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A comparative study of the life-histories of mammalian schistosomes

Published online by Cambridge University Press:  06 April 2009

Eric S. Loker
Affiliation:
Department of Zoology, Oregon State University, Corvallis, Oregon 97331

Summary

Available data in the literature pertaining to the life-history characteristics of all known species of mammalian schistosomes have been gathered, and correlations between such variables as length of pre-patent period, adult worm size, rate of progeny production and progeny size have been explored. Accommodation of the schistosome life-cycle to the constraints imposed by certain host characteristics such as life-expectancy and size is discussed. Of the 23 known species of mammalian schistosomes, 20 species apparently rely to a major extent on relatively large-bodied and long-lived mammals such as primates, ungulates and proboscideans for their transmission. Only 1 species, Schistosomatium douthitti, is exclusively dependent on rodents for its transmission. S. douthitti attains maturity within its definitive host faster than any other mammalian schistosome, and is the only species known to be capable of producing viable eggs by facultative parthenogenesis. For all species of mammalian schistosomes, adult worm size, as estimated by female length, is positively correlated with the number of uterine eggs contained within the female (r = 0·682). For the 7 species for which data exist, rate of egg production/worm pair/day is positively correlated with uterine egg counts (r = 0·873) and inversely correlated with egg length (r = −0·787) and miracidium length (r = −0·953). Length of the pre-patent period is positively correlated with egg length (r = 0·503). With respect to the molluscan host, the number of cercariae produced by snails is positively correlated with the shell size of the snail (r = 0·657). For the 5 species for which data exist, the rate of egg production is inversely correlated with shell size of the intermediate host (r = −0·955) and the common logarithm of the number of cercariae produced (r = −0·893). Comparisons between species suggest that exceptionally low rates of cercariae production in the intermediate host may be compensated for by rapid rates of egg production in the definitive host, implying a degree of integration in the schistosome life-cycle not previously appreciated. Most species of mammalian schistosomes have long-lived definitive hosts, and snail hosts capable of producing many cercariae; compensatory relationships are therefore less obvious in such species. Additional quantitative data on all aspects of schistosome life-histories, particularly rate and duration of egg production, are needed to confirm or refute the relationships discussed above.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

