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Patterns of sexual reproduction among parasitic platyhelminths

Published online by Cambridge University Press:  06 April 2009

P. M. Nollen
P. M. Nollen
Affiliation:
Department of Biological Sciences, Western Illinois University, Macomb, Illinois 61455, USA
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Summary

Previous studies on the spermatogenesis and oogenesis of digeneans, monogeneans and cestodes are reviewed, including those in which isotopic labelling techniques have been utilized in order to determine the temporal duration of spermatogenic development stages. Similar labelling experiments have also provided information on the development and movement of oocytes in the female reproductive tract as well as indicating patterns of cell division and development in vitelline glands. The literature relating to the inseminative behaviour of parasitic platyhelminths is considered from a number of viewpoints including the patterns of cross-and self-insemination that occur in hermaphroditic digeneans, the mating behaviour of dioecious schistosomes, spermatophore production and insemination among monogeneans and the inseminative behaviour of polyzoic cestodes. The implications of selfing among parasitic platyhelminths are considered with respect to possible genetically deleterious consequences. In addition, consideration is given to the mechanisms underlying the fact that some species require cross-insemination or at least the presence of another worm in order to undergo normal growth and sexual development. Finally, experimental studies are reviewed which shed light on the strength of the barriers against hybridization that exist between well-defined species of parasitic platyhelminths.

Type
Research Article
Information
Parasitology , Volume 86 , Issue 4 , April 1983 , pp. 99 - 120
Copyright
Copyright © Cambridge University Press 1983

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References

REFERENCES

Anderson, M. C. (1935). Gametogenesis in the primary generation of a digenetic trematode, Proterometra macrostoma Horsfall, 1935. Transactions of the American Microscopical Society 54, 271–97.CrossRefGoogle Scholar
Armstrong, J. C. (1965). Mating behaviour and development of schistosomes in the mouse. Journal of Parasitology 51, 605–16.CrossRefGoogle ScholarPubMed
Atkinson, K. H. & Atkinson, B. G. (1980). Biochemical basis for the continuous copulation of female Schistosoma mansoni. Nature, London 283, 478–9.CrossRefGoogle ScholarPubMed
Awwad, M. & Bell, D. R. (1978) Faecal extract attracts copulating schistosomes. Annals of Tropical Medicine and Parasitology 72, 389–90.CrossRefGoogle ScholarPubMed
Bacha, W. J. (1966). Viable egg production in Zygocotyle lunata following monometacercarial infections. Journal of Parasitology 52, 1216–17.CrossRefGoogle ScholarPubMed
Beaver, P. C. (1937). Experimental studies on Echinostoma revolutum (Froelich) a fluke from birds and mammals. Illinois Biological Monographs 15, 131–48.Google Scholar
Berntzen, H. K. & Mueller, J. F. (1972). In vitro cultivation of Spirometra spp. (Cestoda) from the plerocercoid to gravid adult. Journal of Parasitology 58, 750–2.CrossRefGoogle ScholarPubMed
Blankespoor, H. D. (1974). Host induced variation in Plagiorchis nobeli Park, 1936 (Plagior-chidae: Trematoda). American Midland Naturalist 92, 415–33.CrossRefGoogle Scholar
