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Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model?

Published online by Cambridge University Press:  18 February 2010

D. HOOLE ,
V. CARTER  and
S. DUFOUR
D. HOOLE*
Affiliation:
School of Life Sciences, Huxley Building, Keele University, Keele, Staffordshire, ST5 5BG, UK
V. CARTER
Affiliation:
School of Life Sciences, Huxley Building, Keele University, Keele, Staffordshire, ST5 5BG, UK
S. DUFOUR
Affiliation:
UMR BOREA Biologie des Organismes et Ecosystèmes Aquatiques, CNRS 7208/IRD 207/ /MNHN/UPMC Musėum National d'Histoire Naturelle, 7 rue Cuvier, 75231Pariscedex 05, France
*
*Corresponding author: School of Life Sciences, Huxley Building, Keele University, Keele, Staffordshire, ST5 5BG, UK. Tel: +44 (0)1782 733673; Fax: +44 (0)1782 733516; E-mail: d.hoole@biol.keele.ac.uk
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Summary

Since its use as a model to study metazoan parasite culture and in vitro development, the plerocercoid of the tapeworm, Ligula intestinalis, has served as a useful scientific tool to study a range of biological factors, particularly within its fish intermediate host. From the extensive long-term ecological studies on the interactions between the parasite and cyprinid hosts, to the recent advances made using molecular technology on parasite diversity and speciation, studies on the parasite have, over the last 60 years, led to significant advances in knowledge on host-parasite interactions. The parasite has served as a useful model to study pollution, immunology and parasite ecology and genetics, as well has being the archetypal endocrine disruptor.

Keywords

L. intestinalisendocrine disruptionpollutionimmunologyparasite ecologyparasite speciation
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 425 - 438
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Abd Allah, A. T., Wanas, M. Q. S. and Thompson, S. N. (1997). Effects of heavy metals on survival and growth of Biomphalaria glabrata Say (Gastropoda: Pulmonata) and interaction with Schistosome infection. Journal of Molluscan Studies 63, 79–86.CrossRefGoogle Scholar
Adamek, Z., Barus, V. and Prokes, M. (1996). Summer diet of roach (Rutilus rutilus) infested by Ligula intestinalis (Cestoda) plerocercoids in the Dalesice Reservoir (Czech Republic). Folia Zoologica 45, 347–354.Google Scholar
Antonopoulou, E., Mayer, I., Borg, B., Swanson, P., Murza, I. and Christoforov, O. (1999). Effects of testosterone on gonadotropins, testes, and plasma 17alpha, 20beta-dihydroxy-4-pregnene-3-one levels in postbreeding mature Atlantic salmon, Salmo salar, male parr. Journal of Experimental Zoology 284, 425–436.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Arme, C. (1968). Effects of the plerocercoid 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. (1975). Tapeworm-host interactions. In Symbiosis (ed. Jennings, D. H. and Lee, D. L.), pp 505–532. Cambridge University Press, Cambridge.Google Scholar
Arme, C. (1997). Ligula intestinalis: interactions with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 83–84.CrossRefGoogle Scholar
Arme, C., Griffiths, D. V. and Sumpter, J. P. (1982). Evidence against the hypothesis that the plerocercoid larva of Ligula intestinalis (Cestoda: Pseudophyllidea) produces a sex steroid that interferes with host reproduction. Journal of Parasitology 68, 169–171.CrossRefGoogle Scholar
Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fishes. Journal of Parasitology 54, 272–280.CrossRefGoogle ScholarPubMed
Aydogdu, A., Selver, M. and Cirak, V. K. (2008). Comparison of helminth species and their prevalence in rudd (Scardinius erythrophalmus L. 1758) in Golbasi Dam Lake and Kocadere Stream in Bursa Province of Turkey. Turkish Journal of Veterinary and Animal Sciences 32, 389–393.Google Scholar
Barber, I. and Huntingford, F. A. (1996). Parasite infection alters schooling behaviour: Deviant positioning of helminth-infected minnows in conspecific groups. Proceedings of the Royal Society of London Series B-Biological Sciences 263, 1095–1102.Google Scholar
