Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-12-01T07:16:58.529Z Has data issue: false hasContentIssue false
  • English
  • Français

Parthenogenesis and asexual multiplication among parasitic platyhelminths

Published online by Cambridge University Press:  06 April 2009

P. J. Whitfield  and
N. A. Evans
P. J. Whitfield
Affiliation:
Zoology Department, King's College, Strand, London WC2
N. A. Evans
Affiliation:
Zoology Department, King's College, Strand, London WC2
Get access Rights & Permissions [Opens in a new window]

Summary

Among flatworms with parasitic and commensal modes of existence, parthenogenesis and asexual multiplication appear to be largely confined to the Digenea and Cestoda, the only parasitic platyhelminths that routinely utilize indirect life-cycles. Parthenogenesis is apparently restricted to a minority of adult digeneans and cestodes inhabiting their final hosts, and a survey is made of the particular modes of parthenogenesis (i.e. apomictic, automictic and generative) which are employed by such adults. Asexual (amictic) multiplication, in the form of fissioning, is demonstrated by young adults of the cyclophyllidean cestode, Mesoces-toides corti, but is otherwise not exhibited by adult cestodes or digeneans, other than in the perplexing phenomenon of proglottid formation in polyzoic tapeworms. Secondary multiplication is of ubiquitous occurrence in digenean life-cycles in the form of the proliferation which takes place within sporocysts and rediae (germinal sacs) located in the first intermediate host. The controversy concerning the nature of this multiplication is reconsidered in the context of recent findings which have centred on cellular aspects. On the basis of present evidence germinal sac multiplication should be regarded as an asexual rather than a parthen-ogenetic process. The cestode asexual multiplication which occurs in intermediate hosts is a function of the metacestode stage of development. Metacestode proliferation is only known from about 20 species and 6 families of polyzoic cestodes with approximately half the described instances occurring in the family Taeniidae. The organization of these proliferative metacestodes, findings concerning their totipotent stem cells and the ontogeny of buds and new scolices are all reviewed. Finally, the capacity for population expansion of multiplicative larval digeneans and metacestodes are compared, while the ecological roles and the genetical consequences of both parthenogenesis and amictic multiplication in the two taxa are also examined.

Type
Research Article
Information
Parasitology , Volume 86 , Issue 4 , April 1983 , pp. 121 - 160
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

Ali-khan, Z. & Siboo, R. (1980). Pathogenesis and host response in subcutaneous alveolar hydatidosis. I. Histogenesis of alveolar cyst and a qualitative analysis of the inflammatory infiltrates. Zeitschrift für Parasilenkunde 62, 241–54.CrossRefGoogle Scholar
Anderson, R. M., Whitfield, P. J. & Mills, C. A. (1977). An experimental study of the population dynamics of an ectoparasitic digenean Transversotrema patialense. Journal of Animal Ecology 46, 555–80.CrossRefGoogle Scholar
Armstrong, J. C. (1965). Mating behaviour and development of schistosomes in the mouse. Journal of Parasitology 51, 605–16.CrossRefGoogle ScholarPubMed
Beaver, P. C. (1937). Experiments on regeneration in the trematode Echinostoma revolutum. Journal of Parasitology 23, 423–4.CrossRefGoogle Scholar
Bednarz, S. (1962). The developmental cycle of germ cells in Fasciola hepatica L. 1758 (Trematodes, Digenea). Zoologica Poloniae 12, 439–66.Google Scholar
Bell, G. (1982). The Masterpiece of Nature: the Evolution and Genetics of Sexuality. London and Canberra: Croom Helm.Google Scholar