Boddington, M. J. & Mettrick, D. F. (1981). Production and reproduction in Hymenolepis diminuta (Platyhelminthes: Cestoda). Canadian Journal of Zoology 59, 1962–72.CrossRefGoogle Scholar
Burton, P. R. (1960). Gametogenesis and fertilization in the frog lung fluke, Haematoleochus medioplexus Stafford (Trematoda: Plagiorchiidae). Journal of Morphology 107, 93–121.CrossRefGoogle ScholarPubMed
Buttner, A. (1955). Les distomes progenetiques sont-ils des pre-adultes ou des adultes veritables? Baleur evolutive de la progenese chez les Digenea. Comptes Rendus Societe de Biologic 149, 267–72.Google Scholar
Bychowski, B. E. (1961). Monogenetic Trematodes, their Classification and Phylogeny. Moscow: Leningrad Academy of Science USSR. English translation by Hargis, W. J. and Oustinoff, P. C.. Washington DC, American Institute of Biological Sciences.Google Scholar
Cable, R. M. (1931). Studies on the germ cell cycle of Cryptocotyle lingua Creplin. I. Gametogenesis in the adult. Quarterly Journal of Microscopical Science 74, 563–89.Google Scholar
Chen, P. D. (1937). The germ cell cycle in the trematode Paragonimus kellicotti Ward. Transactions of the American Microscopical Society 56, 208–36.CrossRefGoogle Scholar
Ciordia, H. (1956). Cytological studies of the germ cell cycle in the trematode family Bucephalidae. Transactions of the American Microscopical Society 75, 103–16.CrossRefGoogle Scholar
Clough, E. R. (1981). Morphology of reproductive organs and oogenesis in bisexual and unisexual transplants of mature Schistosoma mansoni females. Journal of Parasitology 67, 535–9.CrossRefGoogle ScholarPubMed
Colgan, G. J. & Nollen, P. M. (1977). Studies on the growth, development, and infectivity of Philophthalmus hegeneri Penner and Fried 1963 in the chick. Journal of Parasitology 63, 675–80.CrossRefGoogle ScholarPubMed
Cornford, E. M. & Hunt, M. E. (1981). Glucose transfer from male to female schistosomes. Science 213, 1269–71.CrossRefGoogle Scholar
Cox, D. D., Ciordia, H. & Jones, A. W. (1956). Variations in Hymenolepis serrula Oswald 1951 (Cestoda: Hymenolepidae) a cestode from the smoky shrew, Sorex fumeus Millon 1895, with special reference to three geographic areas. Journal of the Tennessee Academy of Sciences 31, 289–99.Google Scholar
Douglas, L. T. (1963). The development of organ systems in nematotaeniid cestodes. III. Gametogenesis and embryonic development in Baerietta diana and Distoichometra kozloffi. Journal of Parasitology 49, 530–58.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1973). A comparative study of the reproductive system of mature, immature, and ‘unisexual’ female Schistosoma mansoni. Parasitology 67, 165–83.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1975). Schistosoma mansoni: development of the vitelline cell, its role in drug sequestration and changes induced by astiban. Parasitology 38, 240–56.Google ScholarPubMed
Erasmus, D. A., Popiel, I. & Shaw, J. R. (1982). A comparative study of the vitelline cell in Schistosoma mansoni S. haematobium S. japonicum and S. matthei. Parasitology 84, 283–7.CrossRefGoogle Scholar
Fairley, N. H. (1920). A comparative study of experimental Bilharziasis in monkeys contrasted to the hitherto described lesions in man. Journal of Pathology and Bacteriology 23, 289–314.CrossRefGoogle Scholar
Fan, P. C. & Chiang, C. H. (1970). Exposure of kittens and puppies to single metacercariae of Paragonimus westermani from Taiwan. Journal of Parasitology 56, 48–54.CrossRefGoogle ScholarPubMed
