Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T12:45:37.983Z Has data issue: false hasContentIssue false
  • English
  • Français

Ovoviviparity in platyhelminth life-cycles

Published online by Cambridge University Press:  06 April 2009

R. C. Tinsley
R. C. Tinsley
Affiliation:
Department of Zoology, Westfield College, London University, London NW3 7ST
Get access Rights & Permissions [Opens in a new window]

Summary

The encapsulated embryos of platyhelminths may be retained and complete their development in utero in a range of circumstances. However, hatching within the parent (the criterion of ovoviviparity) is relatively rare and larvae generally emerge only after deposition. Viviparity is characterized by the nutritional dependency of the unencapsulated larva upon the parent, but in several cases larvae retained within a shell also receive parental nutrients during intra-uterine development. Uptake of exogenous nutrients via shell pores occurs in Schistosoma mansoni but the eggs, which gain all the advantages of intra-uterine retention, are supported by host nutrients.

Intra-uterine larval development avoids the hazards of development in the external environment and eliminates the time delay between oviposition and infection. Deposition of immediately infective offspring may be concentrated in time and space to exploit periods of host vulnerability. The control and precision of transmission is illustrated by examples in which the opportunity for invasion is restricted because of either host behaviour or environmental instability. This strategy has been an important factor in the evolution of polystomatid monogeneans, and its effectiveness is demonstrated by comparison of the life-cycles of Polystoma integerrimum and Pseudodiplorchis americanus. Ovoviviparity also increases reproductive potential in some polystomatids by extending the period of multiplication and by increasing established populations through internal re-infection. In Eupolystoma alluaudi, the capacity for ovoviviparity is programmed into larval development and this regulates population growth within individual hosts.

Type
Research Article
Information
Parasitology , Volume 86 , Issue 4 , April 1983 , pp. 161 - 196
Copyright
Copyright © Cambridge University Press 1983