Bennett, H. J. (1936). The life history of Cotylophoron cotylophorum, a trematode of ruminants. Illinois Biological Monographs 14, 1–119.Google Scholar
Bentley, A. G. M. (1973). Studies on the development and regenerative capabilities of the tegument of parasitic platyhelminths. Ph.D. dissertation, Tulane University.Google Scholar
Bilqees, F. M. (1968). Observations on budding gradient in Taenia crassiceps (Zeder, 1800) Rud. 1810. Rivista di Parassitologia 29, 261–4.Google Scholar
Bilqees, F. M. (1970). Histological study of external budding in Taenia crassiceps. Australian Journal of Zoology 18, 1–7.CrossRefGoogle Scholar
Bolla, R. I. & Roberts, L. S. (1971). Developmental physiology of cestodes. IX. Cytological characteristics of the germinative region of Hymenolepis diminuta. Journal of Parasitology 57, 267–77.CrossRefGoogle ScholarPubMed
Boray, J. C. (1969). Experimental fascioliasis in Australia. Advances in Parasitology 7, 95–210.CrossRefGoogle ScholarPubMed
Bortoletti, G. & Ferretti, G. (1971). Observations on the ultrastructure of the tegument in the larval forms of Hydatigera (=Taenia) taeniaeformis and considerations on the development of the cyclophyllidean cestode larvae. Rivista di Parassitologia 32, 249–71.Google Scholar
Bortoletti, G. & Ferretti, G. (1973). Investigation on the larval forms of Echinococcus granulosus with electron microscope. Rivista di Parassitologia 34, 89–110.Google Scholar
Bortoletti, G. & Ferretti, G. (1978). Ultrastructural aspects of fertile and sterile cysts of Echinococcus granulosus developed in hosts of different species. International Journal for Parasitology 8, 421–32.CrossRefGoogle ScholarPubMed
Bronsted, H. V. (1955). Planarian regeneration. Biological Reviews 30, 65–126.CrossRefGoogle Scholar
Brooks, F. G. (1930). Studies on the germ cycles of trematodes. American Journal of Hygiene 12, 299–340.Google Scholar
Brown, D. S. (1980). Freshwater Snails of Africa and their Medical Importance. London: Taylor and Francis.Google Scholar
Brumpt, E. (1936). Précis de Parasitologic, 5th Ed., pp. 1–1082. Paris: Masson and Cie.Google Scholar
Cable, R. M. (1934). Studies on the germinal cycle of Cryptocotyle lingua. II. Germinal development in the larval stages. Quarterly Journal of Microscopical Science 76, 573–614.Google Scholar
Cable, R. M. (1974). Phylogeny and taxonomy of trematodes with reference to marine species. In Symbiosis in the Sea, (ed. Vernberg, W. B.), pp. 173–93. Columbia: University of South Carolina Press.Google Scholar
Cable, R. M. (1982). Phylogeny and taxonomy of malacobothrean flukes. In Parasites – Their World and Ours (ed. Mettrick, D. F. and Desser, S. S.), pp. 194–7. Elsevier Biomedical Press.Google Scholar
Campbell, R. A. (1973). Studies on the biology of the life cycle of Cotylurus flabelliformis (Trematoda: Strigeidae). Transactions of the American Microscopical Society 92, 629–40.CrossRefGoogle ScholarPubMed
Cannon, L. R. G. (1971). The life cycle of Bunodera sacculata and B. luciopercae in Algonquin Park, Ontario. Canadian Journal of Zoology 49, 1417–29.CrossRefGoogle Scholar
Cary, L. R. (1909). The life history of Diplodiscus temperatus Stafford, with special reference to the development of the parthenogenetic eggs. Zoologische Jahrbucher 28, 595–659.Google Scholar
Clark, W. C. (1974). Interpretation of life history pattern in the Digenea. International Journal for Parasitology 4, 115–23.CrossRefGoogle ScholarPubMed
Cohen, J. (1977). Reproduction. London: Butterworths.Google Scholar
Cort, W. W., Ameel, D. J. & Van Der Woude, A. (1954). Germinal development in the sporocysts and rediae of the digenetic trematodes. Experimental Parasitology 3, 185–225.CrossRefGoogle ScholarPubMed