Faust, E. C. & Meleney, H. E. (1924). Studies on schistosomiasis japonicum. American Journal of Hygiene Monograph Series 3, 1–339.Google Scholar
Faust, E. C., Jones, C. A. & Hoffman, W. A. (1930). Studies on schistosomiasis mansoni in Puerto Rico II. Biological studies 2. The mammalian phase of the life cycle. Puerto Mean Journal of Public Health and Tropical Medicine 10, 133–96.Google Scholar
Featherston, D. W. (1971). Taenia hydatigera III. Light and electron microscope study of spermatogenesis. Zeitschrift fur Parasitenkunde 37, 148–68.Google Scholar
Fletcher, M., Woodruff, D. S., Loverde, P. T. & Asch, H. L. (1980). Genetic differences between Schistosoma mekongi and Schistosoma japonicum: an electrophoretic study. In The Mekong Schistosome, Malacological Reviews, Suppl. 2, pp. 113–22.Google Scholar
Floyd, R. D. & Nollen, P. M. (1977). Effects of stressful conditions on the development and movement of reproductive cells in Schistosoma mansoni. Journal of Parasitology 63, 87–90.CrossRefGoogle ScholarPubMed
Foreyt, W. J. & Todd, A. C. (1976). Development of the large American liver fluke, Fascioloides magna, in white-tailed deer, cattle, and sheep. Journal of Parasitology 62, 26–32.CrossRefGoogle ScholarPubMed
Foreyt, W. J., Samuel, W. M. & Todd, A. C. (1977). Fascioloides magna in white-tailed deer (Odocoileus virginianus): Observations on the pairing tendency. Journal of Parasitology 63, 1050–2.CrossRefGoogle ScholarPubMed
Fried, B. (1962). Growth of Philophthalmus sp. (Trematoda) in the eyes of chicks. Journal of Parasitology 48, 395–9.CrossRefGoogle ScholarPubMed
Fried, B. & Alenick, D. S. (1981). Localization, length, and reproduction in single- and multiple-worm infections of Echinostoma revolutum (Trematoda) in the chick. Parasitology 82, 49–53.CrossRefGoogle ScholarPubMed
Fried, B. & Gioscia, R. M. (1976). Tentative identification of cholesterol as a chemoattractant for metacercarial pairing in Leucochloridiomorpha constantiae (Trematoda). Journal of Parasitology 62, 326–7.CrossRefGoogle Scholar
Fried, B. & Harris, K. R. (1971). Reproduction in single- and double-worm infections of Leucochloridiomorpha constantiae (Mueller, 1935) in the chick. Journal of Parasitology 57, 866–8.CrossRefGoogle Scholar
Fried, B. & Holmes, M. L. (1979). Further studies on the development of Leucochloridiomorpha constantiae (Trematoda) metacercariae on the chick chorioallantois. Proceedings of the Helminthological Society of Washington 46, 70–3.Google Scholar
Fried, B. & Roberts, T. M. (1972). Pairing in Leucochloridiomorpha constantiae (Mueller, 1935) (Trematoda) in vitro, in the chick, and on the chorioallantois. Journal of Parasitology 58, 88–91.CrossRefGoogle ScholarPubMed
Fried, B. & Robinson, G. A. (1981). Pairing and aggregation of Amblosoma suwaense (Trematdoa: Brachylaimidae) metacercariae in vitro and partial characterization of lipid involved in chemo-attraction. Parasitology 82, 225–9.CrossRefGoogle Scholar
Fried, B., Tancer, R. B. & Fleming, S. J. (1980). In vitro pairing of Echinostoma revolutum (Trematoda) metacercariae and adults and characterization of worm products involved in chemoattraction. Journal of Parasitology 66, 1014–8.CrossRefGoogle ScholarPubMed
Gönnert, R. (1955). Schistosomiasis Studien II. Über die Eibildung bei Schistosoma mansoni und das Schicksal der Wirtsorganismis. Zeitschrift für Tropenmedicine und Parasitologie 6, 33–52.Google Scholar
Gresson, R. A. R. (1964). Oogenesis in the hermaphroditic Digenea (Trematoda). Parasitology 54, 409–21.CrossRefGoogle Scholar