Barus, V. and Prokes, M. (1994). Parasite load of Ligula intestinalis plerocercoids in adult silverbream, Blicca bjoerkna. Helminthologia 31, 91–94.Google Scholar
Barus, V., Sebela, M. and Prokes, M. (1997). On the possible free-living phase of the Ligula intestinalis plerocercoids (Ligulidae). Helminthologia 34, 173–174.Google Scholar
Barus, V., Tenora, F. and Kracmer, S. (2000). Heavy metal (Pb, Cd) concentrations in adult tapeworms (Cestoda) parasitizing birds. Helminthologia 37, 131–136.Google Scholar
Barus, V., Tenora, F., Kracmar, S. and Prokes, M. (2001). Accumulation of heavy metals in Ligula intestinalis plerocercoids (Pseudophyllidea) of different age. Helminthologia 38, 29–33.Google Scholar
Bauer, O. N. and Stolyarov, V. P. (1961). Formation of the parasite fauna and parasitic diseases of fish in hydroelectric reservoirs. In: Parasitology of Fishes (ed. Dogiel, V. A., Petrushevski, G. K. and Polyanski, Y. L.), pp. 246–254. Oliver and Boyd, London.Google ScholarPubMed
Bean, C. W. and Winfield, I. J. (1989). Biological and ecological effects of a Ligula intestinalis (L.) infestation of the gudgeon, Gobio gobio (L.) in Lough Neagh, Northern Ireland. Journal of Fish Biology 34, 135–147.CrossRefGoogle Scholar
Bean, C. W. and Winfield, I. J. (1992). Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Netherlands Journal of Zoology 42, 416–429.Google Scholar
Berglund, I., Antonopoulou, E., Mayer, I. and Borg, B. (1995). Stimulatory and inhibitory effects of testosterone on testes in Atlantic salmon male parr. Journal of Fish Biology 47, 586–598.CrossRefGoogle Scholar
Black, G. A. and Fraser, J. M. (1984). Dynamics of Ligula intestinalis (L.) in Catastomus commersoni (Lacėpėde). Journal of Fish Biology 25, 139–146.CrossRefGoogle Scholar
Bouzid, W., Lek, S., Mace, M., Ben Hassine, O. K., Etienne, R., Legal, L. and Loot, G. (2008 b). Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. Journal of Zoological Systematics and Evolutionary Research 46, 289–296.CrossRefGoogle Scholar
Bouzid, W., Stefka, J., Hypsa, V., Lek, S., Scholz, T., Legal, L., Ben Hassine, O. K. and Loot, G. (2008 a). Geography and host specificity: Two forces behind the genetic structure of freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). International Journal for Parasitology 38, 1465–1479.CrossRefGoogle ScholarPubMed
Britton, J. R., Jackson, M. C. and Harper, D. M. (2009). Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology 136, 1367–1373.CrossRefGoogle Scholar
Brown, S. P., Loot, G., Grenfell, B. T. and Geugan, J. F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation. Parasitology 123, 519–529.CrossRefGoogle ScholarPubMed
Brown, S. P., Loot, G., Teriokhin, A., Brunel, A., Brunel, C. and Guegan, J. F. (2002). Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation? International Journal for Parasitology 32, 817–824.CrossRefGoogle ScholarPubMed
Burrough, R. J. and Kennedy, C. R. (1979). The occurrence and natural alleviation of stunting in a population of roach, Rutilus rutilus (L.). Journal of Fish Biology 15, 93–109.CrossRefGoogle Scholar
Carreau, S., Bourguiba, S., Lambard, S., Galeraud-Denis, I., Genissel, C. and Levallet, J. (2002). Reproductive system: aromatase and estrogens. Molecular and Cellular Endocrinology 193, 137–143.CrossRefGoogle ScholarPubMed
Carter, V., Pierce, R., Dufour, S., Arme, C. and Hoole, D. (2005). The tapeworm Ligula intesinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 130, 939–945.CrossRefGoogle Scholar
Claridge, P. N., Hardisty, M. W., Potter, I. C. and Williams, C. V. (1985). Abundance, life history and ligulosis in the gobies (Teleosti) of the inner Severn estuary. Journal of the Marine Biological Association of the United Kingdom 65, 951–968.CrossRefGoogle Scholar
Cowx, I. G., Rollins, D. and Tumwebaze, R. (2008). Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. Journal of Fish Biology 73, 2249–2260.CrossRefGoogle Scholar
