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Intra-uterine larval development of the polystomatid monogeneans, Pseudodiplorchis americanus and Neodiplorchis scaphiopodis

Published online by Cambridge University Press:  06 April 2009

J. Cable  and
R. C. Tinsley
J. Cable
Affiliation:
School of Biological Sciences, Queen Mary and Westfield College, London University, Mile End Road, London E1 4NS
R. C. Tinsley
Affiliation:
School of Biological Sciences, Queen Mary and Westfield College, London University, Mile End Road, London E1 4NS
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Abstract

Larvae of the monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis develop within egg capsules retained in the uterus of the parent parasite. This study reveals adaptations for the storage and nutrition of infective stages which have no known precedent amongst other platyhelminths. The vitelline system is greatly reduced and appears to contribute little to embryo nutrition. An electron-dense ‘shell’ which encloses the newly formed embryos is subsequently replaced by a thin flexible sac composed of concentric layers of membranes which are derived from the uterus wall. Further membranes are added to this multi-laminate structure as the encapsulated embryos pass along the uterus, and this enables the sac to expand continuously as the larva inside it grows. The capsule lining extends into fine cytoplasmic processes which ‘plumb in’ to the larval tegument between ciliated cells. These connexions are packed with glycogen and appear to perform a placenta-like function. The unique adaptations correlate with the demands of the life-cycle. Large numbers of oncomiracidia (up to 300) can be packed, in membranous sacs, within the storage capacity of the uterus; direct transfer of nutrients from parent to offspring enables resources to be supplied over an extended period; and infective larvae can be maintained in readiness for an unpredictable opportunity for transmission.

Keywords

MonogeneaPolystomatidaeegglarval developmentultrastructure
Type
Research Article
Information
Parasitology , Volume 103 , Issue 2 , October 1991 , pp. 253 - 266
Copyright
Copyright © Cambridge University Press 1991