Guilford, H. G. (1955). Gametogenesis in Heronimus chelydrae McCallum. Transactions of the American Microscopial Society 74, 182–90.CrossRefGoogle Scholar
Halton, D. W. & Hardcastle, A. (1976). Spermatogenesis in a monogenean, Diclidophora merlangi. International Journal for Parasitology 6, 43–53.CrossRefGoogle Scholar
Halton, D. W., Stranock, S. D. & Hardcastle, A. (1974). Vitelline cell development in monogenean parasites. Zeitschrift für Parasitenkunde 45, 45–61.CrossRefGoogle ScholarPubMed
Halton, D. W., Stranock, S. D. & Hardcastle, A. (1976). Fine structure observations on oocyte development in monogeneans. Parasitology 73, 13–23.CrossRefGoogle ScholarPubMed
Hashiguchi, Y., Takei, T. & Miyazaki, I. (1969) Studies on a single worm infection of albino rats with Paragonimus ohirai Miyazaki, 1939. Japanese Journal of Parasitology 18, 612–17.Google Scholar
Howell, M. J. & Bearup, A. J. (1967). The life histories of two bird trematodes of the family Philophthalmidae. Proceedings of the Linnean Society of New South Wales 9, 182–94.Google Scholar
Hyman, L. H. (1951). The Invertebrates, vol. 2. Platyhelminthes and Rhyncocoela. New York: McGraw-Hill.Google Scholar
Imperia, P. S., Fried, B. & Eveland, L. K. (1980). Pheromonal attraction of Schistosoma mansoni females toward males in the absence of worm-tactile behaviour. Journal of Parasitology 66, 682–4.CrossRefGoogle Scholar
Irwin, S. W. B. & Threadoold, L. T. (1970). Electron-microscope studies on Fasciola hepatica VIII. The development of the vitelline cells. Experimental Parasitology 28, 399–411.CrossRefGoogle ScholarPubMed
Jones, A. W. (1951). Hybridization in the tapeworm. Journal of Heredity 42, 264–6.CrossRefGoogle Scholar
Jones, A. W., Fitzgerald, M. D., Proffitt, M. R., Tan, B. D. & Ward, H. L. (1971). Prolonged selfing in Hymenolepis microstoma (Cestoda). Experimental Parasitology 29, 223–9.CrossRefGoogle ScholarPubMed
Kazacos, K. & Mackiewicz, J. S. (1972). Spermatogenesis in Hunterella nodulosa Mackiewicz and McCrae, 1966 (Cestoidea: Caryophyllidae). Zeitschrift für Parasitenkunde 38, 21–31.CrossRefGoogle Scholar
Kearn, G. C. (1970). The production, transfer and assimilation of spermatophores by Entobdella soleae, a monogenean skin parasite of the common sole. Parasitology 60, 301–11.CrossRefGoogle ScholarPubMed
Khalil, G. M. & Cable, R. M. (1968). Germinal developments in Philophthalmus megalurus (Cort, 1914) (Trematoda: Digenea). Zeitschrift fiir Parasitenkunde 31, 211–31.Google ScholarPubMed
Kinsella, J. M. (1971). Growth, development and intraspecific variation of Quinqueserialis quinquiserialis (Trematoda: Notocotylidae) in rodent hosts. Journal of Parasitology 57, 62–70.CrossRefGoogle Scholar
Kitajima, E. W., Parense, W. L. & Correa, L. R. (1976). The fine structure of Schistosoma mansoni sperm (Trematoda: Digenea). Journal of Parasitology 62, 215–21.CrossRefGoogle ScholarPubMed
Kolzow, R. G. & Nollen, P. M. (1978). Effects of stressful conditions on the development and movement of reproductive cells in Schistosoma japonicum. Journal of Parasitology 64, 994–7.CrossRefGoogle ScholarPubMed
Leon, N. (1927). Accouplement et fecondation du Fasciola hepatica. Annates de Parasitologie Humaine et Comparée 5, 230–8.Google Scholar
Lie, K. J. (1965). Studies on Echinostomatidae. (Trematoda) in Malaya. IX. The Mehlis' gland complex in echinostomes. Journal of Parasitology 51, 789–92.CrossRefGoogle Scholar
