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Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population

Published online by Cambridge University Press:  05 January 2012

M. VANACKER ,
G. MASSON  and
J-N. BEISEL
M. VANACKER
Affiliation:
Université Paul Verlaine –Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosytèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, Rue du Général Delestraint, F-57070 Metz, France
G. MASSON
Affiliation:
Université Paul Verlaine –Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosytèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, Rue du Général Delestraint, F-57070 Metz, France
J-N. BEISEL*
Affiliation:
Université Paul Verlaine –Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosytèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, Rue du Général Delestraint, F-57070 Metz, France
*
*Corresponding author: Tel: +33(0)387378429. Fax: +33(0)387378423. E-mail: beisel@univ-metz.fr
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Summary

Sampling of the fish community was carried out for 20 years in the Mirgenbach reservoir, in North-Eastern France. The prevalence and the mean intensity of Ligula intestinalis (Cestoda) were analysed in roach (Rutilus rutilus) and silver bream (Blicca bjoerkna) populations, the main two infected species. The aim of this study was to investigate the host switch from roach to silver bream and the consequences of L. intestinalis infestation in silver bream, which is an unusual host for this parasite as Ligula parasitism in silver bream appears to be rare. We analysed in detail the relationships between parasitism index (PI), gonadosomatic index (GSI), perivisceral fat abundance (PFA) and condition index (CI) in the silver bream population. In 1998, prevalence of L. intestinalis highlighted a clear host switch from roach to silver bream. In the silver bream population, young fish were the most severely infected and the impact of plerocercoids appeared to be different depending on the host sex. In male silver bream, plerocercoids drew energy from fat reserves even if GSI was also slightly impacted. On the contrary, in females energy was diverted from gonad maturation rather than from perivisceral fat reserves. No significant difference was observed in terms of CI in either sex.

Keywords

Ligula intestinalissilver breamroachhost switchparasitism indexgonadosomatic indexcondition indexperivisceral fat
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 406 - 417
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Arme, C. (1968). Effects of the plerocercoids larva of a pseudophyllidean cestode, Ligula intestinalis, on the pituitary gland and gonads of its host. Biological Bulletin 134, 15–25.CrossRefGoogle Scholar
Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in british fishes. The Journal of Parasitology 54, 272–280.CrossRefGoogle ScholarPubMed
Baglinière, J. L. and Le Louarn, H. (1987). Caractéristiques sclalimétriques des principales espèces de poissons d'eau douce de France. Bulletin Français de la Pêche et de la Pisciculture 306, 1–39. doi: 10.1051/kmae:1987005.CrossRefGoogle Scholar
Barber, I. and Svensson, P. A. (2003). Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126, 359–367. doi: 10.1017/S0031182002002925.CrossRefGoogle ScholarPubMed
Barnabé, G. (1994). Biological basis of fish culture. In Aquaculture Biology and Ecology of Cultured Species (ed. Barnabé, G.), pp. 227–372. Ellis Horwood, New York, USA.CrossRefGoogle Scholar
Baruš, V. and Prokeš, M. (1994). Parasite load of Ligula intestinalis plerocercoids in adult silver bream Blicca bjoerkna. Helminthologia 31, 91–94. doi: 10.279/S11687-94.Google Scholar