Craig, L. H. (1975). Himasthla quissetensis and Lepocreadium setiferoides: Emergence patterns from their molluscan host, Nassarius obsoletus. Experimental Parasitology 38, 56–63.CrossRefGoogle ScholarPubMed
De Rycke, P. H. & Pennoit-De Cooman, E. (1978). Serial passages of larval Echinococcus granulosus from equine origin in mice. I. Infection with protoscolices. Zeitschrift für Parasitenkunde 155, 229–34.Google Scholar
Dinnik, J. A. & Dinnik, N. N. (1964). The influence of temperature on the succession of redial and cercarial generations of Fasciola gigantica in a snail host. Parasitology 54, 59–65.CrossRefGoogle Scholar
Dollfus, R.-P. (1964). Sur le cycle évolutif d'un cestode Diphyllide. Annates de Parasitologie humaine et comparée 39, 235–41.CrossRefGoogle Scholar
Dönoes, J. (1971). The potential number of redial generations in echinostomatids (Trematoda). International Journal for Parasitology 1, 51–9.Google Scholar
Dronen, N. O. (1978). Host–parasite population dynamics of Haematoloechus coloradensis. Cort, 1915 (Digenea: Plagiorchiidae). The American Midland Naturalist 99, 330–49.CrossRefGoogle Scholar
Eckert, J., Von Brand, T. & Voce, M. (1969). Asexual multiplication of Mesocestoides corti (Cestoda) in the intestine of dogs and skunks. Journal of Parasitology 55, 241–9.Google Scholar
Edson, K. M., Vinson, S. B., Stoltz, D. B. & Summers, M. D. (1981). Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host. Science 211, 582–3.CrossRefGoogle Scholar
Edwards, S. & Mueller, J. (1978). On the apparent absence of C-virus-like particles in the Caryophyllaeidae. Journal of Parasitology 64, 877.CrossRefGoogle Scholar
Espin, P. (1982). Transversotrema patialense: the role of cross-insemination in successful reproduction. Parasitology 85, 5.Google Scholar
Fischer, H. & Freeman, R. S. (1969). Penetration of parenteral plerocercoids of Proteocephalus ambloplitis (Leidy) into the gut of smallmouth bass. Journal of Parasitology 55, 766–74.Google Scholar
Freeman, R. S. (1956). Life history studies on Taenia mustelae Gmelin, 1790 and the taxonomy of certain taenioid cestodes from mustelidae. Canadian Journal of Zoology 34, 219–42.CrossRefGoogle Scholar
Freeman, R. S. (1962). Studies on the biology of Taenia crassiceps (Zeder, 1800). Rudolphi, 1810 (Cestoda). Canadian Journal of Zoology 40, 969–90.CrossRefGoogle Scholar
Freeman, R. S. (1970). Terminology of cestode development. Journal of Parasitology 56, 106–7.Google Scholar
Freeman, R. S. (1973). Ontogeny of cestodes and its bearing on their phylogeny and systematica. Advances in Parasitology 11, 481–557.Google Scholar
Fried, B. & Penner, L. R. (1964). Healing of wounds following partial or complete amputation of body parts in a trematode, Philophthalmus hegeneri. Journal of Parasitology 50, 266.Google Scholar
Fujino, T. & Ishii, Y. (1982). Ultrastructural studies on spermatogenesis in a parthenogenetic type of Paragonimus westermani (Kerbert 1878) proposed as P. pulmonalis (Baelz 1880). Journal of Parasitology 68, 433–41.CrossRefGoogle Scholar
Gerritsen, J. (1980). Sex and parthenogenesis in sparse populations. The American Naturalist 115, 718–42.Google Scholar
Gilman, R. H., Mondal, G., Maksud, M., Alam, E., Rutherford, E., Gilman, J. B. & Khan, M. U. (1982). Endemic focus of Fasciolopsis buski infection in Bangladesh. American Journal of Tropical Medicine and Hygiene 31, 796–802.CrossRefGoogle ScholarPubMed
Ginetsinskaya, T. A. (1965). The nature of trematode life cycles (In Russian, English summary). Vestnik Leningradskogo gosudarstrennogo Universiteta Ser. Biol. 20, 5–13.Google Scholar
Giovannola, A. (1936). Inversion in the periodicity of emission of cercariae from their snail hosts by reversal of light and darkness. Journal of Parasitology 22, 292–5.CrossRefGoogle Scholar