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References

REFERENCES

Abdel-Malek, E. T. G. (1959). Natural and experimental infection of some bulinid snails in the Sudan with Schistosoma haematobium. Proceedings of the Sixth International Congress of Tropical Medicine and Malaria 2, 4352.Google Scholar
Anderson, R. M. & May, R. M. (1979). Prevalence of schistosome infections within molluscan populations, observed patterns and theoretical predictions. Parasitology 79, 6394.CrossRefGoogle ScholarPubMed
Armstrong, J. C. (1965). Mating behavior and development of schistosomes in the mouse. Journal of Parasitology 51, 605–16.CrossRefGoogle ScholarPubMed
Barretto, A. C. & Barbosa, F. S. (1959). Vector qualities of the hosts of Schistosoma mansoni in northeastern Brazil. IV. Elimination of cercariae of Schistosoma mansoni by Australorbis glabratus of different diameters. Annals of the Society of Biology of Pernambuco 16, 1318.Google Scholar
Belding, D. L. (1965). Textbook of Clinical Parasitology. 3rd edition. New York: Appleton-Century-Crofts.Google Scholar
Berberian, D. A., Paquin, H. O. Jr. & Fantauzzi, A. (1953). Longevity of Schistosoma haematobium: observations based on a case. Journal of Parasitology 39, 517–19.CrossRefGoogle ScholarPubMed
Bourns, T. K. R., Ellis, J. C. & Rau, M. E. (1973). Migration and development of Trichobilharzia ocellata (Trematoda: Schistosomatidae) in its duck host. Canadian Journal of Zoology 51, 1021–30.CrossRefGoogle Scholar
Brown, D. S. (1980). Freshwater Snails of Africa and their Medical Importance. London: Taylor and Francis Ltd.Google Scholar
Brumpt, E. (1931). Description de deux bilharzies de mammiferes africains. Schistosoma curassoni sp. inquir. et. Schistosoma rodhaini n.sp. Annales de Parasitologic Humaine et Comparée 9, 325–38.CrossRefGoogle Scholar
Bushara, M. O., Majid, A. A., Saad, A. M., Hussein, M. F., Taylor, M. G., Dargie, J. D., Marshall, T. F. de C. & Nelson, G. S. (1980). Observations on cattle schistosomiasis in the Sudan, a study of comparative medicine. II. Experimental demonstration of naturally acquired resistance to Schistosoma bovis. American Journal of Tropical Medicine and Hygiene 29, 442–51.CrossRefGoogle Scholar
Byram, J. E. & von Lichtenberg, F. (1980). Experimental infection with Schistosoma mekongi in laboratory animals: parasitological and pathological findings. In The Mekong Schistosome (ed. Bruce, J. I. and Sornmani, S.), pp. 125–59, Malacological Review, Suppl. 2, Whitmore Lake, Michigan.Google Scholar
Carmichael, A. C. & Muchlinski, A. E. (1980). Survival of Schistosomatium douthitti during hibernation in the natural host, Zapus hudsonius. Journal of Parasitology 66, 365–6.CrossRefGoogle Scholar
Carney, W. P., Brown, R. J., van Peenen, P. F. D., Purnomo, , Birahim, B. & Koesharjono, . (1977 a). Schistosoma incognitum from Cikurai, West Java, Indonesia. International Journal for Parasitology 7, 361–6.CrossRefGoogle ScholarPubMed
Carney, W. P., Purnomo, , van Peenen, P. F. D., Brown, R. J. & Sudomo, M. (1977 b). Schistosoma incognitum from mammals of Central Sulawesi, Indonesia. Proceedings of the Helminthological Society of Washington 44, 150–5.Google Scholar
Chauhan, A. S., Srivastava, C. B. & Chauhan, B. S. (1973). Studies on the trematode fauna of India. Part 6. Digenea: Schistosomatidae. A monographic aid to the identification of Indian schistosomes. Journal of the Zoological Society of India 25, 83127.Google Scholar
Cheever, A. W. & Anderson, L. A. (1971). Rate of destruction of Schistosoma mansoni eggs in the tissues of mice. American Journal of Tropical Medicine and Hygiene 20, 62–8.CrossRefGoogle ScholarPubMed
Cheever, A. W. & Duvall, R. H. (1974). Single and repeated infections of grivet monkeys with Schistosoma mansoni: parasitological and pathological observations over a 31-month period. American Journal of Tropical Medicine and Hygiene 23, 884–94.CrossRefGoogle Scholar
Cheever, A. W., Duvall, R. H. & Barral-Netto, M. (1982). Parasitological and pathological findings in Capuchin monkeys infected with Schistosoma japonicum or Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 31, 983–7.CrossRefGoogle ScholarPubMed
Cheever, A. W., Kirschstein, R. L. & Reardon, L. V. (1970). Schistosoma mansoni infection of presumed natural origin in Cercopithecus monkeys from Tanzania and Ethiopia. Bulletin of the World Health Organization 42, 486–90.Google ScholarPubMed
Cheever, A. W., Torky, A. H. & Shirbiney, M. (1975). The relation of worm burden to passage of Schistosoma haematobium eggs in the urine of infected patients. American Journal of Tropical Medicine and Hygiene 24, 284–8.CrossRefGoogle ScholarPubMed
Cheever, A. W., Erickson, D. G., Sadun, E. G. & von Lichtenberg, F. (1974). Schistosoma japonicum infections in monkeys and baboons: parasitological and pathological findings. American Journal of Tropical Medicine and Hygiene 23, 5164.CrossRefGoogle Scholar
Chiu, J. K. & Kao, C. T. (1973). Studies on host-parasite relationships of Ilan strain of Schistosoma japonicum in animals. I. Prepatent period. Chinese Journal of Microbiology 6, 72–9.Google Scholar
