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Developmental changes in the tegument of four microphallid metacercariae in their second (crustacean) intermediate hosts

Published online by Cambridge University Press:  05 June 2009

K.V. Galaktionov
Affiliation:
Murmansk Marine Biological Institute, Russian Academy of Sciences Kola Scientific Centre, 17 Vladimirskaya Street, 183101, Murmansk, Russia
I.I. Malkova
Affiliation:
Murmansk Marine Biological Institute, Russian Academy of Sciences Kola Scientific Centre, 17 Vladimirskaya Street, 183101, Murmansk, Russia
S.W.B. Irwin*
Affiliation:
School of Applied Biological and Chemical Sciences, University of Ulster at Jordanstown, Shore Road, Newtownabbey, Co. Antrim, Northern Ireland, BT37 0QB
D.H. Saville
Affiliation:
School of Applied Biological and Chemical Sciences, University of Ulster at Jordanstown, Shore Road, Newtownabbey, Co. Antrim, Northern Ireland, BT37 0QB
J.G. Maguire
Affiliation:
School of Applied Biological and Chemical Sciences, University of Ulster at Jordanstown, Shore Road, Newtownabbey, Co. Antrim, Northern Ireland, BT37 0QB
*
* Author for correspondence.

Abstract

The morphology of the tegument of four microphallid metacercariae from the stage of invasive cercariae to their maturation as encysted metacercariae inside their crustacean second intermediate hosts is described. The tegument of the metacercariae developed surface lamellae and projections which, along with coated vesicles in the surface syncytium, indicated that the tegument had an absorptive function. The disappearance of secretory granules from the tegument at the same time as the appearance of the first cyst wall suggested that the tegument had a role in primary cyst production. Following this, the metacercariae continued to grow and seemingly retained their absorptive ability. The tegument was also involved in the transport of material into the perimetacercarial lumen prior to its eventual inclusion in the developing inner cyst layers. It appeared that this material originated in tegumental cells located amongst the parenchymal cells beneath the tegumental syncytial layer. On completion of the secondary cyst layers there was a gradual degeneration of structures associated with absorption and a progressive accumulation of dense discoid granules traceable to underlying tegumental cells. All four microphallid species (Maritrema arenaria, M. subdolum, Levinseniella brachysoma and Microphallus claviformis) demonstrated the same developmental pattern but the period spent in each stage differed depending on the time spent migrating to encystment sites. The pattern of tegumental development described is thought to be applicable to all microphallid metacercariae and possibly to other metacercariae which undergo growth and development in their second intermediate hosts.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 1996