Grey, A. J. & Mackiewicz, J. S. (1980). Chromosomes of caryophyllidean cestodes: diploidy, triploidy and parthenogenesis in Glaridacris catostomi. International Journal for Parasitology 10, 397–107.Google Scholar
Guilford, H. G. (1958). Observations on the development of the miracidium and the germ cell cycle in Heronimus chelydrae MacCallum (Trematoda). Journal of Parasitology 44, 64–74.Google Scholar
Gustafsson, M. K. S. (1977). Aspects of the cytology and histogenesis in cestodes with special reference to the genus Diphyllobothrium. Ph.D. thesis, Abo Akademi, Abo, Finland.Google Scholar
Haight, M., Davidson, D. & Pasternak, J. (1977 a). Relationship between nuclear morphology and the phases of the cell cycle during cercarial development of the digenetic trematode Trichobilharzia ocellata. Journal of Parasitology 63, 267–73.Google Scholar
Haight, M., Davidson, D. & Pasternak, J. (1977 b). Cell cycle analysis in developing cercariae of Trichobilharzia ocellata (Trematoda: Schistosomatidae). Journal of Parasitology 63, 274–81.CrossRefGoogle ScholarPubMed
Harris, K. R. & Cheng, T. C. (1972). Presumptive neurosecretion in Leucochloridiomorpha constantiae (Trematoda) and its possible role in governing maturation. International Journal for Parasitology 2, 361–7.Google Scholar
Hart, J. L. (1968). Regeneration of tetrathyridia of Mesocestoides (Cestoda: Cyclophyllidea) in vivo and in vitro. Journal of Parasitology 54, 950–6.CrossRefGoogle ScholarPubMed
Haswell, W. A. & Hill, J. P. (1893). On Polycercus: a proliferating cystic parasite of the earthworm. Proceedings of the Linnean Society of New South Wales 8, 365–76.Google Scholar
Heyneman, D. (1960). On the origin of complex life-cycles in the digenetic flukes, pp. 133–152. In Libro Homenaje al Dr. Eduardo Caballero y Caballero. Mexico: Secretaria de Educacion publica.Google Scholar
Hodasi, J. K. M. (1972). The output of cercariae of Fasciola hepatica by Lymnaea truncatula and the distribution of metacercariae on grass. Parasitology 64, 53–60.Google Scholar
Insler, G. D. & Roberts, L. S. (1980 a). Developmental physiology of cestodes. XV. A system for testing possible crowding factors in vitro. Journal of Experimental Zoology 211, 45–54.CrossRefGoogle Scholar
Insler, G. D. & Roberts, L. S. (1980 b). Developmental physiology of cestodes. XVI. Effects of certain excretory products on incorporation of 3H-thymidine into DNA of Hymenolepis diminuta. Journal of Experimental Zoology 211, 55–61.CrossRefGoogle 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 Muller) (Gymnophallidae). Parasitology 57, 607–25.CrossRefGoogle Scholar
James, B. L., Sannia, A. & Bowers, E. A. (1976). Parasites of birds and shellfish. In Bury Inlet Symposium. Swansea: University College of Swansea.Google Scholar
Jennings, J. B. (1971). Parasitism and commensalism in the Turbellaria. Advances in Parasitology 91, 1–32.Google Scholar
Jones, M. F. & Alicata, J. E. (1935). Development and morphology of the cestode, Hymenolepis cantaniana, in coleopteran and avian hosts. Journal of the Washington Academy of Science 25, 237–47.Google Scholar
Jordan, P. & Wbbbb, G. (1969). Human Schistosomiasis. London: Heineman.Google Scholar
Jourdane, J. & Theron, A. (1980). Schistosoma mansoni: Cloning by microsurgical transplantation of sporocysts. Experimental Parasitology 50, 349–57.Google Scholar
Jourdane, J., Theron, A. & Combes, C. (1980). Demonstration of several sporocysts generations as a normal pattern of reproduction of Schistosoma mansoni. Acta Tropica 37, 177–82.Google ScholarPubMed
Joyeux, C. H. & Baer, J. G. (1936). Cestodes. In Faune de France, vol. 30. Paris: Paul Lechevalier et fils.Google Scholar