Crews, A. E. and Yoshino, T. P. (1989). Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Experimental Parasitology 68, 326–334.CrossRefGoogle ScholarPubMed
Cruz, M. and Canario, A. V. (1999). cDNA cloning and expression of brain and ovary aromatase in tilapia, Oreochromis mossambicus. Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish, Bergen, July 1999, 193.Google Scholar
Dejen, E., Vijverberg, J. and Sibbing, F. A. (2006). Spatial and temporal variation of cestode infection and its effects on two small barbs (Barbus humilis and Barbus tanapelagius) in Lake Tana, Ethiopa. Hydrobiologia 556, 109–117.CrossRefGoogle Scholar
Dubinina, M. N. (1966). Tapeworms (Cestoda, Ligulidae) of the Fauna of the USSR. Moscow; Nauka Publishers, Translation 1980, Amerind, New Dehli.Google Scholar
Dufour, S., Delerue-Le Belle, N. and Fontaine, Y. A. (1983). Development of a heterologous radioimmunoassay for eel (Anguilla anguilla L.) gonadotropin. General and Comparative Endocrinology 49, 404–413.CrossRefGoogle Scholar
Dufour, S., Weltzien, F.-A., Sebert, M.-E., Le Belle, N., Vidal, B., Vernier, P. and Pasqualini, C. (2005). Dopaminergic inhibition of reproduction in teleost fishes: ecophysiological and evolutionary implications. Annals of the New York Academy of Sciences 1040, 9–22.CrossRefGoogle ScholarPubMed
Ergonul, M. B. and Altindag, A. (2005 a). The effects of Ligula intestinalis plerocercoids on the growth features of tench, Tinca tinca. Turkish Journal of Veterinary and Animal Sciences 29, 1337–1341.Google Scholar
Ergonul, M. B. and Altindag, A. (2005 b). The occurrence and dynamics of Ligula intestinalis in its cyprinid fish host, tench Tinca tinca, in Morgan Lake (Ankara, Turkey). Veterinarni Medicina 50, 537–542.CrossRefGoogle Scholar
Feist, G. and Schreck, C. B. (1996). Brain-pituitary-gonadal axis during early development and sexual differentiation in the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology 102, 394–409.CrossRefGoogle ScholarPubMed
Fenton, A. and Rands, S. A. (2006). The impact of parasite manipulation and predator foraging behavior on predator-prey communities. Ecology 87, 2832–2841.CrossRefGoogle ScholarPubMed
Gonzalez, A. and Piferrer, F. (1999). Cytochrome p450 aromatase enzyme acivity and reproduction in teleost fish: studies in the European sea bass (Dicentrarchus labrax). Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish, Bergen, July 1999, 39–42.Google Scholar
Groves, K. L. and Shields, B. A. (2001). Observations on the plerocercoid stage of the tapeworm Ligula in three species of fish from the lower Crooked River of central Oregon. Journal of Aquatic Animal Health 13, 285–289.2.0.CO;2>CrossRefGoogle Scholar
Hajirostamloo, M. (2008). The occurrence and parasite-host of Ligula intestinalis in Sattarkhan Lake (East Azerbaijan-Iran). Journal of Animal and Veterinary Advances 7, 221–225.Google Scholar
Harries, J. E., Janbakshs, A., Jobling, S., Matthiessen, P., Sumpter, J. P. and Tyler, C. R. (1999). Estrogenic potency of effluent from two sewage treatment works in the United Kingdom. Environmental Toxicology and Chemistry 18, 932–937.CrossRefGoogle Scholar
Harries, J. E., Sheahan, D. A., Jobling, S., Matthiessen, P., Neall, P. R., Sumpter, J. P., Taylor, T. and Zaman, N. (1997). Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environmental Toxicology and Chemistry 16, 535–542.CrossRefGoogle Scholar
Harris, M. T. and Wheeler, A. (1974). Ligula infestation of bleak Alburnus alburnus (L.) in the tidal Thames. Journal of Fish Biology 6, 181–188.CrossRefGoogle Scholar
Hatice, T. K., Erdogan, Z. and Coz-rakovac, R. (2006). The occurrence of Ligula intestinalis (L.) observed in chub (Leuciscus cephalus L.) from Caparlipatlak Dam lake, Ivrindi-Balikesir, Turkey. Periodicum Biologorum 108, 183–187.Google Scholar
Hecker, M. and Karbe, L. (2005). Parasitism in fish – an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195–207.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. Chemophere 66, 542–552.CrossRefGoogle ScholarPubMed
