Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T06:33:50.206Z Has data issue: false hasContentIssue false

One of the most complex life-cycles among trematodes: a description of Parvatrema margaritense (Ching, 1982) n. comb. (Gymnophallidae) possessing parthenogenetic metacercariae

Published online by Cambridge University Press:  23 January 2006

K. V. GALAKTIONOV
Affiliation:
White Sea Biological Station, Zoological Institute of the Russian Academy of Sciences, Universitetskaja naberezhnaja 1, 199034 Saint Petersburg, Russia
S. W. B. IRWIN
Affiliation:
School of Environmental Sciences, University of Ulster, Shore Road, Newtownabbey, Co. Antrim, N. Ireland BT37 0QB, UK
D. H. SAVILLE
Affiliation:
School of Environmental Sciences, University of Ulster, Shore Road, Newtownabbey, Co. Antrim, N. Ireland BT37 0QB, UK

Abstract

This study used light and electron microscopy to provide observations and morphometric details of the life-cycle of the gymnophallids (Trematoda, Digenea), Parvatrema margaritense (Ching, 1982) n. comb., the parthenogenetic metacercariae (‘germinal sacs’) of which were previously described by Ching (1982) as Cercaria margaritensis. The research was instigated by the discovery, on the Barents Sea coast, of a high prevalence of gymnophallid sporocysts and cercariae in the bivalve Turtonia minuta and an equivalent presence of distinctive gymnophallid metacercariae in the gastropod Margarites helicinus. Experiments and data obtained from naturally infected M. helicinus demonstrated that cercariae released from the bivalves invaded the gastropods to give rise to the metacercariae. Two generations (M1 and M2) of these parthenogenetic metacercariae were formed in the extrapallial cavities of their bivalve hosts and they, in turn, gave rise to a third generation (M3) which was shown to infect marine ducks such as the eider (Somateria mollissima). As only small numbers of cercariae are released from T. minuta, it was concluded that the inclusion of parthenogenetic metacercariae in the life-cycle is particularly significant. It allows each cercaria that infects M. helicinus to give rise to over 2000 invasive metacercariae. Evidence suggests that the parthenogenetic metacercariae are commensal rather that parasitic in the pallial cavities of their hosts. Implications of this for theories of early digenean evolution are discussed.

