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Endocrine effects of the tapeworm Ligula intestinalis in its teleost host, the roach (Rutilus rutilus)

Published online by Cambridge University Press:  07 December 2009

P. GERAUDIE*
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
C. BOULANGE-LECOMTE
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
M. GERBRON
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
N. HINFRAY
Affiliation:
Institut National de l'Environnement Industriel et des Risques, Unité d'évaluation des Risques, BP 2, 60550Verneuil-en-Halatte, France
F. BRION
Affiliation:
Institut National de l'Environnement Industriel et des Risques, Unité d'évaluation des Risques, BP 2, 60550Verneuil-en-Halatte, France
C. MINIER
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
*
*Corresponding author: Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France. Tel: +33 232 74 43 90. Fax: +33 232 74 43 14. E-mail: perrine.maltret@univ-lehavre.fr

Summary

The effects of parasite infection by the cestode Ligula intestinalis on the reproductive function and endocrine system of wild roach Rutilus rutilus were evaluated. Gonad maturation, plasma vitellogenin, plasma steroid concentrations (i.e. progesterone, 11-keto-testosterone and 17-β-estradiol) and brain aromatase activity were investigated in relation with parasitization. A low prevalence (8%) of ligulosed roach and a moderate impact of parasitization (mean parasitization index of 8·8%) were found in the studied population. Inhibition of gonad maturation generally resulted from infestation but 5% of the ligulosed roach nevertheless reached maturity. Main sex steroid plasma content was depleted in both genders. Male 11-keto-testosterone, female 17-β-estradiol and progesterone plasma concentrations of both genders were, respectively, 27, 5 and 3 times lower in ligulosed fish when compared to their non-infected counterparts. Progesterone levels were negatively correlated with the parasitization index in females. Brain aromatase activity of infected roach was reduced to 50% of that of the non-infected fish. These results demonstrate significant negative effects on the reproductive function of wild roach infected by the tapeworm L. intestinalis collected from a site with low contamination.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infection in British fishes. Journal of Parasitology 54, 272280.CrossRefGoogle ScholarPubMed
Arme, C. (1997). Ligula intestinalis: Interaction with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 8384.CrossRefGoogle Scholar
Barus, V. and Prokes, M. (2002). Length and weight of Ligula intestinalis plerocercoids (Cestoda) parasitizing adult cyprinid fishes (Cyprinidae): a comparative analysis. Helminthologia 39, 2934.Google Scholar
Blanar, C. A., Munkittrick, K. R., Houlahan, J., MacLatchy, D. L. and Marcogliese, D. J. (2009). Pollution and parasitism in aquatic animals: A meta-analysis of effect size. Aquatic Toxicology 93, 1828.CrossRefGoogle ScholarPubMed
Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Carter, V., Pierce, R., Dufour, S., Arme, C. and Hoole, D. (2005). The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 130, 939945.CrossRefGoogle ScholarPubMed
Claisse, D. (1989). Chemical contamination of French coasts: The results of ten years mussel watch. Marine Pollution Bulletin 20, 523528.CrossRefGoogle Scholar
Couteau, J., Flaman, J. M., Minier, C. and Cachot, J. (2008) Detection of environmental mutagens using the Facim assay. Marine Environmental Research 66, 6263.CrossRefGoogle ScholarPubMed
Dence, W. (1958). Studies on ligula-infected common shiners (Notropis cornutus frontalis Agassiz) in the Adirondacks. Journal of Parasitology 44, 334338.CrossRefGoogle ScholarPubMed
Fulton, T. W. (1904). The rate of growth of fishes. Fisheries Board of Scotland, Annual Report 22, Part 3, pp. 141241.Google Scholar
Geraudie, P., Gerbron, M., Hill, E. and Minier, C. (2009). Roach (Rutilus rutilus) reproductive cycle: a study of biochemical and histological parameters in a low contaminated site. Fish Physiology and Biochemistry. (in the Press.) DOI: 10.1007/s10695-009-9351-5.Google Scholar