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References

Bjorkman, N. & Thorsell, W. (1963). On the fine morphology of the formation of egg-shell globules in the vitelline glands of the liver fluke (Fasciola hepatica L.). Experimental Cell Research 32, 153–6.CrossRefGoogle Scholar
Cable, J. (1989). Ultrastructural adaptations of polystomatid monogeneans to extreme environmental conditions. Ph.D. thesis, University of London.Google Scholar
Coil, W. H. (1965). Observations on egg shell formation in Hydrophitrema gigantica Sauders, 1960 (Hemiuridae: Digenea). Zeitschrift für Parasitenkunde 25, 510–17.CrossRefGoogle Scholar
Coil, W. H. (1987). The early egg of Austramphilina elongata (Cestodaria). Parasitology Research 73, 451–7.CrossRefGoogle Scholar
Coil, W. H. & Kuntz, R. E. (1963). Observations on the histochemistry of Syncoelium spathulatum n. sp. Proceedings of the Helminthological Society, Washington 30, 60–5.Google Scholar
Coil, W. H. & Reid, W. A. (1965). Desmogonius desmogonius Stephens, 1911 (Pronocephalidae: Digenea), a redescription with observations on egg filament formation. Zeitschrift für Parasitenkunde 25, 506–9.CrossRefGoogle ScholarPubMed
Davies, R. E. & Roberts, L. S. (1983). Platyhelminthes – Eucestoda. In Reproductive Biology of Invertebrates. Vol. I. Oogenesis, Oviposition and Oosorption (ed. Adiyodi, K. G. & Adiyodi, R. G.), pp. 109–33. Chichester: J. Wiley & Sons.Google Scholar
Domenici, L. & Gremigni, V. (1977). Fine structure and functional role of the coverings of the eggs in Mesostoma ehrenbergii (Focke) (Turbellaria, Neorhabdocoela). Zoomorphologie 88, 247–57.CrossRefGoogle Scholar
Gremigni, V. & Domenici, L. (1976). Uptake of maternal nutrients during embryonic development in the subitaneous eggs of the turbellarian Mesostoma ehrenbergii (Focke). Monitore Zoologico Italiano 10, 229–38.Google Scholar
Gremigni, V. & Domenici, L. (1977). On the role of specialized, peripheral cells during embryonic development of subitaneous eggs in the turbellarian Mesostoma ehrenbergii (Focke): an ultrastructural and autoradiographic investigation. Acta Embryologiae Experimentalis 2, 251–65.Google Scholar
Halton, D. W., Stranock, S. D. & Hardcastle, A. (1974). Vitelline cell development in monogenean parasites. Zeitschrift für Parasitenkunde 45, 45–61.CrossRefGoogle ScholarPubMed
Holy, J. M. & Wittrock, D. D. (1982). Electron microscopy of eggshell formation in Halipegus eccentricus (Trematoda: Hemiuridae). Proceedings of the Fifth International Congress of Parasitology: Molecular and Biochemical Parasitology Supplement, p. 712.Google Scholar
Holy, J. M. & Wittrock, D. D. (1986). Ulstrastructure of the female reproductive organs (ovary, vitellaria and Mehlis' gland) of Halipegus eccentricus (Trematoda: Derogenidae). Canadian Journal of Zoology 64, 2203–12.CrossRefGoogle Scholar
Irwin, S. W. B. & Threadgold, L. T. (1970). Electron microscope studies on Fasciola hepatica. VIII. The development of the vitelline cells. Experimental Parasitology 28, 399–411.CrossRefGoogle ScholarPubMed
Kawanaka, M., Hayashi, S. & Ohtomo, H. (1983). Nutritional requirements of Schistosoma japonicum eggs. Journal of Parasitology 69, 857–61.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1986). The eggs of monogeneans. Advances in Parasitology 25, 175–273.CrossRefGoogle ScholarPubMed
Lamothe-Argumedo, R. (1986). Monogéneos de los anfibios de México. VII. Hallazgo de Pseudodiplorchis americanus (Rodgers y Kuntz, 1940) Yamaguti 1963 en Baja California sur México. Anales del Instituto de Biología Universidad de Nacional Autónoma México, Zoología 56, 291–300.Google Scholar
Lewis, P. R. & Knight, D. P. (1977). Staining methods for sectioned material. In Practical Methods in Electron Microscopy, vol. 5, part 1 (ed. Glauert, A. M., pp. 159–66. Amsterdam: North-Holland.Google Scholar
Lyukshiria, L. M. (1980). Histochemical study of the vitellaria of Polystoma integerrimum. Konfeneutsiya Ukrainskago Parazitologicheskogo obslichestva Tezisy dokladov Chast 3-Kiev, USSR, Naukova Duinke pp. 41–2.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
Neil, P. J. G., Smith, J. H., Doughty, B. L. & Kemp, M. (1988). The ultrastructure of the Schistosoma mansoni egg. American Journal of Tropical Medicine and Hygiene 39, 52–65.CrossRefGoogle Scholar
Pappas, P. W. & Read, C. P. (1975). Membrane transport in helminth parasites: a review. Experimental Parasitology 37, 469–530.CrossRefGoogle ScholarPubMed
Pence, D. B. (1970). Electron microscope and histochemical studies on the eggs of Hymenolepis diminuta. Journal of Parasitology 56, 84–97.CrossRefGoogle ScholarPubMed
Price, G. D. & Whitecross, M. I. (1983). Cytochemical localisation of ATPase activity on the plasmalemma of Chara corallina. Protoplasma 16, 65–74.CrossRefGoogle Scholar
Rodgers, L. O. (1941). Diplorchis scaphiopi, a new polystomatid monogenean fluke from the spadefoot toad. Journal of Parasitology 27, 153–7.CrossRefGoogle Scholar
Threadgold, L. T. (1982). Fasciola hepatica: stereological analysis of vitelline cell development. Experimental Parasitology 54, 352–65.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1983). Ovoviviparity in platyhelminth life-cycles. Parasitology 86, 161–96.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1990). Host behaviour and opportunism in parasite life cycles. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 158–92. London: Taylor & Francis.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. & Jackson, H. C. (1988). Pulsed transmission of Pseudodiplorchis americanus (Monogenea) between desert toads (Scaphiopus couchii). Parasitology 97, 437–52.CrossRefGoogle Scholar
Tocque, K. (1990). The reproductive strategy of a monogenean parasite in a desert environment. Ph.D. thesis, University of London.Google Scholar
Tocque, K. & Tinsley, R. C. (1991). The influence of desert temperature cycles on the reproductive biology of Pseudodiplorchis americanus (Monogenea). Parasitology 103, 111–19.CrossRefGoogle Scholar
Wattel, W. (1974). PA-TCH-SP: A PAS-type staining method for polysaccharide in electron microscopy. LKB Application Note 147.Google Scholar
Wilson, R. A. (1967). The structure and permeability of the shell and vitelline membrane of the egg of Fasciola hepatica. Parasitology 57, 47–58.CrossRefGoogle Scholar
Wittrock, D. D. (1982). Structure and origin of the eggshell of Quinqueserialis quinqueserialis (Trematoda: Notocotylidae). Zeitschrift für Parasitenkunde 67, 37–44.CrossRefGoogle Scholar
Woods, A. M. & Gay, J. L. (1983). Evidence for a neckband delimiting structural and physiological regions of the host plasma membrane associated with haustoria of Albugo candida. Physiological Plant Pathology 23, 73–88.CrossRefGoogle Scholar