Hernandez-Rauda, R., Otero, J., Rey, P., Rozas, G. and Aldegunde, M. (1996). Dopamine and serotonin in the trout (Oncorhynchus mykiss) pituitary: main metabolites and changes during gonadal recrudescence. General and Comparative Endocrinology 103, 13–23.CrossRefGoogle ScholarPubMed
Holmes, J. C. and Bethel, W. M. (1972). Modification of the intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. W. & Wright, C. A.). Journal of the Linnean Society 51, 123–149.Google Scholar
Hoole, D. (1994). Tapeworm infections in fish: past and present problems. In Parasitic Diseases of Fish (ed. Pike, A. D. & Lewis, J. W.), pp. 119–140. Samara Publishing Ltd, Tresaith, Dyfed.Google Scholar
Hoole, D (1997). The effects of pollutants on the immune response of fish: implications for helminths. Parassitologia 39, 219–225.Google Scholar
Hoole, D. and Arme, C. (1982). Ultrastructural studies on the cellular response of roach, Rutilus rutilus L., to the plerocercoid larva of the pseudophyllidean cestode, Ligula intestinalis. Journal of Fish Diseases 5, 131–144.CrossRefGoogle Scholar
Hoole, D. and Arme, C. (1983 a). Ligula intestinalis (Cestoda: Pseudophyllidea): An ultrastructural study on the cellular response of roach fry, Rutilus rutilus. International Journal for Parasitolology 13, 359–363.CrossRefGoogle Scholar
Hoole, D. and Arme, C. (1983 b). Ultrastructural studies on the cellular response of fish hosts following experimental infection with the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). Parasitology 87, 139–149.CrossRefGoogle Scholar
Hoole, D. and Arme, C. (1985). The in vitro culture and tegumental dynamics of the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). International Journal for Parasitology 16, 609–615.CrossRefGoogle Scholar
Hoole, D. and Arme, C. (1986). The role of serum leucocyte adherence to the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). Parasitology 92, 413–424.CrossRefGoogle Scholar
Hoole, D. and Arme, C. (1988). Ligula intestinalis (Cestoda: Pseudophyllidea): phosphorycholine inhibition of fish leucocyte adherence. Diseases of Aquatic Organisms 5, 29–33.CrossRefGoogle Scholar
Huang, Y. S., Schmitz, M., Le Belle, N., Chang, C. F., Querat, B. and Dufour, S. (1997). Androgens stimulate gonadotropin-II beta-subunit in eel pituitary cells in vitro. Molecular and Cellular Endocrinology 131, 157–166.CrossRefGoogle ScholarPubMed
Izyumova, N. A. (1987). Parasitic Fauna of Reservoir Fishes of the USSR and its Evolution. Amerind Publishing Co. Pvt. Ltd, New Dehli.Google Scholar
Joose, J. and Van Elk, R. (1986). Trichobilharzia ocellata: physiological characterisation of giant growth, glycogen depletion, and absence of reproductive activity in the intermediate snail host, Lymnaea stagnalis. Experimental Parasitology 62, 1–13.CrossRefGoogle Scholar
Juhasz, S. (1979). Studies on the nature of the protease inhibitor of Ligula intestinalis. Helminthologia 16, 293–298.Google Scholar
Kanamori, A., Kagawa, H. and Nagahama, Y. (1987). Gonadotropin receptors in the postovulatory ovary of amago salmon (Oncorhynchus rhodurus). General and Comparative Endocrinology 66, 210–217.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Burrough, R. J. (1981). The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilus rutilus (L.). Journal of Fish Biology 19, 105–126.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kerr, T. (1948). The pituitary in normal and parasitised roach (Leuciscus rutilus). Quarterly Journal of Microscopic Science 89, 129–137.Google Scholar
Khalil, M., Furness, D., Polwart, A. and Hoole, D. (2009). X-ray microanalysis (EDXMA) of cadmium-exposed eggs of Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) and the influence of this heavy metal on coracidial hatch and activity. International Journal for Parasitology 39, 1093–1098.CrossRefGoogle ScholarPubMed
