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An ultrastructural study of the early cercarial development in Prosorhynchoides borealis (Digenea: Bucephalidae) with special reference to formation of the primitive epithelium

Published online by Cambridge University Press:  01 June 2008

I.M. Podvyaznaya  and
K.V. Galaktionov
I.M. Podvyaznaya*
Affiliation:
The Laboratory of Parasitic WormsZoological Institute, Russian Academy of Sciences, St. Petersburg199034, Russia
K.V. Galaktionov
Affiliation:
The White Sea Biological Station, Zoological Institute, Russian Academy of Sciences, St. Petersburg199034, Russia
*
*Fax: +7 (812) 328 2941podvyaznaya_vermes@zin.ru
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Abstract

Primitive epithelium and outer tegumental layer formation during early cercarial development was studied in Prosorhynchoides borealis using electron microscopy. It demonstrated that germinal cells freely floating in the sporocyst body cavity divide to give rise to naked cell aggregates. These early embryos are highly irregular in outline and are composed of blastomeres differing in size and structure. In embryos consisting of about 12–14 cells a few (possibly only two) superficial macromeres become concave and produce thin extensions which envelop the embryonic mass before fusing to form a syncytial primitive epithelium. This primitive epithelium forms syncytial connections with underlying embryonic cells. Primordial tegumental cells become apparent in late germinal balls below the primitive epithelium. These cells expand and fuse to give rise to an embryonic nucleated tegument. The embryonic tegument is connected to peripheral embryonic cells by thin cytoplasmic bridges until the basement lamina is formed. Subsequently, the primitive epithelium is shed by the embryos and the nuclei in the embryonic tegument undergo pyknotic degeneration. These results are analysed and compared with data from studies on other trematode species and it is concluded that the primitive epithelium is derived from the embryo in at least the majority of digeneans.

Type
Research Papers
Information
Journal of Helminthology , Volume 82 , Issue 2 , June 2008 , pp. 101 - 108
Copyright
Copyright © Cambridge University Press 2008