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References

Alderson, G.D. (1975) Ultrastructure and histochemistry of the metacercarial cyst of Spelotrema nicolli (Microphallidae: Trematoda). International Journal for Parasitology 5, 659665.CrossRefGoogle Scholar
Bakke, T.A. (1982) Histology and biology of the larval stages of Leucochloridium Carus, 1835 (Trematoda, Digenea) as revealed by light and electron microscopy. Fauna Norvegica., Ser.A 3, 4156.Google Scholar
Belopolskaya, M.M. (1963) [Family Microphallidae Travassos, 1920. pp. 259502in Skrjabin, K.I. (Ed.) Trematodes of man and animals] Vol. 21 Moscow, Nauka Press, (in Russian).Google Scholar
Benjamin, L.R. & James, B.L. (1987) The development of the metacercariae of Maritrema linguilla Jag. 1908 (Digenea; Microphallidae) in the intermediate host Ligia oceanica (L). Parasitology 94, 221231.CrossRefGoogle Scholar
Bibby, M.C. & Rees, G. (1971a) The ultrastructure of the epidermis and associated structures in the metacercaria, cercaria and sporocyst of Diplostomum phoxini (Faust, 1918). Zeitschrift für Parasitenkunde 37, 169186.CrossRefGoogle ScholarPubMed
Bibby, M.C. & Rees, G. (1971b) The uptake of radioactive glucose in vivo and in vitro by the metacercaria Diplostomum phoxini (Faust) and its conversion to glycogen. Zeitschrift für Parasitenkunde, 37, 187197.CrossRefGoogle ScholarPubMed
Caulfield, J.P., Yuan, H.-C., Cianci, C.M.L. & Hein, A. (1988) Schistosoma mansoni: development of the cercarial glycocalyx. Experimental Parasitology 65, 1019.CrossRefGoogle ScholarPubMed
Chappell, L.H. (1980) The biology of the external surfaces of helminth parasites. Proceedings of the Royal Society of Edinburgh B79, 145171.Google Scholar
Davies, C. (1979) The forebody glands and surface features of the metacercariae and adults of Microphallus similis. International Journal for Parasitology 9, 553564.CrossRefGoogle Scholar
Davies, C. (1980) A comparative ultrastructural study of in vivo and in vitro derived adults of Microphallus similis. International Journal for Parasitology 10, 217226.CrossRefGoogle Scholar
Erasmus, D.A. (1977) The host–parasite interface of trematodes. Advances in Parasitology 15, 201242.CrossRefGoogle ScholarPubMed
Galaktionov, K.V. (1988) Cercaria and metacercaria of Levinseniella brachysoma (Trematoda, Microphallidae) from the White Sea invertebrates. Parazitologiya 22, 305311 (in Russian).Google Scholar
Galaktionov, K.V. (1993) Trematode life cycles as components of ecosystems. Apatity, Kola Scientific Centre Press (in Russian).Google Scholar
Galaktionov, K.V. & Dobrovolskii, A.A. (1987) Hermaphroditic generation of Trematodes. Leningrad: Nauka Press (in Russian).Google Scholar
Galaktionov, K.V. & Malkova, I.I. (1990) Tegument structure of cercariae of microphallid trematodes. Parazitologiya 24, 301308 (in Russian).Google ScholarPubMed
Galaktionov, K.V. & Malkova, I.I. (1994) The glands of trematode cercariae of the family Microphallidae Travassos, 1920. International Journal for Parasitology 24, 595604.CrossRefGoogle ScholarPubMed
Halton, D.W. & Johnston, B.R. (1982) Functional morphology of the metacercarial cyst of Bucephaloides gracilescens (Trematoda: Bucephalidae). Parasitology 85, 4552.CrossRefGoogle Scholar
Hanna, R.E.B., (1980) Fasciola hepatica: glycocalyx replacement in the juvenile as a possible mechanism for protection against host immunity. Experimental Parasitology 50, 103114.CrossRefGoogle ScholarPubMed
Harris, K.R., Cheng, T.C. & Cali, A. (1974) An electron microscope study of the tegument of the metacercaria and adult of Leucochloridiomorpha constantiae (Trematoda: Brachylaemidae). Parasitology 68, 5767.CrossRefGoogle ScholarPubMed
Higgins, J.C. (1979) The role of the tegument of the metacercariae stage of Bucephalus haimeanus (Lacaze-Duthiers, 1854) in the absorption of particulate material and small molecules in solution. Parasitology 78, 99106.CrossRefGoogle Scholar
Irwin, S.W.B., Maguire, J.G. & Saville, D.H. (1990) Identification of the cercarial stage of Maritrema arenaria (syn. M. gratiosum) (Trematoda: Microphallidae). Journal of Natural History 24, 949954.CrossRefGoogle Scholar