Chu, K. Y. & Dawood, I. K. (1970). Cercarial production from Biomphalaria alexandrina infected with Schistosoma mansoni. Bulletin of the World Health Organization 42, 569–74.Google ScholarPubMed
Clarke, A. H. (1981). The Freshwater Molluscs of Canada. Ottawa: National Museum of Natural Sciences, National Museums of Canada.CrossRefGoogle Scholar
Coelho, M. de V. & Barbosa, F. S. (1956). Qualidades de vetor dos hospedeiros de Schistosoma mansoni no Nordeste do Brasil. III. Duração da infestação e eliminação de cercarias em Tropicorbis centimetralis. Publicações Avulsas Centro de Pesquisas Aggeu Magalhães 5, 2130.Google Scholar
Coelho, P. M. Z., Dias, M., Mayrink, W., Magalhães, P., Mello, M. N. & Costa, C. A. (1979). Wild reservoirs of Schistosoma mansoni from Caratinga, an endemic schistosomiasis area of Minas Gerais State, Brazil. American Journal of Tropical Medicine and Hygiene 28, 163–4.CrossRefGoogle Scholar
Coles, G. C. (1973). The effect of diet and crowding on the shedding of Schistosoma mansoni cercariae by Biomphalaria glabrata. Annals of Tropical Medicine and Parasitology 67, 419–23.CrossRefGoogle Scholar
Combes, C., Leger, N. & Golvan, Y. J. (1975). Le rôle du rat dans la dynamique de l'endémie schistosomienne en Guadeloupe. Comptes rendus de l' Académic des Sciences, Paris 281, 1059.Google ScholarPubMed
Cowper, S. G. (1953). Schistosomiasis in Mauritius. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 564–79.CrossRefGoogle ScholarPubMed
Damian, R. T., Greene, N. D., Meyer, K. F., Cheever, A. W., Hubbard, W. J., Hawes, M. E. & Clark, J. D. (1976). Schistosoma mansoni in baboons. III. The course and characteristics of infection, with additional observations on immunity. American Journal of Tropical Medicine and Hygiene 25, 299306.CrossRefGoogle ScholarPubMed
Davis, G. M. (1980). Snail hosts of Asian Schistosoma infecting man: evolution and coevolution. In The Mekong Schistosome (ed. Bruce, J. I. and Sornmani, S.), pp. 195238, Malacological Review, Suppl. 2, Whitmore Lake, Michigan.Google Scholar
Davis, G. M. & Carney, W. P. (1973). Description of Oncomelania hupensis lindoensis, first intermediate host of Schistosoma japonicum in Sulawesi (Celebes). Proceedings of the Academy of Natural Sciences of Philadelphia 125, 134.Google Scholar
Dinnik, J. A. & Dinnik, N. N. (1965). The schistosomes of domestic ruminants in Eastern Africa. Bulletin of the Epizootic Diseases of Africa 13, 341–59.Google ScholarPubMed
Dutt, S. C. (1967). Studies on Schistosoma nasale Rao, 1933. I. Morphology of the adults, egg and larval stages. Indian Journal of Veterinary Science and Animal Husbandry 37, 249–62.Google Scholar
Dutt, S. C. & Srivastava, H. D. (1961). Morphology and life history of the mammalian blood-fluke, Orientobilharzia dattai (Dutt and Srivastava). I. Morphology of the adult, egg and miracidium. Indian Journal of Veterinary Science and Animal Husbandry 31, 288303.Google Scholar
Dutt, S. C. & Srivastava, H. D. (1962 a). Biological studies on Orientobilharzia dattai (Dutt and Srivastava, 1952) Dutt and Srivastava, 1955 – a blood fluke of ruminants. Indian Journal of Veterinary Science and Animal Husbandry 32, 216–28.Google Scholar
Dutt, S. C. & Srivastava, H. D. (1962 b). Studies on the morphology and life history of the mammalian blood fluke, Orientobilharzia dattai (Dutt and Srivastava, 1952) Dutt and Srivastava, 1955. III. Definitive host specificity. Indian Journal of Veterinary Science and Animal Husbandry 32, 260–8.Google Scholar
Dutt, S. C. & Srivastava, H. D. (1968). Studies on Schistosoma nasale Rao, 1933. II. Molluscan and mammalian hosts of the blood-fluke. Indian Journal of Veterinary Science and Animal Husbandry 38, 210–16.Google Scholar
El-Gindy, M. S. (1951). Post-cercarial development of Schistosomatium douthitti (Cort, 1914) Price 1931 in mice, with special reference to the genital system (Schistosomatidae-Trematoda). Journal of Morphology 89, 151–85.CrossRefGoogle Scholar
Fain, A. (1952). Description de la cercaire de Schistosoma intercalatum Fisher 1934 et d'une nouvelle xiphidocercaire du groupe Ornatae (sous-groupe Prima). Annates de la Société Beige de Médecine Tropicale 32, 433–3.Google Scholar
Fain, A., Thienpont, D., Herin, V. & Deramee, O. (1953). Observations sur Schistosoma rodhaini Brumpt au Ruanda Urundi, et description de la cercaire de ce schistosome. Annates de la Société Beige de Médecine Tropicale 33, 423–43.Google Scholar
Farley, J. (1971). A review of the family Schistosomatidae: excluding the genus Schistosoma from mammals. Journal of Helminthology 45, 289320.CrossRefGoogle ScholarPubMed
Faust, E. C. & Hoffman, W. A. (1934). Studies on schistosomiasis mansoni in Puerto Rico. III. Biological studies. 1. The extra-mammalian phase of the life cycle. Puerto Rico Journal of Public Health and Tropical Medicine 10, 147.Google Scholar
Faust, E. C. & Meleney, H. E. (1924). Studies on schistosomiasis japonica. American Journal of Hygiene, Monograph Series 3, 1339.Google Scholar