Kir, I. and Tekin-Ozan, S. (2005). Occurrence of helminths in tench (Tinca tinca L., 1758) of Kovada (Isparta) Lake, Turkey. Bulletin of the European Association of Fish Pathologists 25, 75–81.Google Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today, 12, 111–115.CrossRefGoogle Scholar
Larralde, C., Morales, J., Terrazas, I., Govezensky, T. and Romano, M. C. (1995). Sex hormone changes induced by the parasite lead to feminization of the male host murine Taenia crassiceps cysticercosis. Journal of Steriod Biochemistry and Molecular Biology 52, 575–580.CrossRefGoogle ScholarPubMed
Li, J., Liao, X. and Yang, H. (2000). Molecular characterization of a parasitic tapeworm (Ligula) based on DNA sequences from formalin-fixed specimens. Biochemical Genetics 38, 309–322.CrossRefGoogle ScholarPubMed
Li, J. J. and Liao, X. H. (2003). The taxonomic status of Digramma (Pseudophyllidea: Ligulidae) inferred from DNA sequences. Journal of Parasitology 89, 792–799.CrossRefGoogle ScholarPubMed
Lin, Y. C., Rikihisa, Y., Kono, H. and Gu, Y. (1990). Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female rats. Experimental Parasitology 70, 344–352.CrossRefGoogle Scholar
Logan, F. J., Horák, A, Štefka, J., Aydogdu, A. and Scholz, T. (2004). The phylogeny of diphyllobothriid tapeworms (Cestoda: Pseudophyllidea) based on ITS-2 rDNA sequences. Parasitology Research 94, 10–15.CrossRefGoogle ScholarPubMed
Loot, G., Aulagnier, S., Lek, S., Thomas, F. and Guegan, J. F. (2002 a). Experimental demonstration of a behavioural modification in a cyprinid fish, Rutilus rutilus (L.) induced by a parasite, Ligula intestinalis. Canadian Journal of Zoology-Revue Canadienne de Zoologie 80, 738–744.CrossRefGoogle Scholar
Loot, G., Brosse, S., Lek, S. and Guegan, J. F. (2001 a). Behaviour of roach (Rutilus rutilus) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 1219–1227.CrossRefGoogle Scholar
Loot, G., Fancisco, P., Santoul, F., Lek, S. and Guegan, J. F. (2001 b). The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Archiv für Hydrobiologie 152, 511–525.CrossRefGoogle Scholar
Loot, G., Lek, S., Brown, S. P. and Guegan, J. F. (2001 c). Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea). Journal of Parasitology 87, 1002–1010.CrossRefGoogle ScholarPubMed
Loot, G., Lek, S., Dejean, D. and Guegan, J. F. (2001 d). Parasite-induced mortality in three host populations of the roach Rutilus rutilus (L.) by the tapeworm Ligula intestinalis (L.). Annales de Limnologie – International Journal of Limnology 37, 151–159.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.CrossRefGoogle Scholar
Loot, G., Poulin, R., Lek, S. and Guegan, J. F. (2002 b). 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, 168–177.CrossRefGoogle Scholar
Mahon, R. (1976). Effect of the cestode Ligula intestinalis on spottail shiners, Notropis hudsonius. Canadian Journal of Zoology 54, 2227–2229.CrossRefGoogle ScholarPubMed
Mataskasi, I. and Juhasz, S. (1977). Ligula intestinalis (L. 1758): Investigation on plerocercoids and adults for protease inhibitor activities. Parasitologia Hungarica 10, 51–60.Google Scholar
Matskasi, I. and Nemeth, I. (1979). Ligula intestinalis (Cestoda: Pseudophyllidea): Studies on the properties of proteolytic and protease inhibitor activities of the plerocercoid larvae. International Journal for Parasitology 9, 27–33.CrossRefGoogle Scholar
McMasters, M. E., Van der Kraak, G. J. and Munkittrick, K. R. J. (1996). An epidemiological evaluation of the biochemical basis for steroid hormonal depressions in fish exposed to industrial wastes. Great Lakes Research 22, 53–71.Google Scholar
Melamed, P., Rosenfeld, H., Elizur, A. and Yaron, Z. (1998). Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comparative Biochemistry and Physiology. C: Comparative Pharmacology and Toxicology 119, 325–338.Google Scholar
Montero, M., Le Belle, N., Vidal, B. and Dufour, S. (1996). Primary cultures of dispersed pituitary cells from estradiol-pretreated female silver eels (Anguilla anguilla L.): immunocytochemical characterization of gonadotropic cells and stimulation of gonadotropin release. General and Comparative Endocrinology 104, 103–115.CrossRefGoogle ScholarPubMed