Larson, O.R., Uglem, G.L. & Lee, K.J. (1988) Fine structure and permeability of the metacercarial cyst wall of Clinostomum marginatum (Digenea). Parasitology Research 74, 352355.CrossRefGoogle ScholarPubMed
Lo, S.-L., Hall, J.E., Allender, P.A. & Kleiner, A.S. (1975) Scanning electron microscopy of an opecoelid cercaria and its encystment and encapsulation in an insect host. Journal of Parasitology 61, 413417.CrossRefGoogle Scholar
Lumsden, R.D. (1975) Surface ultrastructure and cytochemistry of parasitic helminths. Experimental Parasitology 37, 267339.CrossRefGoogle ScholarPubMed
Panin, V., Zdarska, A. & Nesterenko, L. (1986) Ultrastructure of parthenites and larvae of dicrocoeliid trematodes. pp. 2548in Gvozdev, E.Y. & Zdarska, Z. (Eds) Functional morphology of trematode and cestode larvae. Alma-Ata: Nauka Press, (in Russian).Google Scholar
Popiel, I. (1976) The ultrastructure of the metacercaria of Cercaria stunkardi Palombi, 1934 (Digenea: Opecoelidae) in an experimental intermediate host, Amphithoe rubricata. Norwegian Journal of Zoology 24, 353364.Google Scholar
Samuelson, J.C. & Caulfield, J.P. (1985) The cercarial glycocalyx of Schistosoma mansoni. Journal of Cell Biology 100, 14231434.CrossRefGoogle ScholarPubMed
Sharma, P.N. & Hanna, R.E.B. (1988) Ultrastructure and cytochemistry of the tegument of Orthocoelium scoliocoelium and Paramphistomum cervi (Trematoda: Digenea). Journal of Helminthology 62, 331343.CrossRefGoogle ScholarPubMed
Shannon, W. Jr. & Bogitsh, B.J. (1971) Megalodicus temperatus: comparative radioautography of glucose-3H and galactose-3H incorporation. Experimental Parasitology 29, 309319.CrossRefGoogle ScholarPubMed
Smyth, J.D. & Halton, D.W. (1983) The physiology of trematodes, 2nd edn.Cambridge, Cambridge University Press.Google Scholar
Stanier, J.E., Woodhouse, M.A. & Griffin, R.L. (1968) Light and electron-microscopic observations on the metacercaria of a Spelotrema sp. (Trematoda: Microphallidae) encysted in Carcinus maenas. Journal of Invertebrate Pathology 10, 269282.CrossRefGoogle ScholarPubMed
Stein, P.C. & Lumsden, R.D. (1971a) The ultrastructure of developing metacercarial cyst of Ascocotyle leighi Burton, 1956 (Heterophyidae). Proceedings of the Helminthological Society of Washington 38, 110.Google Scholar
Stein, P.C. & Lumsden, R.D. (1971b) An ultrastructural and cytochemical study of metacercarial cyst development in Ascocotyle pachycystis Schroeder and Leigh, 1965. Journal of Parasitology 57, 12311246.CrossRefGoogle ScholarPubMed
Strong, P. & Cable, R.M. (1972) Fine structure and development of the metacercarial cyst in Microphallus opacus. Journal of Parasitology 58, 9298.CrossRefGoogle ScholarPubMed
Threadgold, L.T. (1984) Parasitic platyhelminths. in Bereiter, Hahn J., Matoltsy, A.G. & Richards, S.K. (Eds) Biology of the integument.1. Invertebrates. Berlin, Springer-Verlag.Google Scholar
Uglem, G.L. & Larson, O.R. (1987) Facilitated diffusion and active transport systems for glucose in metacercariae of Clinostomum marginatum (Digenea). International Journal for Parasitology 17, 847850.CrossRefGoogle Scholar
Weber, P. & Sonntag, J. (1989) The fine structure of the body wall of adult Paragonimus uterobilateralis. Tropical Medicine and Parasitology 40, 422428.Google ScholarPubMed
Wilson, R.A. & Barnes, P.E. (1974) The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology 68, 239258.CrossRefGoogle ScholarPubMed
Zdarska, Z. & Soboleva, T.N. (1982) Ultrastructure of the tegument of Hasstilesia ovis larval stages. Folia Parasitologica 29, 367370.Google Scholar
Zdarska, A. & Soboleva, T.N. (1984) Ultrastructure of the metacercaria and sporocyst sac of Leucochloridium perturbatum Pojmanska, 1969. Folia Parasitologica 31, 133139.Google Scholar
Zdarska, A., Soboleva, T.N. & Osipovskaya, L.L. (1982) Ultrastructure of the tegument and associated structures of Leucochloridium paradoxum sporocyst and metacercaria. Folia Parasitologica 29, 247251.Google Scholar