Kendall, S. B. (1965). Relationships between species of Fasciola and their molluscan hosts. Advances in Parasitology 3, 59–98.CrossRefGoogle Scholar
Khalil, G. M. & Cable, R. M. (1968). Germinal development in Philophthalmus megalurus (Cort, 1911) (Trematoda: Digenea). Zeitschrift für Parasitenkunde 31, 211–31.CrossRefGoogle Scholar
Kisielewska, K. (1960). The life cycle of the tapeworm Pseudodiorchis prolifer (Villot, 1890) comb nova (Pseudodiorchis multispinosa, Zarnowski, 1955). Acta parasitologic polonica 8, 197–204.Google Scholar
Kumazawa, H. & Suzuki, N. (1983). Kinetics of proglottid formation, maturation and shedding during development of Hymenolepis nana. Parasitology 86, 275–89.Google Scholar
Kunz, R. E., Myers, B. J. & Katzberg, A. A. (1970). Sparganosis and ‘proliferative’ spargana in vervets (Cercopithecus aethiops) and baboons (Papio sp.) from East Africa. Journal of Parasitology 56, 196–7.Google Scholar
Lascano, E. F., Coltorti, E. A. & Varela-Diaz, V. M. (1975). Fine structure of the germinal membrane of Echinococcus granulosus cysts. Journal of Parasitology 61, 853–60.CrossRefGoogle ScholarPubMed
Lender, T. (1974). The role of neurosecretion in freshwater planarians. In Biology of the Turbellaria (ed. Rizer, N. W. and Morse, M. P.), pp. 460–75. New York: McGraw-Hill.Google Scholar
Leuckart, R. (1886). The Parasites of Man. Translated by Hoyle, W. E.. 771 pp. Edinburgh: Y. J. Pentland.Google Scholar
Llewellyn, J. (1965). The evolution of parasitic platyhelminths. Symposium of the British Society for Parasitology 3, 47–78.Google Scholar
Loehr, K. A. & Mead, R. W. (1980). Changes in embryonic cell frequencies in the germinative and immature regions of Hymenolepis citelli during development. Journal of Parasitology 66, 792–6.CrossRefGoogle ScholarPubMed
Mackiewicz, J. S. (1981). Caryophyllidea (Cestoidea): Evolution and classification. Advances in Parasitology 19, 139–206.Google Scholar
Manning, G. S. & Ratanarat, C. (1970). Fasciolopsis buslci (Lankester, 1857) in Thailand. American Journal of Tropical Medicine and Hygiene 19, 613–19.Google Scholar
McClelland, G. & Bourns, T. K. R. (1969). Effects of Trichobilharzia ocellata on growth, reproduction and survival of Lymnaea stagnalis. Experimental Parasitology 24, 137–46.Google Scholar
Mead, R. W. (1982). Changes in germinative cell frequencies in the germinative region of Hymenolepis diminuta during development. Journal of Parasitology 68, 95–9.Google Scholar
Meyerhof, E. & Rothschild, M. (1940). A prolific trematode. Nature, London 146, 367–8.CrossRefGoogle Scholar
Miyazaki, I. (1978). Two types of the lung fluke which has been called Paragonimus westermani (Kerbert, 1878). Medical Bulletin of Fukuoka University 5, 251–63.Google Scholar
Moore, J. (1981). Asexual reproduction and environmental predictability in cestodes (Cyclophyllidea: Taeniidae). Evolution 35, 723–41.Google Scholar
Morseth, D. J. (1967). Fine structure of the hydatid cyst and protoscolex of Echinococcus granulosus. Journal of Parasitology 53, 312–25.Google Scholar
Mueller, J. F., Hart, E. P. & Walsh, W. P. (1963). Human sparganosis in the United States. Journal of Parasitology 49, 294–6.Google Scholar
Mueller, J. F. & Strano, A. J. (1974 a). Sparganum proliferum, a sparganum infected with a virus? Journal of Parasitology 60, 15–19.Google Scholar
Mueller, J. F. & Strano, A. J. (1974 b). The ubiquity of type-C viruses in spargana of Spirometra spp. Journal of Parasitology 60, 398.Google Scholar
Muller, R. (1975). Worms and Disease. A Manual of Medical Helminthology. London: Heineman.Google Scholar
Nollen, P. M. (1983). Patterns of sexual reproduction among parasitic platyhelminths. Symposia of the British Society for Parasitology 20, 99–120.Google Scholar