Morgan, D. L. (2003). Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda). Environmental Biology of Fishes 66, 155–167.CrossRefGoogle Scholar
Morley, N. J., Crane, M. and Lewis, J. W. (2001 a). Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. International Journal for Parasitology 31, 1211–1217.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2001 b). Toxicity of cadmium and zinc to encystment and in vitro excystment of Parorchis acanthus (Digenea: Philophthalmidae). Parasitology 122, 75–79.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2001 c). Toxicity of cadmium and zinc to miracidia of Schistosoma mansoni. Parasitology 122, 81–85.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2002). Toxicity of cadmium and zinc mixtures to Diplostomum spathaceum (Trematode: Diplostomidae) cercarial survival. Archives of Environmental Contamination and Toxicology 43, 28–33.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2003). Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematode: Diplostomidae). Folia Parasitologica 122, 81–85.Google Scholar
Morley, N. J., Lewis, J. W. and Hoole, D. (2006). Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission. Journal of Helminthology 80, 137–149.CrossRefGoogle ScholarPubMed
Morrison, B. R. S. (1977). Observations on the tapeworm (Ligula intestinalis) a parasite of roach (Rutilus rutilus) in the lake of Menteith, Perthshire. Proceedings of the 8th British Coarse Fish Conference, 101–107.Google 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.CrossRefGoogle Scholar
Nagahama, Y. (1999). Gonadal steroid hormones: major regulators of gonadal sex differentiation and gametogenesis in fish. Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish, Bergen, July 1999, 211–221.Google Scholar
Nocillado, J. N. and Elizur, A. (2008). Neuroendocrine regulation of puberty in fish: insights from the grey mullet (Mugil cephalus) model. Molecular Reproduction and Development 75, 355–361.CrossRefGoogle ScholarPubMed
Okubu, K. and Aida, K. (2001). Gonadotrophin-releasing hormones (GnRHs) in a primitive teleost, the arowana: phylogenetic evidence that three paralogous lineages of GnRH occurred prior to the emergence of teleosts. General and Comparative Endocrinology 124, 125–133.CrossRefGoogle Scholar
Olson, P. D., Littlewood, D. T. L., Griffiths, D., Kennedy, C. R. and Arme, C. (2002). Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. Journal of Helminthology 76, 171–174.CrossRefGoogle ScholarPubMed
O'Neill, D. F., Powell, J. F., Standen, E. M., Youson, J. H., Warby, C. M. and Sherwood, N. M. (1998). Gonadotropin-releasing hormone (GnRH) in ancient teleosts, the bonytongue fishes: putative origin of salmon GnRH. General and Comparative Endocrinology 112, 415–425.CrossRefGoogle ScholarPubMed
Orr, T. S. C. (1968). Distribution and specificity of the plerocercoid of Ligula intestinalis (L) in the Northamptonshire area. Journal of Helminthology XLII, 117–124.CrossRefGoogle Scholar
Penlington, M. C., Williams, M. A., Sumpter, J. P., Rand-Weaver, M., Hoole, D. and Arme, C. (1997). Isolation and characterisation of mRNA encoding the salmon- and chicken-II type gonadotrophin-releasing hormones in the teleost fish Rutilus rutilus (Cyprinidae). Journal of Molecular Endocrinology 19, 337–346.CrossRefGoogle ScholarPubMed
Peter, R. E., Chang, J. P., Nahorniak, C. S., Omeljaniuk, R. J., Sokolowska, M., Shih, S. H. and Billard, R. (1986). Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Progress in Hormone Research 42, 513–548.Google ScholarPubMed
Pietrock, M., Marcoliese, D. J. and McLaughlin, J. D. (2002). Effects of cadmium upon longevity of Diplostomum sp. (Trematoda: Diplostomidae) cercariae. Chemosphere 47, 29–33.CrossRefGoogle ScholarPubMed
Pollard, D. A. (1974). The biology of a landlocked form of the normally catadromous Salmoniform fish Galaxius maculates (Jenyns). VI. Effects of cestode and nematode parasites. Australian Journal of Marine and Freshwater Research 25, 105–120.CrossRefGoogle Scholar