Baruš, V. and Prokeš, M. (2002). Length and weight of Ligula intestinalis plerocercoids (Cestoda) parasitizing adult cyprinid fishes (Cyprinidae): a comparative analysis. Helminthologia 39, 29–34. doi: 10.278/S11687-02.Google Scholar
Billard, R., Bry, C. and Gillet, C. (1981). Stress, environment and reproduction in teleost fish. Stress and Fish 9, 185–208.Google Scholar
Bouzid Lamine, W. (2008). Structure génétique de Ligula intestinalis (Cestode: Diphyllobothriidea), parasite des poissons d'eau douce. Thèse de l'Université Toulouse III, Paul Sabatier, France.Google Scholar
Brown, S. P., Loot, G., Grenfell, B. T. and Guégan, J-F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519–529. doi: 10.1017/S0031182001008678.CrossRefGoogle ScholarPubMed
Carter, V., Pierce, R., Dufour, S., Arme, C. and Hoole, D. (2005). The tapeworm Ligula intestinalis (cestoda: Pseudophyllidae) inhibits LH expression and puberty in its teleost host Rutilus rutilus. Reproduction 130, 939–945. doi: 10.1530/rep.100742.CrossRefGoogle Scholar
CEN & AFNOR (2005). Water Quality – Sampling of Fish with Multi-mesh Gillnets. NF EN 14757.Google Scholar
Dembski, S. (2005). Stratégies d'occupation spatiale en milieu lacustre : réponses de l'ichtyofaune dans un réservoir échauffé, non stratifié. Thèse de doctorat: Sciences de la Vie, Hydrobiologie. Université de Metz, France.Google Scholar
Dembski, S., Masson, G., Wagner, P. and Pihan, J-C. (2008). Habitat use by YOY in the littoral zone of an artificially heated reservoir. International Revue of Hydrobiology 93, 243–255. doi: 10.1002/iroh.200710911.CrossRefGoogle Scholar
Dubinina, M. N. (1980). Tapeworms, (Cestoda, ligulidae) of the Fauna of the URSS. Amerind Publishing Co. Ltd, New Dehli, India.Google Scholar
Ergonul, M. B. and Altindag, A. (2005). The occurrence and dynamics of Ligula intestinalis in its cyprinid fish host tench Tinca tinca in Mogan lake (Ankara, Turkey). Veterinarni Medicina 12, 537–542.CrossRefGoogle Scholar
Flesch, A., Masson, G. and Moreteau, J-C. (1994). Comparaison de trois méthodes d’échantillonnage utilisées dans l’étude de la répartition de la perche (Perca fluviatilis) dans un lac-réservoir. Congrès International de Limnologie – Océanographie et Journées Ichtyologiques N°2, Evian, France (25/05/1983). Cybium 18, 39–56.Google Scholar
Flesch, A., Masson, G. and Moreteau, J-C. (1995). Temporal distribution of perch (Perca fluviatilis L.) in a lake-reservoir (Moselle, France): analysis of catches with vertical gill nets. Hydrobiologia 300–301, 335–343. doi: 10.1007/BF00024474.CrossRefGoogle Scholar
Geraudie, P., Gerbron, M., Hill, E. and Minier, C. (2010). Roach (Rutilus rutilus) reproductive cycle: a study of biochemical and histological parameters in a low contaminated site. Fish Physiology and Biochemistry 36, 767–777. doi: 10.1007/s10695-009-9351-5.CrossRefGoogle Scholar
Glazunova, A. A. and Polunina, Y. Y. (2009). Copepods as the first intermediate hosts of Ligula intestinalis L.: parasites of bream Abramis brama L. in the Vistula Lagoon of the Baltic Sea. Inland Water Biology 2, 371–376. doi: 10.1134/S1995082909040129.CrossRefGoogle Scholar
Hecker, M. and Karbe, L. (2005). Parasitism in fish – an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195–207. doi: 10.1016/j.aquatox.2004.12.008.CrossRefGoogle Scholar
Hecker, M., Sanderson, J. T. and Karbe, L. (2007). Suppression of aromatase activity in populations of bream (Abramis brama) from the river Elbe, Germany. Chemosphere 66, 542–552. doi: 10.1016/j.chemosphere.2006.05.046.CrossRefGoogle ScholarPubMed
Izumova, N. A. (1987). Parasitic Fauna of Reservoir Fishes of the URSS and its Evolution. Amerind Publishing CO. Pvt. Ltd, New Dehli, India.Google Scholar