Novak, M. (1972). Quantitative studies on the growth and multiplication of tetrathyridia of Mesocestoides corti Hoeppli, 1925 (Cestoda: Cyclophyllidea) in rodents. Canadian Journal of Zoology 50, 1189–96.CrossRefGoogle ScholarPubMed
Novak, M. (1974). Acceleration of the growth of tetrathyridial populations of Mesocestoides corti (Cestoda: Cyclophyllidea) by splenectomy. International Journal for Parasitology 4, 165–8.Google Scholar
Novak, M. (1975 a). Gonadectomy, sex hormones and the growth of populations of Mesocestoides tetrathyridia in mice. International Journal for Parasitology 5, 269–74.Google Scholar
Novak, M. (1975 b). Cortisone and the growth of populations of Mesocestoides tetrathyridia in mice. International Journal for Parasitology 5, 517–20.Google Scholar
Novak, M. (1979). Environmental temperature and the growth of Mesocestoides corti populations in mice. International Journal for Parasitology 9, 429–33.Google Scholar
Ogren, R. E. (1968). The basic cellular pattern for undifferentiated oncospheres of Hymenolepis diminuta. Transactions of the American Microscopical Society 87, 448–63.Google Scholar
Opuni, E. K. (1970). Asexual multiplication in Cysticercus pisiformis. Journal of Helminthology 44, 321–2.Google Scholar
Parshad, V. R. & Crompton, D. W. T. (1981). Aspects of acanthocephalan reproduction. Advances in Parasitology 19, 73–138.Google Scholar
Patterson, J. T. (1927). Polyembryony in animals. Quarterly Reviews in Biology 2, 399–462.Google Scholar
Pearson, J. C. (1972). A phylogeny of life cycle patterns of the Digenea. Advances in Parasitology 10, 153–89.Google Scholar
Pennoit-de cooman, E. & De Rycke, P. H. (1970). Experimental secondary echinococcosis of Echinococcus granulosus. I. Development in different strains of mice. Zeitschrift für Parasitenkunde 34, 362–70.CrossRefGoogle ScholarPubMed
Pieper, M. B. (1953). The life history and germ cell cycle of Spirorchis artericola (Ward, 1921). Journal of Parasitology 39, 310–25.CrossRefGoogle Scholar
Premvati, (1955). Cercaria multiplicata n.sp. from the snail Melanoides tuberculatus (Muller). Journal of the Zoological Society of India 7, 13–23.Google Scholar
Price, P. W. (1977). General concepts on the evolutionary biology of parasites. Evolution 31, 405–20.CrossRefGoogle ScholarPubMed
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google Scholar
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 31, 417–33.Google Scholar
Rees, G. (1969). Cestodes from Bermuda fishes and an account of Acompsocephalum tortum (Linton, 1905) gen. nov. from the lizard fish Synodus intermedius (Agassiz). Parasitology 59, 519–48.Google Scholar
Roberts, L. S. (1980). Development of Hymenolepis diminuta in its definitive host. In Biology of the Rat Tapeworm, Hymenolepis diminuta (ed. Arai, H. P.), pp. 357–423. New York: Academic Press.Google Scholar
Roberts, L. S. & Insler, G. D. (1982). Developmental physiology of cestodes. XVII. Some biological properties of putative ‘crowding factors’ in Hymenolepis diminuta. Journal of Parasitology 68, 263–9.CrossRefGoogle ScholarPubMed
Rossbach, E. (1906). Beiträge zur Anatomie und Entwicklungsgeschichte der Redien. Zeitschrift für Wissenschaftliche Zoologie 84, 361–445.Google Scholar
Sakaguchi, Y. (1980). Karyotype and gametogenesis of the common liver fluke, Fasciola sp. Japanese Journal of Parasitology 29, 507–13.Google Scholar
Sakaguchi, Y. & Tada, I. (1980). Karyotypic studies of lung flukes, Paragonimus iloktsuenensis, P. sadoensis and P. westermani. Japanese Journal of Parasitology 29, 251–6.Google Scholar
Sakamoto, T. & Sugimura, M. (1970). Studies on echinococcosis. XXIII. Electron microscopical observations on histogenesis of larval Echinococcus multilocularis. Japanese Journal of Veterinary Research 18, 131–44.Google Scholar