Richards, K. S. and Arme, C. (1981). The effects of the plerocercoid larva of the pseudophyllidean cestode Ligula intestinalis on the musculature of bream (Abramis brama). Zeitschrift für Parasitenkunde 65, 207–215.CrossRefGoogle Scholar
Sasi, H. (2005). Incidence of Ligula intestinalis from Transcaucasian barb. Indian Veterinary Journal 82, 790–791.Google Scholar
Shargh, S., Shamsaii, M. and Karimi, S. (2008). Distribution of parasitic cestode Ligula intestinalis in Mazandaran region. Iranian Journal of Parasitology 3, 26–33.Google Scholar
Shields, B. A., Groves, K. L., Rombaugh, C. and Bellmore, R. (2002). Ligulosis associated with mortality in largescale suckers. Journal of Fish Biology 61, 448–455.CrossRefGoogle Scholar
Smyth, J. D. (1947). Studies on tapeworm physiology II Cultivation and development of Ligula intestinalis in vitro. Parasitology 48, 173–181.CrossRefGoogle Scholar
Stefka, J., Gilleard, J. S., Grillo, V. and Hypsa, V. (2007). Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea). Molecular Ecology Notes 7, 794–796.CrossRefGoogle Scholar
Stefka, J., Hypsa, V. and Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 1187–1206.CrossRefGoogle ScholarPubMed
Sures, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126 (Suppl.), S53–S60.CrossRefGoogle Scholar
Sures, B. (2008 a). Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 80, 434–438.CrossRefGoogle Scholar
Sures, B. (2008 b). Host-parasite interactions in polluted environments. Journal of Fish Biology 73, 1–10.CrossRefGoogle Scholar
Sures, B. and Siddall, R. (1999). Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 66–72.CrossRefGoogle ScholarPubMed
Sures, B., Taraschewski, H. and Siddall, R. (1997). Heavy metal concentrations in adult acanthocephalans and cestodes compared to their fish hosts and to establish free-living bioindicators. Parassitologia 39, 213–218.Google ScholarPubMed
Sweeting, R. A. (1976). Studies on Ligula intestinalis (L.) effects in a roach population in a gravel pit. Journal of Fish Biology 9, 515–522.CrossRefGoogle Scholar
Sweeting, R. A. (1977). Studies on Ligula intestinalis, some aspects of the pathology in the second intermediate host. Journal of Fish Biology 10, 43–50.CrossRefGoogle Scholar
Szalai, A. J., Yang, X. and Dick, T. A. (1989). Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in transmission. Journal of Parasitology 75, 571–576.CrossRefGoogle ScholarPubMed
Taylor, M. J. and Hoole, D. (1989 a). Ligula intestinalis (L.) (Cestoda: Pseudophyllidea): plerocercoid-induced changes in the spleen and pronephros of roach, Rutilus rutilus (L.) and gudgeon, Gobio gobio. Journal of Fish Biology 34, 583–528.CrossRefGoogle Scholar
Taylor, M. J. and Hoole, D. (1989 b). Ligula intestinalis (Cestoda: Pseudophyllidea): an ultrastructural study of the cellular response of roach fry, Rutilus rutilus, to an unusual intramuscular infection. Journal of Fish Diseases 12, 523–528.CrossRefGoogle Scholar
Taylor, M. J. and Hoole, D. (1993). Ligula intestinalis (L.) (Cestoda: Pseudophyllidea): polarization of cyprinid leucocytes as an indicator of host- and parasite-derived chemoattractants. Parasitology 107, 433–440.CrossRefGoogle ScholarPubMed
Taylor, M. J. and Hoole, D. (1994). Modulation of fish lymphocyte proliferation by extracts and isolated proteinase inhibitors of Ligula intestinalis (Cestoda). Fish and Shellfish Immunology 4, 221–230.CrossRefGoogle Scholar
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, 191–198.CrossRefGoogle Scholar
Tekin-Ozan, S. and Barlas, M. (2008). Concentrations of selected heavy metals in Ligula intestinalis L. 1758 plerocercoids (Cestoda) compared to it host's (Tinca tinca L. 1758) organs from Beysehir Lake (Turkey). Helminthologia 45, 76–80.CrossRefGoogle Scholar
Tekin-Ozan, S. and Kir, I. (2005). Comparative study on the accumulation of heavy metals in different organs of tench (Tinca tinca L. 1758) and plerocercoids of its endoparasite Ligula intestinalis. Parasitology Research 97, 156–159.CrossRefGoogle ScholarPubMed