Lindner, E. (1914). Uber die Spermatogenese von Schistosoma haematobium Bilh. mit besonderer Beruchsichtigung der Geschlechtschromosomen. Archiv für Zellforschung 12, 516–38.Google Scholar
Llewellyn, J. & Euzet, L. (1964). Spermatophores in the monogenean Entobdella diadema Monticelli from the skin of stingrays, with a note on the taxonomy of the parasite. Parasitology 54, 337–44.CrossRefGoogle Scholar
Macdonald, S. & Caley, J. (1975). Sexual reproduction in the monogenean Diclidophora merlangi: Tissue penetration by sperms. Zeitschrift für Parasitenkunde 45, 323–34.CrossRefGoogle ScholarPubMed
Macfarlane, W. V. (1939). Life-cycle of Coitocaecum anaspidis Hickman, a New Zealand digenetic trematode. Parasitology 31, 172–84.CrossRefGoogle Scholar
Markell, E. K. (1939). Gametogenesis and egg shell formation in Probolitrema californiense Stunkard 1935 (Trematoda: Gorgoderidae). Transactions of the American Microscopical Society 62, 27–56.CrossRefGoogle Scholar
Martin, D. R. (1969). Lecithodendriid trematodes from the bat Peropteryz kappleri in Columbia including a discussion of allometric growth and significance of ecological isolation. Proceedings of the Helminthological Society of Washington 36, 250–60.Google Scholar
Mayr, E. (1969). The biological meaning of species. Biological Journal of the Linnean Society 1, 311–20.CrossRefGoogle Scholar
Michaels, R. M. (1969). Mating of Schistosoma mansoni in vitro. Experimental Parasitology 25, 58–71.CrossRefGoogle ScholarPubMed
Moore, D. V., Yolles, T. K. & Meleney, H. E. (1954). The relationship of male worms to the sexual development of female Schistosoma mansoni. Journal of Parasitology 40, 166–85.CrossRefGoogle Scholar
Moseley, C. & Nollen, P. M. (1973). Autoradiographic studies on the reproductive system of Philophthalmus hegeneri Penner and Fried, 1963. Journal of Parasitology 59, 650–4.CrossRefGoogle ScholarPubMed
Nelson, P. D. & Fried, B. (1979). Growth and reproduction in single- and ten-worm infections of Zygocotyle lunata (Trematoda) in the chick. Zeitschrift für Parasitenkunde 60, 97–100.CrossRefGoogle Scholar
Nez, M. M. & Short, R. B. (1957). Gametogenesis in Schistosomatium douthitti (Cort) (Schisto-somatidae: Trematoda). Journal of Parasitology 43, 167–82.CrossRefGoogle ScholarPubMed
Niyamasena, S. G. (1940). Chromosomen und Geschlecht bei Bilharzia mansoni. Zeitschrift für Parasitenkunde 11, 690–701.CrossRefGoogle Scholar
Nollen, P. M. (1968). Autoradiographic studies on reproduction in Philophthalmus megalurus (Cort, 1914) (Trematoda). Journal of Parasitology 54, 43–8.CrossRefGoogle ScholarPubMed
Nollen, P. M. (1971). Viability of a self-fertilizing strain of Philophthalmus megalurus (Trematoda: Digenea). Journal of Parasitology 57, 1222–6.CrossRefGoogle ScholarPubMed
Nollen, P. M. (1975). Studies on the reproductive system of Hymenolepis diminuta using autoradiography and transplantation. Journal of Parasitology 61, 100–4.CrossRefGoogle ScholarPubMed
Nollen, P. M. (1978). Studies on the reproductive system of Philophthalmus gralli using autoradiography and transplantation. Journal of Parasitology 64, 613–6.CrossRefGoogle Scholar
Nollen, P. M. (1981). Localization of [3H]thymidine in oocyte mitochondria from Schistosoma mansoni. Journal of Parasitology 67, 355–61.CrossRefGoogle ScholarPubMed
Nollen, P. M., Floyd, R. D., Kolzow, R. G. & Deters, D. L. (1976). The timing of reproductive cell development and movement in Schistosoma mansoni, Schistosoma japonicum, and Schistosoma haematobium using techniques of autoradiography and transplantation. Journal of Parasitology 62, 227–31.CrossRefGoogle ScholarPubMed