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References

Al-Salman, H.A. & James, B.L. (1988) Ultrastructure of the tegument in daughter sporocyst and cercarial embryos of Meiogymnophallus minutus (Digenea: Gymnophallidae). International Journal for Parasitology 18, 231–242.Google Scholar
Bartoli, P., Gibson, D.I. & Bray, R.A. (2006) Prosorhynchoides gracilescens (Rudolphi 1819) (Digenea: Bucephalidae) from Lophius piscatorius L. is a species complex: a redescription of this species (sensu stricto) from the western Mediterranean and the description of P. borealis n. sp. from the northern North-East Atlantic. Systematic Parasitology 63, 203–221.Google Scholar
Bednarz, S. (1973) The development cycle of the germ-cells in several representatives of Trematoda (Digenea). Zoologica Poloniae 23, 279–326.Google Scholar
Bils, F. & Martin, W.E. (1966) Fine structure and development of the trematode integument. Transactions of the American Microscopical Society 85, 78–88.CrossRefGoogle ScholarPubMed
Chen, P.D. (1937) The germ cell cycle in the trematode Paragonimus kellicotti Ward. Transactions of the American Microscopical Society 56, 208–236.Google Scholar
Cheng, T.C. (1961) Studies on the morphogenesis, development and germ cell cycle in the sporocysts and cercariae of Glypthelmins pennsylvaniensis Cheng, 1961 (Trematoda: Brachycoeliidae). Proceedings of the Pennsylvania Academy of Science 35, 10–22.Google Scholar
Cheng, T.C. & Bier, J.W. (1972) Studies on molluscan schistosomiasis: an analysis of the development of the cercaria of Schistosoma mansoni. Parasitology 64, 129–142.Google Scholar
Cheng, T.C. & James, H.A. (1960) Studies on the germ cell cycle, morphogenesis and development of the cercarial stage of Crepidostomum cornutum (Osborn,1903) (Trematoda: Allocreadiidae). Transactions of the American Microscopical Society 79, 75–85.CrossRefGoogle Scholar
Dobrovolskij, A.A. (1965) Some new data on life-history of the fluke Opisthioglyphe ranae Fröhlich, 1791 (Plagiorchiidae). Helminthologia 6, 205–221(in Russian).Google Scholar
Dobrovolskij, A.A. (1971) The life-history of Macrodera longicollis (Abildgaard, 1788) Lühe, 1909 (Trematoda, Ochetosomatidae). Vestnik Leningradskogo Universiteta (Biol.) 15, 9–20(in Russian).Google Scholar
Dunn, M.C. (1959) Studies on the germ cell cycle of Neorenifer wardi. Transactions of the American Microscopical Society 78, 385–408.CrossRefGoogle Scholar
Dunn, T.S., Dang, P.H., Hanna, R.E.B. & Nisami, W.A. (1992) Embryological development of the cercarial tegument of Paramphistomum epiclitum in the planorbid snail, Indoplanorbis exustus. Journal of Helminthology 66, 243–254.CrossRefGoogle Scholar
Galaktionov, K.V. & Dobrovolskij, A.A. (2003) The biology and evolution of trematodes. 592 pp. Dordrecht, Kluwer.Google Scholar
Gerasyov, P.I. & Dobrovolskij, A.A. (1977) Development of hermaphroditic generation of Astiotrema trituri (Trematoda: Plagiorchiidae). Parazitologicheskii Sbornik 27, 89–111(in Russian).Google Scholar
Göbel, E.P. & Pan, J.P. (1985) Ultrastructure of the daughter sporocyst and developing cercaria of Schistosoma japonicum in experimentally infected snails, Oncomelania hupensis hupensis. Zeitschrift für Parasitenkunde 71, 227–240.Google Scholar
Halton, D.W. & McCrae, J.M. (1985) Development of the tegument and alimentary tract in a digenetic trematode, Fellodistomum fellis. Parasitology 90, 193–204.CrossRefGoogle Scholar
Hockley, D.J. (1972) Schistosoma mansoni: the development of the cercarial tegument. Parasitology 64, 245–252.CrossRefGoogle ScholarPubMed
Irwin, S.W.B., Galaktionov, K.V., Malkova, I.I., Saville, D.H. & Fitzpatrick, S.M. (2003) An ultrastructural study of reproduction in the parthenogenetic metacercariae of Cercaria margaritensis Ching, 1982 (Digenea: Gymnophallidae). Parasitology 126, 261–271.CrossRefGoogle ScholarPubMed
Ishii, T. (1934) Studies on the development of Fasciolopsis buski. I. Development of the eggs outside the host. Journal of the Medical Association of Formosa 33, 349–378.Google Scholar
James, B.L. & 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, 607–625.Google Scholar
James, B.L., Bowers, E.A. & Richards, J.G. (1966) The ultrastructure of the daughter sporocyst of Cercaria bucephalopsis haimeana Lacaze-Duthiers, 1854 from the edible cockle, Cardium edule L. Parasitology 56, 753–762.CrossRefGoogle ScholarPubMed
Maldonado, J.F. (1967) Schistosomiasis in America. 120 pp. Barcelona, Editorial Cientifico-Medica.Google Scholar
Matricon-Gondran, M. (1971) Origine et différenciation du tégument d'un trématode digénétique: étude ultrastructurale chez Cercaria pectinata (larve de Bacciger bacciger, Fellodistomatidés). Zeitschrift für Zellforschung 120, 488–524.Google Scholar
Meuleman, E.A. & Holzmann, P.J. (1975) The development of the primitive epithelium and true tegument in the cercaria of Schistosoma mansoni. Zeitschrift für Parasitenkunde 45, 307–318.Google Scholar
Meuleman, E.A., Holzmann, P.J. & Peet, R.C. (1980) The development of daughter sporocysts inside the mother sporocyst of Schistosoma mansoni with special reference to the ultrastructure of the body wall. Zeitschrift für Parasitenkunde 61, 201–212.Google Scholar
Podvyaznaya, I. (2007) An ultrastructural study of reproduction in the sporocysts of Prosorhynchoides gracilescens (Digenea: Bucephalidae). Parasitology Research 101, 35–42.CrossRefGoogle ScholarPubMed
Rees, G. (1940) Studies on the germ cell cycle of the digenetic trematode Parorchis acanthus Nicoll. Part II. Structure of the miracidium and germinal development in the larval stages. Parasitology 32, 372–391.CrossRefGoogle Scholar
Rees, G. & Day, M.F. (1976) The origin and development of the epidermis and associated structures in the cercaria of Cryptocotyle lingua (Creplin) (Digenea: Heterophyidae) from Littorina littorea (L.). Proceedings of the Royal Society of London B 192, 299–321.Google Scholar
Rifkin, E. (1970) An ultrastructural study of the interaction between the sporocysts and the developing cercariae of Schistosoma mansoni. Journal of Parasitology 56, 284.Google Scholar
Tihomirov, I.A. (1980) Life cycle of Philophthalmus rhionica sp. nov. (Trematoda: Philophthalmidae). PhD Thesis, Leningrad State University, Leningrad, USSR (in Russian).Google Scholar
Tyler, S. & Hooge, M. (2004) Comparative morphology of the body wall in flatworms (Platyhelminthes). Canadian Journal of Zoology 82, 194–210.Google Scholar
Tyler, S. & Tyler, M.S. (1997) Origin of the epidermis in parasitic platyhelminths. International Journal for Parasitology 27, 715–738.Google Scholar
Žd'árská, Z. (1995) Ultrastructure of the primitive epithelium of Echinostoma revolutum (Digenea: Echinostomatidae) cercaria. Folia Parasitologica 42, 266–268.Google Scholar
Žd'árská, Z. & Soboleva, T.N. (1985) Electron microscope observations of the sporocyst of Postharmostomum gallinum Witenberg, 1923 (Brachylaimidae). Folia Parasitologica 32, 227–230.Google Scholar