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

Anderson, M. (1981). The change with host age of the composition of the ancyrocephaline (monogenean) populations of parasites on thick-lipped grey mullets at Plymouth. Journal of the Marine Biological Association of the United Kingdom 61, 833–42.CrossRefGoogle Scholar
Beverley-Burton, M. (1962). Some monogenetic trematodes from Amphibia in Southern Rhodesia including a new species, Polystoma mashoni sp.n., from Bufo regularis (Reuss). Journal of Parasitology 48, 752–7.CrossRefGoogle ScholarPubMed
Bourgat, R. (1977). Étude comparative des polystomes (Monogènes) de ranidés (Anoures) du sud Togo. Description de Polystoma togoensis n.sp. Bulletin du Museum National d'histoire naturelle (Paris), serie 3 Zoologie 312, 447–63.Google Scholar
Bourgat, R. & Salami-Cadoux, M.-L. (1974). Contribution à l'étude de Eupolystoma alluaudi (de Beauchamp, 1913) (Monogenea: Polystomatidae). Annates de Parasitologie humaine et comparee (Paris) 48, 755–60.CrossRefGoogle Scholar
Bovet, J. (1967). Contribution à la morphologie et à la biologie de Diplozoon paradoxum v. Nordmann, 1832. Bulletin de la Société neuchdteloise des Sciences naturelles 90, 63–159.Google Scholar
Burton, P. R. (1962). In vitro uptake of radioglucose by a frog lung-fluke and correlation with the histochemical identification of glycogen. Journal of Parasitology 48, 874–82.CrossRefGoogle ScholarPubMed
Bychowsky, B. E. (1957). Monogenetic Trematodes, their Classification and Phytogeny. Moscow and Leningrad: Academy of Sciences U.S.S.R (in Russian). English translation by Hargis, W. J. and Oustinoff, P. C. (1961). Washington: American Institute of Biological Sciences.Google Scholar
Chubb, J. C. (1977). Seasonal occurrence of helminths in freshwater fishes. Part I Monogenea. In Advances in Parasitology vol. 15 (ed. Dawes, B.) pp. 133–199. London and New York: Academic Press.Google Scholar
Combes, C. (1967). Biologie des Polystomatidae (Monogenea): existence et démonstration expérimentale des possibilites de cycle interne direct. Bulletin de la Société Zoologique de France 92, 129–33.Google Scholar
Combes, C. (1968). Biologie, écologie des cycles et biogéographie de digènes et monogenes d'amphibiens dans l'est des Pyrénées. Memoires du Muséum National d'histoire naturelle (Paris), série A Zoologie 51, 1–195.Google Scholar
Combes, C. (1972). Ecologie des Polystomatidae (Monogenea): facteurs influencant le volume et la rythme de la ponte. International Journal for Parasitology 2, 233–8.CrossRefGoogle Scholar
Combes, C. (1981). In Biology of Monogeneans (Workshop 4, EMOP 3). Parasitology 82, 63–4.Google Scholar
Combes, C., Bourgat, R. & Salami-Cadoux, M.-L. (1976). Valeur adaptative du mode de transmission chez les Polystomatidae (Monogenea). Bulletin d'Ecologie 7, 207–14.Google Scholar
Combes, C. & Channing, A. (1978–1979). Polystomatidae (Monogenea) d'amphibiens d'Afrique du Sud: Polystoma natalensis n.sp., parasite de Strongylopus grayi (Smith, 1849). Vie Milieu 28–, 61–8.Google Scholar
Crandall, R. B. (1960). The life history and affinities of the turtle lung-fluke, Heronimus chelydrae MacCallum, 1902. Journal of Parasitology 46, 289–307.CrossRefGoogle ScholarPubMed
Duellman, W. E. & Lescure, J. (1973). Life history and ecology of the hylid frog Osteocephalus taurinus, with observations on larval behavior. Occasional papers of the Museum of Natural History, (Kansas) 13, 1–12.Google Scholar
Dupouy, J. & Combes, C. (1977). Existence d'un cycle interne de reproduction chez Polystoma grassei Euzet, Combeset Knoepffler, 1966 (Monogenea; Polystomatidae) en Afrique équatoriale. Annates des Sciences Naturelles (Paris), Zoologie 19, 397–400.Google Scholar
Euzet, L., Bourgat, R. & Salami-Cadoux, M.-L. (1974). Polystoma galamensis (Monogenea) parasite de Rana galamensis Duméril et Bibron, 1841, au Togo. Annates de Parasitologic humaine et comparée (Paris) 49, 63–8.CrossRefGoogle Scholar