Sasada, K. (1978). Studies on the chromosomes of parasitic helminths (II). Triploidy and cytological mechanism of parthenogenesis in Diphyllobothrium erinacei (Cestoda: Diphyllo-bothriidae). Japanese Journal of Parasitology 27, 547–60.Google Scholar
Schmidt, J. M. & Todd, K. S. (1978). Life cycle of Mesocestoides corti in the dog (Canis familiaris). American Journal of Veterinary Research 39, 1490–3.Google Scholar
Scott, J. S. (1965). The development and morphology of Polycercus lumbrici (Cestoda: Cyclophyllidea). Parasitology 55, 127–43.CrossRefGoogle Scholar
Senft, A. W. & Weller, T. H. (1956). Growth and regeneration of Schistosoma mansoni in vitro. Proceedings of the Society for Experimental Biology 93, 16–19.Google Scholar
Shimazu, T. (1981). Experimental completion of the life-cycle of the lung fluke, Paragonimus westermani, in the laboratory. Japanese Journal of Parasitology 30, 173–7.Google Scholar
Short, R. B. (1952 a). Sex studies on Schistosomatium douthitti (Cort 1914), Price, 1931. (Trematoda: Schistosomatidae). American Midland Naturalist 47, 1–54.Google Scholar
Short, R. B. (1952 b). Uniparental miracidia of Schistosomatium douthitti and their progeny (Trematoda: Schistosomatidae). American Midland Naturalist 48, 55–68.Google Scholar
Short, R. B. & Menzbl, M. Y. (1959). Chromosomes in parthenogenetic miracidia and embryonic cercariae of Schistosomatium douthitti. Experimental Parasitology 8, 249–64.Google Scholar
Siebert, A. E., Good, A. H. & Simmons, J. G. (1978). Kinetics of primary and secondary infections with Taenia crassiceps metacestodes (Zeder, 1800) Rudolphi, 1810 (Cestoda: Cyclophyllidea). International Journal for Parasitology 8, 39–43.CrossRefGoogle ScholarPubMed
Sillman, E. I. (1962). The life history of Azygia longa (Leidy 1851) (Trematoda: Digenea) and notes on A. acuminata Goldberger 1911. Transactions of the American Microscopical Society 81, 43–65.Google Scholar
Slais, J. (1973). Functional morphology of cestode larvae. Advances in Parasitology 11, 395–480.Google Scholar
Sluiters, J. F., Brussaard-Wust, & Meuleman, E. A. (1980). The relationship between miracidial dose, production of cercariae and reproductive activity of the host in the combination Trichobilharzia ocellata and Lymnaea stagnalis. Zeitschrift filr Parasitenkunde 63, 13–26.Google Scholar
Smyth, J. D. (1976). Introduction to Animal Parasitology, 2nd Ed. London: Hodder and Stoughton.Google Scholar
Smyth, J. D., Miller, H. J. & Howkins, A. B. (1967). FÜRther analysis of the factors controlling strobilization, differentiation and maturation of Echinococcus granulosus in vitro. Experimental Parasitology 21, 31–41.CrossRefGoogle ScholarPubMed
Specht, D. & Voge, M. (1965). Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. Journal of Parasitology 51, 268–72.Google Scholar
Specian, R. D. (1981). Hymenolepis diminuta: paraldehyde fuchsin staining of the rostellar glands following destrobilization and reimplantation. Journal of Parasitology 67, 278–9.Google Scholar
Stunkard, H. W. (1967). Platyhelminth parasites of invertebrates. Journal of Parasitology 53, 673–82.Google Scholar
Suomalainen, E. (1950). Parthenogenesis in animals. Advances in Genetics 3, 193–253.Google Scholar
Suomalainen, E. (1962). Significance of parthenogenesis in the evolution of insects. Annual Review of Entomology 7, 349–66.Google Scholar
Taylor, M. G., Amin, M. B. A. & Nelson, G. S. (1969). ‘Parthenogenesis’ in Schistosoma mattheei. Journal of Helminthology 43, 197–206.Google Scholar
Tennant, D. H. (1906). A study on the life history of Bucephalus haimeanus; a parasite of the oyster. Quarterly Journal of microscopical Science 49, 635–93.Google Scholar