Nollen, P. M. & Pyne, J. L. (1979). Observations on spermatogenesis and inseminative behavior of Megalodiscus temperatus in frogs. Journal of Parasitology 65, 35–7.CrossRefGoogle ScholarPubMed
Nollen, P. M., Pyne, J. L., Moseley, C. & Bunker, D. (1975). Inseminatory behavior of Philophthalmus megalurus and Philophthalmus hegeneri in concurrent infections of chicks. International Journal for Parasitology 5, 99–101.CrossRefGoogle ScholarPubMed
Paling, J. E. (1966). The functional morphology of the genitalia of the spermatophore-producing monogenean parasite Diplectanum aequans (Wagener) Diesing, with a note on the copulationof the parasite. Parasitology 56, 367–83.CrossRefGoogle ScholarPubMed
Palombi, A. (1982). La copulazione nei trematodi richerchi sul significato fiscologico del canale di Laurer. Archivio Zoologico Italiano, Torino 17, 123–51.Google Scholar
Perkins, K. W. (1956). Studies on the morphology and biology of Acetodextra amiuri (Stafford) (Trematoda: Heterophyidae). American Midland Naturalist 55, 139–61.CrossRefGoogle Scholar
Pitchford, P. J. (1961). Observations on a possible hybrid between two schistosomes. Schistosoma haematobium and Schistosoma matthei. Transactions of the Royal Society of Tropical Medicine and Hygiene 55, 44–51.CrossRefGoogle Scholar
Popiel, I. & Erasmus, D. A. (1981). Schistosoma mansoni: changes in the rate of tyrosine uptake by unisexual females after stimulation by males male extract. Journal of Helminthology 55, 33–7.CrossRefGoogle Scholar
Price, E. W. (1953). The fluke situation in American ruminants. Journal of Parasitology 39, 119–34.CrossRefGoogle ScholarPubMed
Rankin, J. S. (1938). Studies on the trematode genus Brachycoelium Duj. I. Variation in species characteristics with reference to the validity of the described species. Transactions of the American Microscopical Society 57, 358–75.CrossRefGoogle Scholar
Rausch, R. (1947). Some observations on the host relationship in Microphallus opacus (Ward, 1894) (Trematoda: Microphallidae). Transactions of the American Microscopical Society 40, 59–63.CrossRefGoogle Scholar
Rees, G. (1939). Studies on the germ cell cycle of the digenetic trematode. Parorchis acanthus Nicoll. Part I. Anatomy of the genitalia and gametogenesis. Parasitology 31, 417–33.CrossRefGoogle Scholar
Rogers, W. A. & Ulmer, M. J. (1962). Effects of continued selfing on Hymenolepis nana (Cestoda). Proceedings of the Iowa Academy of Sciences 69, 557–71.Google Scholar
Rybicka, A. (1966). Embryogenesis in cestodes. In Advances in Parasitology. vol. 4, (ed. Dawes, B.) New York: Academic Press.Google Scholar
Severinghaus, A. E. (1928). Sex studies on Schistosoma japonicum. Quarterly Journal of Microscopical Science 71, 635–702.Google Scholar
Shaw, J. R. (1977). Schistosoma mansoni: pairing in vitro and development of females from single sex infections. Experimental Parasitology 41, 54–65.CrossRefGoogle ScholarPubMed
Shaw, J. R., Marshall, I. & Erasmus, D. A. (1977). Schistosoma mansoni: in vitro stimulation of vitelline cell development by extracts of male worms. Experimental Parasitology 42, 14–20.CrossRefGoogle ScholarPubMed
Short, R. B. (1948). Intergeneric crosses among schistosomes. Journal of Parasitology 34, 30.Google Scholar
Smyth, J. D. (1954). Studies on tapeworm physiology. VII. Fertilizations of Schistocephalus solidus in vitro. Experimental Parasitology 3, 64–71.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1962). Introduction to Animal Parasitology. Springfield, Illinois: Charles C. Thomas.Google Scholar