Kennedy, C. R., Shears, P. C. and Shears, J. A. (2001). Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257–269. doi: 10.1017/S0031182001008538.CrossRefGoogle ScholarPubMed
Korkmaz, A. S. and Zencir, O. (2009). Annual dynamics of tapeworm, Ligula intestinalis in tench (Tinca tinca) from Beysehir Lake, Turkey. Journal of Animal and Veterinary Advances 8, 1790–1793. doi: 10.3923/java.2009.1790.1793.Google Scholar
Kosheva, A. F. (1956). Influence of the parasites Ligula intestinalis and Digramma interrupta on their fish hosts. Zoologicheski Zhurdal 35, 1629–1632.Google Scholar
Loot, G., Lek, S., Brown, S. P. and Guégan, J-F. (2001 a). Phenotypic modification of roach (Rutilus Rutilus L.) infected with Ligula intestinalis L. (Cestoda : Psedophyllidea). The Journal of Parasitology 87, 1002–1010.CrossRefGoogle ScholarPubMed
Loot, G., Lek, S., Dejean, D. and Guégan, J-F. (2001b). Parasite-induced mortality in three host populations of the roach Rutilus Rutilus (L.) by the tapeworm Ligula intestinalis (L.). Annales de Limnologie 37, 151–159. doi: 10.1051/limn/2001010.CrossRefGoogle Scholar
Loot, G., Poulin, R., Lek, S. and Guégan, J-F. (2002). The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural population of roach, Rutilus rutilus (L.). Ecology of Freshwater Fish 11, 1–10. doi: 10.1034/j.1600-0633.2002.00006.x.CrossRefGoogle Scholar
Loot, G., Park, Y. S., Lek, S. and Brosse, S. (2006). Encounter rate between local populations shapes host selection in complex parasite life cycle. Biological Journal of the Linnean Society 89, 99–106. doi: 10.1111/j.1095-8312.2006.00661.x.CrossRefGoogle Scholar
Lukšiené, D., Sandström, O., Lounasheimo, L. and Andersson, J. (2000). The effects of thermal effluent exposure on the gametogenesis of female fish. Journal of Fish Biology 56, 37–50. doi: 10.1111/j.1095-8649.2000.tb02085.x.CrossRefGoogle Scholar
Maazouzi, C., Masson, G., Izquierdo, M. S. and Pihan, J-C. (2007). Fatty acid composition of the amphipod Dikerogammarus villosus: Feeding strategies and trophic links. Comparative Biochemistry and Physiology Part A 147, 868–875. doi: 10.1016/j.cbpa2007.02.010.CrossRefGoogle ScholarPubMed
Maazouzi, C., Masson, G., Izquierdo, M. S. and Pihan, J-C. (2008). Midsummer heat wave effects on lacustrine plankton: variation of assemblage structure and fatty acid composition. Journal of Thermal Biology 33, 287–296. doi: 10.1016/j.jtherbio.2008.03.002.CrossRefGoogle Scholar
Magalhaes, A. L. B., Bazzoli, N., Santos, G. B. and Rizzo, E. (2004). Reproduction of the South American dogfish characid, Galaeocharax knerii, in two reservoirs from upper Parana River basin, Brazil. Environmental Biology of Fishes 70, 415–425. doi: 10.1023/B:EBFI.0000035436.83329.e8.CrossRefGoogle Scholar
Malek, M., Haseli, M., Mobedi, M. R., Ganjali, M. R. and MacKenzie, K. (2007). Parasites as heavy metal bioindicators in the shark Carcharhinus dussumieri from the Persian Gulf. Parasitology 134, 49–254. doi: 10.1017/S0031182007002508.CrossRefGoogle ScholarPubMed
Marzou, R. (1996). Etude des crustacés planctoniques d'une retenue soumise à des rejets thermiques: description, dynamique et relations avec le peuplement pisciaire. Thèse de l'Université Metz, UFR SciFA, Centre de Recherches Ecologique, Equipe Démoécologie, France.Google Scholar
Masson, G., Dembski, S., Staffolani, F., Wagner, P., Valente, E., Maazouzi, C., Banas, D., Poinsaint, J-F. and Pihan, J-C. (2008). Les populations de poisons dans le réservoir du Mirgenbach (1986–2006. CNPE Cattenom. France): un modèle pour l’étude des effets d'un changement thermique global? Hydroécologie Appliquée 16, 135–167. doi: 10.1051/hydro/2009007.CrossRefGoogle Scholar