Terasaki, K. (1980). Comparative studies on the karyotypes of Paragonimus westermani (s.str.) and P. pulmonalis. Japanese Journal of Parasitology 29, 239–43.Google Scholar
Theron, A. & Jourdane, J. (1979). Sequence de Reconversion des Sporocystes de Schistosoma mansoni. Producteurs de Cercaires, en vue de la Production de Nouvelles Generations de Sporocystes. Zeitschrift filr Parasitenkunde 61, 63–71.Google Scholar
Thomas, A. P. (1883). The life history of the liver fluke (Fasciola hepatica). Quaterly Journal of Microscopical Science 23, 99–133.Google Scholar
Thompson, R. C. A. (1976). The development of broodcapsules and protoscolices in secondary hydatid cysts of Echinococcus granulosus: a histological study. Zeitschrift für Parasitenkunde 51, 31–6.Google Scholar
Tinsley, R. C. (1983). Ovoviparity among parasitic platyhelminths. Symposia of the British Society for Parasitology 20, 161–96.Google Scholar
Tomlinson, J. (1966). The advantages of hermaphroditism and parthenogenesis. Journal of Theoretical Biology 11, 54–8.Google Scholar
Voge, M. (1963). Observations on the habitats of platyhelminths. In The Lower Metazoa, (ed. Dougherty, E. C.) pp. 455–72. Berkeley and Los Angeles: University of California Press.Google Scholar
Vogel, H. (1942) Über die Nachkommenschaft aus Kreuzparungen zwischen Bilharzia mansoni und B. japonica. Zentralblatt für Bakleriologie und Parasitenkunde, Abt. 1. 149, 319–33.Google Scholar
Wagenbach, G. E. & Alldredge, A. L. (1974). Effect of light on the emergence pattern of Plagiorchis micracanthos cercariae from Stagnicola exilis. Journal of Parasitology 60, 782–5.Google Scholar
Webb, R. A. (1977). Evidence for neurosecretory cells in the cestode Hymenolepis microstoma. Canadian Journal of Zoology 55, 1726–33.Google Scholar
Webbe, G. & James, E. (1972). Host-parasite relationships of Bulinus globosus and B. truncatus with strains of Schistosoma haematobium. Journal of Helminthology 46, 185–99.Google Scholar
White, M. J. D. (1970). Heterozygosity and genetic polymorphism in parthenogenetie animals. In Essays in Evolution and Genetics in Honor of Theodosius Dobzhansky (ed. Hecht, M. K. and Steere, W. C.), pp. 237–62. New York: Appleton-Century-Crofts.Google Scholar
Wikgren, B.-J. P. & Gustafsson, M. K. S. (1967). Duration of the cell cycle of germinative cells in plerocercoids ot Diphyllobothrimn dendriticum. Zeitschrift für Parasitenkunde 29, 275–81.Google Scholar
Wikgren, B.-J. P., Knuts, G. M. & Gustafsson, M. K. S. (1970). Circadian rhythm of mitotic activity in the adult gull tapeworm Diphyllobothrium dendriticum. Zeitschrift für Parasitenkunde 34, 242–56.Google Scholar
Williams, G. C. (1975). Sex and Evolution. Princeton: Princeton University Press.Google Scholar
Wilson, R. A. & Denison, J. (1980). The parasitic castration and gigantism of Lymnaea truncatula infected with the larval stages of Fasciola hepatica. Zeitschrift für Parasitenkunde 61, 109–19.Google Scholar
Wilson, R. A., Smith, G. & Thomas, M. R. (1982). Fascioliasis. In Population Dynamics of Infectious Diseases: Theory and Applications (ed. Anderson, R. M.), pp. 262–319. London and New York: Chapman and Hall.Google Scholar
Woodhead, A. E. (1931). The germ cell cycle in the trematode family Bucephalidae. Transactions of the American Microscopical Society 50, 169–87.Google Scholar
Woodhead, A. E. (1954). Bisexual reproduction in the mother sporocyst of Paragonimus kellicotti (Trematoda). Transactions of the American Microscopical Society 73, 16–28.Google Scholar
Woodhead, A. E. (1955). The germ cell cycle in the trematode family Brachylaemidae. Transactions of the American Microscopical society 74, 28–37.Google Scholar
Yamaguti, S. (1959). Systema Helminthum vol. 2., The Cestodes of Vertebrates. New York and London: Interscience Publishers Inc.Google Scholar