Schad. 1982. The use of ecological terms in parasitology. J. Parasitol. 68: 131–133.

    Google Scholar 

  • Muzzall, P.M. 1993. Eubothrium salvelini (Cestoda: Pseudophyllidea) in brook trout, Salvelinus fontinalis, from westcentral lower Michigan. J. Helminthol. Soc. Wash. 60: 134–137.

    Google Scholar 

  • Muzzal, P.M. 1994. Parasites of alewives, Alosa pseudoharengus, from the Great lakes. J. Helminthol. Soc. Wash. 61: 67–72.

    Google Scholar 

  • Nybelin, O.N. 1922. Anatomisch-systematischen Studien über Pseudophyllidien. Göteborgs Kungliga Vetenskaps-och Vitterhets Samhälles Handlingar 26: 1–228.

    Google Scholar 

  • Pasternak, A.F., F.A. Huntingford & D.W. Crompton, 1995. Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110: 395–399.

    Google Scholar 

  • Pool, D.V. 1987. A note on the synonymy of Bothriocephalus acheilognathi Yamaguti, 1934, B. aegyptiacus Ryšavý and Moravec, 1975 and B. kivuensis Baer and Fain, 1958. Parasitol. Res. 73: 146–150.

    Google Scholar 

  • Pool, D.V. & J.C. Chubb. 1985. Acritical scanning electron microscope study of the scolex of Bothriocephalus acheilognathi Yamaguti, 1934, with a review of the taxonomic history of the genus Bothriocephalus parasitizing cyprinid fishes. Syst. Parasitol. 7: 199–211.

    Google Scholar 

  • Poulin, M., A. Curtis & M.E. Rau. 1992. Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105: 265–271.

    Google Scholar 

  • Pulkkinen, K., A.F. Pasternak, T. Hasu & E.T. Valtonen. 2000. Effect of Triaenophorus crassus (Cestoda) infection on behaviour and susceptibility to predation of the first intermediate host Cyclops strenuus (Copepoda). J. Parasitol. 86: 664–670.

    Google Scholar 

  • Scholz, T. 1991. Studies on the development of the cestode Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidae) under experimental conditions. Folia Parasitol. 38: 39–55.

    Google Scholar 

  • Scholz, T. & V. Hanzelová. 1998. Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Studie 2, Academia, Praha. 118 pp.

    Google Scholar 

  • Smith, H.D. 1973. Observations on the cestode Eubothrium salvelini in juvenile stockeye salmon (Oncorhynchus nerka) at Babine Lake, British Columbia. J. Fish. Res. Board Can. 30: 947–964.

    Google Scholar 

  • Sobecka, E. & W. Piasecky. 1993. Parasitic fauna of Arctic charr, Salvelinus alpinus (L., 1758) from the Hornsund region (Spitsbergen). Acta Ichthyologica et Piscatoria 23: 99–106.

    Google Scholar 

  • Sysoev, A.V. 1983. The composition of intermediate hosts of Proteocephalus torulosus (Batsch) (Cestoda: Proteocephalidae) and the dynamics of invasion of Copepoda with this parasite under conditions of Karelia. Helminthologia 20: 97–102.

    Google Scholar 

  • Vik, R. 1963. Studies of the helminth fauna of Norway IV: occurrence and distribution of Eubothrium crassum (Bloch, 1779) and Eubothrium salvelini (Schrank, 1790) (Cestoda) in Norway, with notes on their life cycles. Nytt. Mag. Zool. 11: 47–73.

    Google Scholar 

  • Williams, H. & A. Jones. 1994. Parasitic worms of fish. Taylor & Francis Ltd., London. 593 pp.

    Google Scholar 

  • Wootten, R. 1972. Occurrence of Eubothrium crassum (Bloch, 1779) (Cestoda: Pseudophyllidea) in brown trout Salmo trutta L., and rainbow trout S. gairdneri Richardson, 1836, from Hanningfield Reservoir, Essex. J. Helminthol. 46: 327–339.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01, Košice, Slovakia

    Vladimíra Hanzelová

  2. Laboratoire d'hydrobiologie lacustre, INRA, 75 avenue de Corzent, 74203, Thonon, France

    Vladimíra Hanzelová & Daniel Gerdeaux

  3. Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Tomáš Scholz

  4. Faculty of Biological Sciences, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Roman Kuchta

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  1. Vladimíra Hanzelová
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  2. Tomáš Scholz
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  3. Daniel Gerdeaux
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  4. Roman Kuchta
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Hanzelová, V., Scholz, T., Gerdeaux, D. et al. A Comparative Study of Eubothrium Salvelini and E. crassum (Cestoda: Pseudophyllidea) Parasites of Arctic Charr and Brown Trout in Alpine Lakes. Environmental Biology of Fishes 64, 245–256 (2002). https://doi.org/10.1023/A:1016014505671

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