Smyth, J. D. & Smyth, M. M. (1969). Self-insemination in Echinococcus granidosus in vivo. Journal of Helminthology 43, 383–8.CrossRefGoogle ScholarPubMed
Sogandares-Bernal, F. (1959). Digenetic trematodes of marine fishes from the Gulf of Panama and Bimini, British West Indies. Tulane Studies in Zoology 7. 69–117.Google Scholar
Sogandares-Bernal, F. (1965). Parasites from Louisiana crayfishes. Tulane Studies in Zoology 12, 79–85.Google Scholar
Sogandares-Bernal, F. (1966). Studies on American paragonimiasis IV. Observations on the pairing of adult worms in laboratory infections of domestic cats. Journal of Parasitology 52, 701–3.CrossRefGoogle ScholarPubMed
Sogandakes-Bernal, F. & Hutton, R. F. (1958). Studies on helminth parasites of marine fishes of Tampa, Boca Ciega Bays, and the Gulf of Mexico. Quarterly Journal of the Florida Academy of Sciences 21, 259–73.Google Scholar
Standen, O. D. (1953). The relationship of sex of Schistosoma mansoni to migration within the hepatic portal system of experimentally infected mice. Annals of Tropical Medicine and Parasitology 47, 139–45.CrossRefGoogle ScholarPubMed
Stunkard, H. W. (1957). Intraspecific variation in parasitic flatworms. Systematic Zoology 6, 7–18.CrossRefGoogle Scholar
Taylor, M. G. (1970). Hybridization experiments on five species of African schistosomes. Journal of Helminthology 44, 253–314.CrossRefGoogle ScholarPubMed
Van Der Woude, A. (1954). Germ cell cycle of Megalodiscus temperatus (Stafford, 1905) (Paramphistomidae: Trematoda). American Midland Naturalist 51, 172–202.CrossRefGoogle Scholar
Vogel, H. (1942). Ueber den Einfluss des Geschlechtspartners auf Wachstum und Entwicklung bei Bilharzia mansoni und bei Kreuzpaarungen zwischen verschiedenen Bilharzia-Arten. Zentralblatt für Bakteriologie 148, 78–92.Google Scholar
Wilde, J. (1937). Dactylogyrus macracanthus Wegener als Krankheitserreger auf den Kiemen der Schleie (Tinea tinea L.). Zeitschrift für Parasitenkunde 2, 201–36.Google Scholar
Wilmott, S. (1950). Gametogenesis and early development in Gigantocotyle bathocotyle (Fischoeder, 1901) Nasmark 1937 I. Journal of Helminthology 24, 1–14.CrossRefGoogle Scholar
Willey, C. H. & Goodman, G. C. (1941). Gametogenesis, fertilization and cleavage in the trematode Zygocotyle lunata (Paramphistomidae). Journal of Parasitology 37, 283.CrossRefGoogle Scholar
Willey, C. H. & Koulish, S. (1947). Gametogenesis in Gorgoderina attenuata. Anatomical Record 99, 640–1.Google ScholarPubMed
Williams, H. H. & Mcvicar, A. (1968). Sperm transfer in tetraphyllidea (Platyhelminthes: Cestoda). Nytt Magasin for Zoologi 16, 61–71.Google Scholar
Woodhead, A. E. (1931). The germ cell cycle in the trematode family Bucephalidae. Transactions of the American Microsopical Society 50, 169–88.CrossRefGoogle Scholar
Wright, C. A. & Southgate, V. R. (1976). Hybridization of schistosomes and some of its implications. In Genetic Aspects of Host–Parasite Relationships, (ed. Taylor, A. E. R. and Muller, R.). London: Blackwell.Google Scholar
Wright, C. A., Southgate, V. R., Van Wijk, H. B. & Moore, P. J. (1974). Hybrids between Schistosoma haematobium and Schistosoma intercalatum in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 413–14.CrossRefGoogle ScholarPubMed
Yosufzai, H. K. (1952). Cytological studies on the spermatogenesis of Fasciola hepatica L. La Cellulea 55, 5–19.Google ScholarPubMed