Type
Research Article
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Cable, R. M. ( 1965). ‘Thereby hangs a tail’. Journal of Parasitology 51, 212.CrossRefGoogle Scholar
Cable, R. M. ( 1974). Phylogeny and taxonomy of trematodes with reference to marine species. In Symbiosis in the Sea ( ed. Vernberg, W. E.), pp. 173193. University of South Carolina Press Columbia, South Carolina.
Ching, H. L. ( 1982). Description of germinal sacs of a gymnophallid trematode, Cercaria margaritensis sp. n., in the extrapallial fluid of subtidal snails (Margarites spp.) in British Columbia. Canadian Journal of Zoology, 60, 516520.Google Scholar
Ching, H. L. ( 1995). Evaluation of characters of the digenean family Gymnophallidae Morozov, 1955. Canadian Journal of Fish and Aquaculture Science 52, 7883.CrossRefGoogle Scholar
Chubrik, G. K. ( 1966). Fauna and ecology of trematode larvae from molluscs of the Barents and White Seas. In Life Cycles of Parasitic Worms from Northern Seas ( ed. Poljansky, Yu. I.), pp. 78159. Nauka, Leningrad (in Russian).
Galaktionov, K. V. ( 1996). An experimental study of the unusual life cycle of Parvatrema sp. (Trematoda: Gymnophallidae). Parazitologiya 30, 487494 (in Russian).Google Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. ( 2003). Biology and Evolution of Trematodes. An Essay on the Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Kluwer Academic Publishers, Dordrecht, Boston, London.CrossRef
Galaktionov, K. V., Irwin, S. W. B. and Saville, D. H. ( 2004). Parthenogenetic metacercariae of gymnophallids (Digenea: Gymnophallidae) illustrate early stages of digenetic trematode evolution. In Proceedings of the IX European Multicolloquium of Parasitology (EMOP IX), Valencia, Spain, 18–23 July 2004 ( ed. Mas-Coma, S., Bargies, M. D., Esteban, J. G. and Valero, M. A.), pp. 609610. Artest Gráficas J. Aguilar, S.L., Valencia.
Gibson, D. I. ( 1987). Questions in digenean systematics and evolution. Parasitology 95, 429460.CrossRefGoogle Scholar
Gibson, D. I. and Bray, R. A. ( 1994). The evolutionary expansion and host-parasite relationships of the Digenea. International Journal for Parasitology 24, 12131226.CrossRefGoogle Scholar
Ginetsinskaya, T. A. ( 1968). Trematodes, their Life Cycles, Biology and Evolution. Nauka Publishers, Leningrad (in Russian); English translation: 1988. Translated by Amerind Publishing Co. Pvt. Ltd, New Delhi.
Heyneman, D. ( 1960). On the origin of complex life cycles in digenetic flukes. In Libro Hamenaje al dr. E. Caballero Jubileo 1930–1960. pp. 133152. Mexico.
Irwin, S. W. B., Galaktionov, K. V., Malkova, I. I., Saville, D. H. and Fitzpatrick, S. M. ( 2003). An ultrastructural study of reproduction in the parthenogenetic metacercariae of Cercaria margaritensis Ching, 1982 (Digenea: Gymnophallidae). Parasitology 126, 261271.CrossRefGoogle Scholar
James, B. L. ( 1964). The life cycle of Parvatrema homoeotecnum sp. nov. (Trematoda: Digenea) and review of the family Gymnophallidae Morozov, 1955. Parasitology 54, 141.Google Scholar
James, B. L. ( 1965). The effect of parasitism by larval Digenea on the digestive gland of the intertidal prosobranch, Littorina saxatilis (Olivi) subsp. tenebrosa (Montagu). Parasitology 55, 93115.CrossRefGoogle Scholar
James, B. L. and Bowers, E. A. ( 1967). Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae). Parasitology 57, 607625.CrossRefGoogle Scholar
Jameson, M. A. and Nicoll, M. A. ( 1913). On some parasites of the scoter duck (Oedemia nigra), and their relation to the pearl-inducing trematode in the edible mussel (Mytilus edulis). Proceedings of the Zoological Society of London 1, 5363.Google Scholar
Loos-Frank, B. ( 1969) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativ-Zyklen von Gymnophallus choledochus. Zeitschrift für Parasitenkunde 32, 135156.CrossRefGoogle Scholar
Pearson, J. C. ( 1972). A phylogeny of life-cycle patterns of the Digenea. Advances in Parasitology 10, 153189.CrossRefGoogle Scholar
Pearson, J. C. ( 1992). On the position of the digenean family Heronimidae: an inquiry into a cladistic classification of the Digenea. Systematic Parasitology 21, 81166.CrossRefGoogle Scholar
Podlipaev, S. A. ( 1979). Trematode parthenitae and larvae in the intertidal molluscs of the Eastern Murman. In Ecological and Experimental Parasitology ( ed. Poljansky, Yu. I.), vol. 2, pp. 47101. Izdatel'stvo Leningradskogo Universiteta, Leningrad (In Russian).
Prokofiev, V. V. ( 1994). ‘Ambuscade’ type of cercarial behaviour in marine trematodes. Zoologichesky Zhurnal (Zoological Journal) 73, 1320(in Russian).Google Scholar
Rohde, K. ( 1971). Phylogenetic origin of trematodes. Parasitologische Schriftenreihe 21, 1727.Google Scholar
Rohde, K. ( 1994). The origin of parasitism in the Platyhelminthes. International Journal for Parasitology 24, 10991115.CrossRefGoogle Scholar
Scholz, T. ( 2002). Family Gymnophallidae Odhner, 1905. In Keys to the Trematoda ( ed. Gibson, D. I., Jones, A. and Bray, R. A.), vol. 1, pp. 245251. CABI Publishing and The Natural History Museum, London.CrossRef
Szidat, L. ( 1962). Über eine ungewöhnliche Form parthenogenetischer Vermehrung bei Metacercarien einer Gymnophallus-Art aus Mytilus platensis, Gymnophallus australis n. sp. Des Südatlantik. Zeitschrift für Parasitenkunde 22, 196213.Google Scholar
Tsimbaljuk, A. K., Kulikov, V. V. and Baranova, T. I. ( 1978). Helminths of invertebrates from the intertidal zone of the Iturup island. In Fauna and Vegetation of the Shelf of the Kurile Islands ( ed. Kusakin, O. G.), pp. 69126. Nauka, Moscow (in Russian).