Tekin-Ozan, S. and Kir, I. (2008). Concentrations of some heavy metals in tench (Tinca tinca l., 1758), its endoparasite (Ligula intestinalis L., 1758), sediment and water in Beysehir Lake, Turkey. Polish Journal of Environmental Studies 17, 597–603.Google Scholar
Tenora, F., Barus, V., Kracmer, S. and Dvoracek, J. (2000). Concentrations of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometra ovata (Nematoda) compared to some their hosts (Osteichthyes). Helminthologia 37, 15–18.Google Scholar
Tenora, F., Barus, V. and Prokes, M. (2002). Next remarks to the knowledge of heavy metal concentrations in gravid tapeworm species parasitizing aquatic birds. Helminthologia 39, 143–148.Google Scholar
Tobin, C. (1986). A record of Ligula intestinalis (L.) (Cestoda) from roach (Rutilus rutilus (L.)) in Lough Neagh. Irish Naturalists' Journal 22, 78.Google Scholar
Trubiroha, A., Wuertz, S., Frank, S. N., Sures, B. and Kloas, W. (2009). Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). International Journal for Parasitology 39, 1465–1473.CrossRefGoogle ScholarPubMed
Trudeau, V. L. (1997). Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Reviews of Reproduction 2, 55–68.CrossRefGoogle ScholarPubMed
Tyler, C. R., Santos, E. M. and Prat, F. (1999). Unscrambling the egg-cellular biochemical molecular and endocrine advances in oogenesis. Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish, Bergen, July 1999, 273–279.Google Scholar
Van Dobben, V. H. (1952). The food of the cormorant in the Netherlands. Adrea 40, 1–63.Google Scholar
Vidal, B., Pasqualini, C., Le Belle, N., Holland, M. C. H., Sbaihi, M., Vernier, P., Zohar, Y. and Dufour, S. (2004). Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: a neuroendocrine lock for the onset of puberty. Biology of Reproduction, 71, 1491–1500.CrossRefGoogle ScholarPubMed
Weekes, P. J. and Penlington, B. (1986). First records of Ligula intestinalis (Cestoda) in rainbow trout, Salmo gairdneri, and common bully, Gobiomorphus cotidianus, in New Zealand. Journal of Fish Biology 28, 183–190.CrossRefGoogle Scholar
Williams, M. A. and Hoole, D. (1992). Antibody response of the fish Rutilus rutilus to the metacestode of Ligula intesinalis. Diseases of Aquatic Organisms 12, 83–89.CrossRefGoogle Scholar
Williams, M. A. and Hoole, D. (1995). Immunolabelling of fish host molecules on the tegumental surface of Ligula intestinalis (Cestoda: Pseudophyllidea). International Journal for Parasitology 25, 249–256.CrossRefGoogle ScholarPubMed
Williams, M. A., Penlington, M. C., King, J. A., Hoole, D. and Arme, C. (1998). Ligula intestinalis (Cestoda) infections of roach (Rutilus rutilus) (Cyprinidae): immunocytochemical investigations into the salmon- and chicken-II type gonadotrophin-releasing hormone (GnRH) systems in host brains. Acta Parasitologica 43, 232–235.Google Scholar
Wilson, R. S. (1971). The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129–137.CrossRefGoogle Scholar
Wyatt, R. J. and Kennedy, C. R. (1988). The effects of a change in the growth rate of roach, Rutilus rutilus (L.) on the population biology of the fish tapeworm Ligula intestinalis (L.). Journal of Fish Biology 33, 45–57.CrossRefGoogle Scholar
Wyatt, R. J. and Kennedy, C. R. (1989). Host-constrained epidemiology of the fish tapeworm Ligula intestinalis (L.). Journal of Fish Biology 35, 215–227.CrossRefGoogle Scholar
Xianghua, L. and Zhixin, L. (1987). Distribution of ligulid tapeworms in China. Journal of Parasitology 73, 36–48.CrossRefGoogle Scholar
Yan, L., Swanson, P. and Dickhoff, W. W. (1992). A two-receptor model for salmon gonadotropins (GTH I and GTH II). Biology of Reproduction 47, 418–427.CrossRefGoogle ScholarPubMed
Yu, K. L., He, M. L., Chik, C. C., Lin, X. W., Chang, J. P. and Peter, R. E. (1998). mRNA expression of gonadotropin-releasing hormones (GnRHs) and GnRH receptor in goldfish. General and Comparative Endocrinology 112, 303–311.CrossRefGoogle ScholarPubMed