Hecker, M. and Karbe, L. (2005). Parasitism in fish-an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195207.CrossRefGoogle ScholarPubMed
Hecker, M., Sanderson, T. J. and Karbe, L. (2007). Suppression of aromatase activity in populations of bream (Abramis brama) from the river Elbe, Germany. Chemosphere 66, 542552.CrossRefGoogle ScholarPubMed
Hoole, D. (1994). Tapeworm infections in fish: past and future problems. In Parasitic Diseases of Fish (ed. Pike, A. W. and Lewis, J. W.), pp. 119140. Samara Publishing Ltd. Tresaith, Dyfed, UK.Google Scholar
Jafri, S. I. H. (1990) Gametogenesis in roach, Rutilus rutilus (L.) (Cyprinidae: Teleostei). Pakistan Journal of Zoolology 22, 361377.Google Scholar
Jobling, S., Beresford, N., Nolan, M., Rodgers-Gray, T., Brighty, G. C., Sumpter, J. P., Tyler, C. R. (2002) Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biology of Reproduction 66, 272–228.CrossRefGoogle ScholarPubMed
Jobling, S. and Tyler, C. (2003). Endocrine disruption, parasites and pollutants in wild freshwater Fish Parasitology 126, S103S108.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Burrough, R. J. (1981). The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.). Journal of Fish Biology 19, 115126.CrossRefGoogle Scholar
Kennedy, C. R., Shears, P. C. and Shears, J. A. (2001). Long-term dynamics of Ligula intestinalis and Rutilus rutilus: a study of three epizootic cycles over 31 years. Parasitology 123, 257269.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925931.CrossRefGoogle Scholar
Loot, G., Poulin, R., Lek, S. and Guegan, J.-F. (2002). The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural populations of roach, Rutilus rutilus (L.). Ecology of Freshwater Fish 11, 168177.CrossRefGoogle Scholar
MacKenzie, K. (1999). Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38, 955959.CrossRefGoogle Scholar
Martín-Skilton, R., Lavado, R., Thibaut, R., Minier, C. and Porte, C. (2006). First evidence of endocrine disruption in red mullets – Mullus barbatus – from the NW Mediterranean Sea. Environmental Pollution 141, 6068.CrossRefGoogle Scholar
Minier, C., Caltot, G., Leboulenger, F. and Hill, E. M. (2000). An investigation of the incidence of intersex fish in Seine-Maritime and Sussex regions. Analysis 28, 801806.Google Scholar
Minier, C., Abarnou, A., Le Guellec, A.-M., Jaouen-Madoulet, A., Tutundjian, R., Bocquené, G. and Leboulenger, F. (2006). A pollution monitoring pilot study involving chemical analysis and biomarker measurements in the Seine estuary using zebra mussels (Dreissena polymorpha). Environmental Toxicology and Chemistry 25, 112119.CrossRefGoogle ScholarPubMed
Peck, M. R., Labadie, P., Minier, C. and Hill, E. M. (2007). Profiles of environmental and endogenous estrogens in the zebra mussel (Dreissena polymorpha). Chemosphere 69, 18.CrossRefGoogle ScholarPubMed
Schulz, R. W., de França, L. R., Lareyre, J. J., Legac, F., Chiarini-Garcia, H., Nobrega, R. H. and Miura, T. (2009). Spermatogenesis in fish. General and Comparative Endocrinology (in the Press.) doi:10.1016/j.ygcen.2009.02.013.Google ScholarPubMed
Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170177.CrossRefGoogle ScholarPubMed
Taylor, M. J. and Hoole, D. (1995). The chemiluminescence of cyprinid leucocytes in response to zymosan and extracts of Ligula intestinalis (Cestoda). Fish and Shellfish Immunology 5, 191198.CrossRefGoogle Scholar
Thompson, E. A. and Siiteri, P. K. (1974). Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatization of androstenedione. Journal of Biological Chemistry 219, 53645372.CrossRefGoogle Scholar
Van Dobben, W. H. (1952). The food of the cormorant in the Netherlands, Ardea 40, 163.Google Scholar
Wilson, R. S. (1971). The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129137.CrossRefGoogle Scholar
Yavuzcan, H., Korkmaz, A. S. and Zencir, O. (2003). The infection of tench (Tinca tinca) with Ligula intestinalis plerocercoids in Lake Beysehir (Turkey). Bulletin of the European Association of Fish Pathologists 23, 223227.Google Scholar