Minier, C., Maltret, P., Monsinjon, T., Knigge, T., Leray, J., Lecomte, C., Barka, S., Denier, X., Amara, R., Selleslagh, J., Hill, E. M., Rotchell, J. M., Cubero, E., Ciocan, C., Dussart, G., Trigwell, J., St Pierre, S., Pringle, N. and Pepper, R. (2009). A study on consequences of the tapeworm Ligula intestinalis on its teleost host, the roach (Rutilus rutilus). In Risk Analysis Associated with Endocrine Disruption in the Manche Regions (RAED). Final Report Phase II. Franco-British Interreg European Programme 92–100.Google Scholar
Murua, H. and Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science 33, 23–31.CrossRefGoogle Scholar
Museth, J. (2001). Effects of Ligula intestinalis on habitat use. predation risk and catchability in European minnows. Journal of Fish Biology 59, 1070–1080. doi:10.1006:jfbi.2001.1720.CrossRefGoogle Scholar
Oyoo-Okoth, E., Admiraal, W., Osano, O., Kraak, M. H. S., Ngure, V., Makwali, J. and Orina, P. S. (2010). Use of the fish endoparasite, Ligula intestinalis (L., 1758) in an intermediate cyprinid host (Rastreneobola argentea) for biomonitoring metal contamination in Lake Victoria, Kenya. Lakes & Reservoirs: Research and Management 15, 63–73. doi: 10.1111:j.1440-1770.2010.00423.x.CrossRefGoogle Scholar
Pinder, A. C. (2001). Keys to Larval and Juvenile Stages of Coarse Fishes from Fresh Waters in the British Isles. Freshwater Biological Association. The Ferry House, Ambleside, UK.Google Scholar
Shargh, S., Shamsaii, M. and Karamini, S. (2008). Distribution of parasitic cestod “Ligula intestinalis” in Mazandaran region. Iranian Journal of Parasitology 3, 26–33.Google Scholar
Shields, B. A., Groves, K. L., Rombauch, C. and Bellmore, R. (2002). Ligulosis associated with mortality in largescale suckers. Journal of Fish Biology 61, 448–455. doi: 10.1006/jfbi:2002.2051.CrossRefGoogle Scholar
Simpkins, D. G. and Hubert, W. A. (1996). Proposed revision of the standard-weight equation for rainbow trout. Journal of Freshwater Ecology 11, 319–325. doi: 10.1080/02705060.1996.9664454.CrossRefGoogle Scholar
Spillman, C. J. (1961). Poissons d'Eau Douce (ed. Lechevallier, P.) Faune de France, Paris, France.Google Scholar
Sures, B. (2001). The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquatic Ecology 35, 245–255. doi: 10.1023/A:1011422310314.CrossRefGoogle Scholar
Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177. doi: 10.1016/j.PT.2004.01.014.CrossRefGoogle ScholarPubMed
Trubiroha, A., Wuertz, S., Frank, S. N., Sures, B. and Kloas, W. (2009). Expression of gonadrophin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). International Journal of Parasitology 39, 1465–1473. doi: 10.1016/j.ijpara.2009.05.003.CrossRefGoogle Scholar
Vein, D., Gigleux, M., Flesch, A., Pierre, J-F., Marzou, R. and Pihan, J-C. (1990). Trophic evolution of a reservoir with overheated waters: nuclear power station at Cattenom, Moselle, East France. Annales de Limnologie – International Journal of Limnology 27, 87–98. doi: 10.1051/limn/1991006.CrossRefGoogle Scholar
Vinot, I. and Pihan, J-C. (2005). Circulation of copper in the biotic compartments of a freshwater damned reservoir. Environmental Pollution 133, 169–182. doi: 10.1016/j.envpol.2004.03.002.CrossRefGoogle Scholar
Wallace, R. and Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist 21, 325–343.CrossRefGoogle Scholar
Zimmermann, S., Sures, B. and Taraschewski, H. (1999). Experimental studies on lead accumulation in the eel-specific endoparasites Anguillicola crassus (Nematoda) and Paratenuisentis ambiguous (Acanthocephala) as compared with their host, Anguilla anguilla. Archives of Environmental Contamination and Toxicology 37, 190–195.CrossRefGoogle Scholar