Euzet, L. & Combes, C. (1964). Sur un Polystomatidae (Monogenea) récolté à Madagascar chez Rana mascareniensis Duméril et Bibron. Bulletin de la Société Zoologique de France 89, 392–401.Google Scholar
Euzet, L. & Combes, C. (1965). Parasites des cheloniens malgaches: Polystomoides chabaudi n.sp. (Monogenea) chez la tortue d'eau douce Pelomedusa subrufa Lacépède, 1788. Annates de Parasitologic humaine et comparee (Paris) 40, 445–50.CrossRefGoogle Scholar
Fournier, A. & Combes, C. (1979). Demonstration d'une dualité évolutive des embryons chez Eupolystoma alluaudi (Monogenea: Polystomatidae) et de son rĉle dans la genese du cycle interne. Comptes rendus de l'Academie des Sciences (Paris) D 289, 745–7.Google Scholar
Gallien, L. (1935). Recherches experiméntales sur la dimorphisme évolutif et la biologie de Polystoma integerrimum Frohl. Travaux du Station de Zoologie, Wimereux 12, 1–181.Google Scholar
Guilford, H. G. (1961). Gametogenesis, egg-capsule formation, and early miracidial development in the digenetic trematode Halipegus eccentricus Thomas. Journal of Parasitology 47, 757–64.CrossRefGoogle ScholarPubMed
Harris, P. D. (1982). Studies on the biology of the Gyrodactyloidea (Monogenea). Ph.D. thesis, University of London.Google Scholar
Harris, P. D. (1983). The morphology and life-cycle of the oviparous Öogyrodactylus farlowellae gen. et sp. nov. (Monogenea: Gyrodactyloidea). Parasitology (in the Press).Google Scholar
Holy, J. M. & Wittrock, D. D. (1982). Electron microscopy of egg shell formation in Halipegus eccentricus (Trematoda: Hemiuridae). Proceedings of the Fifth International Congress of Parasitology: Molecular and Biochemical Parasitology Supplement, p. 712.Google Scholar
Johnston, S. J. (1912). On some trematode parasites of Australian frogs. Proceedings of the Linnean Society of New South Wales 37, 285–353.CrossRefGoogle Scholar
Kearn, G. C. (1981). In Biology of Monogeneans (Workshop 4, EMOP 3). Parasitology 82, 57–9.Google Scholar
Kearn, G. C. & Macdonald, S. (1976). The chemical nature of host hatching factors in the monogenean skin parasites Entobdella soleae and Acanthocotyle lobianchi. International Journal for Parasitology 6, 457–66.CrossRefGoogle ScholarPubMed
Ktari, M. H. (1977). Le parasitisme d'Echeneis naucrates L. (Poisson: Téléostéen) par deux monogènes (Monopisthocotylea) du genre Dionchus: D. agassizi Goto, 1899 et D. remorae MacCallum, 1916. Excerta Parasitologica en memoria del doctor Eduardo Caballero y Caballero, Instituto de Biologia, (Mexico) pp. 61–67.Google Scholar
Kulo, S. D. (1980). Parasites de chéloniens en Afrique intertropicale: Polystomoides nabedei n.sp. (Monogenea: Polystomatidae), parasite de la vessie urinaire de la tortue d'eau douce Pelomedusa subrufa Lacépède, 1788 (Chélonien: Pelomedusidae). Annates de Parasitologic humaine et comparée (Paris) 55, 367–77.CrossRefGoogle Scholar
Lees, E. (1962). The incidence of helminth parasites in a particular frog population. Parasitology 52, 95–102.CrossRefGoogle Scholar
Lewert, R. M., Para, J. & Ozcel, M. A. (1970). Miracidial uptake of glucose in intact eggs of Schistosoma mansoni. Journal of Parasitology 56, 1250–1.CrossRefGoogle ScholarPubMed
Llewellyn, J. (1962). The life histories and population dynamics of monogenean gill parasites of Trachurus trachurus (L.). Journal of the Marine Biological Association of the United Kingdom 42, 587–600.CrossRefGoogle Scholar
Llewellyn, J. (1972). Behaviour of monogeneans. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. and Wright, C. A.). Supplement 1 to the Zoological Journal of the Linnean Society 51, 19–30.Google Scholar
Llewellyn, J. (1981). In Biology of Monogeneans (Workshop 4, EMOP 3). Parasitology 82, 64–6.Google Scholar
Macdonald, S. (1974). Host skin mucus as a hatching stimulant in Acanthocotyle lobianchi, a monogenean from the skin of Raja spp. Parasitology 68, 331–8.CrossRefGoogle ScholarPubMed
Macdonald, S. & Llewellyn, J. (1980). Reproduction in Acanthocotyle greeni n.sp. (Monogenea) from the skin of Raia spp. at Plymouth. Journal of the Marine Biological Association of the United Kingdom 60, 81–8.CrossRefGoogle Scholar
Maeder, A.-M. (1973). Monogènes et trématodes parasites d'amphibiens en Côte d'lvoire. Revue suisse de Zoologie 80, 267–322.CrossRefGoogle Scholar
Michaels, R. M. & Prata, A. (1968). Evolution and characteristics of Schistosoma mansoni eggs laid in vitro. Journal of Parasitology 54, 921–30.CrossRefGoogle ScholarPubMed
Murith, D. (1981 a). Contribution à l'étude de la systématique des polystomes (Monogenea: Polystomatidae) parasites d'amphibiens (Anoures) de basse Cĉte d'lvoire. Revue Suisse de Zoologie 88, 475–533.CrossRefGoogle Scholar
Murith, D. (1981 b). Contribution à l'étude de la biologie du developpement des polystomes (Monogenea) parasites d'amphibiens (Anoures) de basse Cote d'lvoire. Bulletin de la Société neuchâteloise des Sciences naturelles 104, 5–33.Google Scholar
Murith, D., Gassmann, M. M. & Vaucher, C. (1978). Contribution à l'étude des polystomes d'amphibiens du Cameroun. Revue Suisse de Zoologie 85, 681–98.CrossRefGoogle Scholar
Murith, D., Vaucher, C. & Combes, C. (1977). Coexistence de la néoténie et du cycle interne chez un Polystomatidae (Monogenea). Comptes rendus de l'Académie des Sciences (Paris) D 284, 187–90.Google Scholar
Nollen, P. M. (1968). Uptake and incorporation of glucose, tyrosine, leucine and thymidine by adult Philophthalmus megalurus (Cort, 1914) (Trematoda), as determined by autoradiography. Journal of Parasitology 54, 295–304.CrossRefGoogle ScholarPubMed
Nollen, P. M., Restaino, A. L. & Alberico, R. A. (1973). Gorgoderina attenuata: uptake and incorporation of tyrosine, thymidine and adenosine. Experimental Parasitology 33, 468–76.CrossRefGoogle ScholarPubMed
Oglesby, L. C. (1961). Ovoviviparity in the monogenetic trematode Polystomoidella oblonga. Journal of Parasitology 47, 237–43.CrossRefGoogle ScholarPubMed
Oliver, G. (1978). Description des deux cas d'ovoviviparité chez les Diplectanidae Bychowsky, 1957 (Monogenea: Monopisthocotylea). Zeitschrift für Parasitenkunde 57, 247–50.CrossRefGoogle Scholar
Ozaki, Y. (1935 a). Studies on the frog trematode Diplorchis ranae. I. Morphology of the adult form with a review of the family Polystomatidae. Journal of Science of the Hiroshima University, Series B 3, 193–225.Google Scholar
Ozaki, Y. (1935 b). Studies on the frog trematode Diplorchis ranae. II. Morphology and behaviour of the swimming larva. Journal of Science of the Hiroshima University, Series B 4, 23–4.Google Scholar
Paling, J. E. (1965). The population dynamics of the monogenean gill parasite Discocotyle sagittata Leuckart, on Windermere trout, Salmo trutta L. Parasitology 55, 667–94.CrossRefGoogle ScholarPubMed
Paul, A. A. (1938). Life history studies of North American freshwater polystomes. Journal of Parasitology 24, 489–510.CrossRefGoogle Scholar
Prudhoe, S. & Bray, R. A. (1982). Platyhelminth Parasites of the Amphibia. British Museum (Natural History) and Oxford University Press.Google Scholar
Race, G. J., Michaels, R. M., Martin, J. H., Larsh, J. E. Jr & Matthews, J. L. (1969). Schistosoma mansoni eggs: an electron microscope study of shell pores and microbarbs. Proceedings of the Society for Experimental Biology and Medicine 130, 990–2.CrossRefGoogle ScholarPubMed
Radha, E. (1975). Studies on the monogenean fauna of Madras coast. Rivista di Parassitologia 36, 7–27.Google Scholar
Rees, F. G. (1939). Studies on the germ-cell cycle of the digenetic trematode Parorchis acanthus Nicoll. Part I. Anatomy of the genitalia and gametogenesis in the adult. Parasitology 31, 417–33.CrossRefGoogle Scholar
Rees, F. 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, 372–91.CrossRefGoogle Scholar
Salami-Cadoux, M.-L. (1975). Transmission et développement du monogène réno-vésical. Eupolystoma alluaudi (de Beauchamp, 1913) Euzet et Combes, 1967. Bulletin de la Socieéé Zoologique de France 100, 283–92.Google Scholar
Salami-Cadoux, M.-L. (1979). Cycles et epidiemiologie de Polystomatidae parasites de l'am-phibien Bufo regularis Reuss au Togo. These de Doctorat, Universite de Perpignan.Google Scholar
Savage, R. M. (1950). Observations on some natural epizootics of the trematode Polystoma integerrimum among tadpoles of Rana temporaria temporaria. Proceedings of the Zoological Society, London 120, 15–37.CrossRefGoogle Scholar
Sternholm, R. L. & Warren, K. S. (1974). Schistosoma mansoni: utilization of exogenous metabolites by eggs in vitro. Experimental Parasitology 36, 222–32.CrossRefGoogle Scholar
Tinsley, R. C. (1973). Observations of Polystomatidae (Monogenoidea) from East Africa with a description of Polystoma makereri n. sp. Zeitschrift für Parasitenkunde 42, 251–63.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1974). Observations on Polystoma africanum Szidat with a review of the inter-relationships of Polystoma species in Africa. Journal of Natural History 8, 355–67.CrossRefGoogle Scholar
Tinsley, R. C. (1978 a) The morphology and distribution of Eupolystoma species (Monogenoidea) in Africa, with a description of E. anterorchis sp.n. from Bufo pardalis at the Cape. Journal of Helminthology 52, 291–302.CrossRefGoogle Scholar
Tinsley, R. C. (1978 b). Oviposition, hatching and the oncomiracidium of Eupolysloma anterorchis (Monogenoidea). Parasitology 77, 121–32.CrossRefGoogle Scholar
Tinsley, R. C. (1978 c). The role of ovoviviparity in the transmission of polystomatid mono-geneans. Parasitology 77, v.Google Scholar
Tinsley, R. C. (1982 a). Pseudodiplorchis americanus (Monogenea): synchronisation of transmission with restricted host availability. Proceedings of the Fifth International Congress of Parasitology: Molecular and Biochemical Parasitology Supplement p. 459.Google Scholar
Tinsley, R. C. (1982 b). The reproductive strategy of a polystomatid monogenean in a desert environment. Parasitology 85, xv.Google Scholar
Tinsley, R. C. & Earle, C. M. (1983). Invasion of vertebrate lungs by the polystomatid monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 86, 501–17.CrossRefGoogle Scholar
Tinsley, R. C. & Owen, R. W. (1975). Studies on the biology of Protopolystoma xenopodis (Monogenoidea): the oncomiracidium and life cycle. Parasitology 71, 445–63.CrossRefGoogle Scholar
Thurston, J. P. (1968). The larva of Oculotrema hippopotami (Monogenea: Polystomatidae). Journal of Zoology 154, 475–80.CrossRefGoogle Scholar
Van der Lande, V. M. & Tinsley, R. C. (1976). Studies on the anatomy, life history and behaviour of Marsupiobdella africana (Hirudinea: Glossiphoniidae). Journal of Zoology 180, 537–63.CrossRefGoogle Scholar
Vande Vusse, F. J. (1976). Parapolystoma crooki sp. n. (Monogenea: Polystomatidae) from Rana magna in the Philippines. Journal of Parasitology 62, 552–5.CrossRefGoogle Scholar
Vaucher, C. (1981). Mesopolystoma samiriensis n. gen., n. sp. (Monogenea: Polystomatidae), parasite de Osteocephalus taurinus Steindachner (Amphibia: Hylidae) en Amazonie peruvienne. Revue Suisse de Zoologie 88, 797–802.CrossRefGoogle Scholar
Williams, J. B. (1960). The dimorphism of Polystoma inlegerrimum (Frolich) Rudolphi and its bearing on relationships within the Polystomatidae: Part I. Journal of Helminthology 34, 151–92.CrossRefGoogle Scholar
Wilson, R. A., Smith, G. & Thomas, M. R. (1982). Fascioliasis. In The population Dynamics of Infectious Diseases: Theory and Applications (ed. Anderson, R. M.). London and New York: Chapman and Hall.Google Scholar
Zeller, E. (1872). Untersuchungen über die Entwicklung und den Bau des Polystomum integerrimum Rud. Zeitschrift für Wissenschaftliche Zoologie 22, 1–28.Google Scholar