Faust, E. C., Jones, C. A. & Hoffman, W. A. (1934). Studies on schistosomiasis mansoni in Puerto Rico. III. Biological studies. 2. The mammalian phase of the life cycles. Puerto Rico Journal of Public Health and Tropical Medicine 10, 133–96.Google Scholar
Fisher, A. C. (1934). A study of the schistosomiasis of the Stanleyville district of the Belgian Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 28, 277306.CrossRefGoogle Scholar
Foster, R. & Broomfield, K. E. (1971). Preliminary studies on the development of Schistosoma mansoni in rhesus monkeys following different regimens of infection. Annals of Tropical Medicine and Parasitology 65, 367–84.CrossRefGoogle ScholarPubMed
Frandsen, F. (1975). Host–parasite relationship of Bulinus forskalii (Ehrenberg) and Schistosoma intercalatum Fisher 1934, from Cameroun. Journal of Helminthology 49, 7384.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979 a). Studies of the relationships between Schistosoma and their intermediate hosts. I. The genus Bulinus and Schistosoma haematobium from Egypt. Journal of Helminthology 53, 1529.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979 b). Studies of the relationships between Schistosoma and their intermediate hosts. II. The genus Bulinus and Schistosoma haematobium from Sudan, Zaire and Zambia. Journal of Helminthology 53, 205–12.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979 c). Studies of the relationship between Schistosoma and their intermediate hosts. III. The genus Biomphalaria and Schistosoma mansoni from Egypt, Kenya, Sudan, Uganda, West Indies (St. Lucia) and Zaire (two different strains: Katanga and Kinshasa). Journal of Helminthology 53, 321–48.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979 d). Studies of the relationships between Schistosoma and their intermediate hosts. IV. The genus Bulinus and Schistosoma bovis from Morocco. Journal of Helminthology 53, 349–55.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979 e). Further studies on the compatibility between S. intercalatum from Cameroun and Zaire and species of Bulinus. Zeitschrift für Parasitenkunde 58, 161–7.CrossRefGoogle ScholarPubMed
Fripp, P. J. (1967). On the morphology of Schistosoma rodhaini (Trematoda, Digenea, Schisto-somatidae). Journal of Zoology 151, 433–52.CrossRefGoogle Scholar
Fripp, P. J. (1968). Some observations on the behavior of the Kampala strain of Schistosoma rodhaini Brumpt in the laboratory. South African Journal of Medical Science 33, 2130.Google ScholarPubMed
Goddard, M. J. & Jordan, P. (1980). On the longevity of Schistosoma mansoni in man on St. Lucia, West Indies. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 185–91.CrossRefGoogle Scholar
Goff, W. L. & Ronald, N. C. (1981). Certain aspects of the biology and life cycle of Heterobilharzia americana in East Central Texas. American Journal of Veterinary Research 42, 1775–7.Google ScholarPubMed
Graber, M. (1978). Schistosoma margrebowiei of cobs in Chad. Journal of Helminthology 52, 72–4.CrossRefGoogle ScholarPubMed
Hairston, N. G. (1965). An analysis of age prevalence data by catalytic models. Bulletin ofthe World Health Organization 33, 163–75.Google ScholarPubMed
Hairston, N. (1973). The dynam ics of transmission. In Epidemiology and Control of Schistosomiasis (ed. Ansari, N.), pp. 250336. Basel: Karger, and Baltimore: University Park Press.Google Scholar
Hsu, H. F. & Hsu, S. H. Li. (1958). The prepatent period of four geographic strains of Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 52, 363–7.CrossRefGoogle ScholarPubMed
Hubendick, B. (1951). Recent Lymnaeidae. Their variation, morphology, taxonomy, nomenclature, and distribution. Kungl. Svenska Vetenskapsakademiens Handlingar 3, 1223.Google Scholar
Hunter, G. W. III, Bennett, H. J., Ingalls, J. W. & Greene, E. (1947). The molluscanintermediate host and schistosomiasis japonica. III. Experimental infection of Oncomelania quadrasi, the molluscan intermediate host of Schistosoma japonicum. American Journal of Tropical Medicine and Hygiene 27, 597602.CrossRefGoogle Scholar
Hussein, M. F. (1971). The pathology of experimental schistosomiasis in calves. Research in Veterinary Science 12, 246–52.CrossRefGoogle ScholarPubMed
Iijima, T., Lo, C.-T. & Ito, Y. (1971). Studies on schistosomiasis in the Mekong Basin. I. Morphological observation of the schistosomes and detection of their reservoir hosts. Japanese Journal of Parasitology 20, 2433.Google Scholar
Jordan, P., von Lichtenberg, F. & Goatly, K. D. (1967). Experimental schistosomiasis in primates in Tanzania. Preliminary observations on the susceptibility of the baboon Papio anubis to Schistosoma haematobium and Schistosoma mansoni. Bulletin of the World Health Organization 37, 393403.Google ScholarPubMed
Jourdane, J. (1978). Permissivité du rat (Rattus rattus) de Guadeloupe à 1'égard de Schistosoma mansoni et mise en évidence d'une migration des schistosomes vers les poumons. Comptes rendus de l'Académie des Sciences, Paris 286, 1001.Google Scholar
Kitikoon, V. (1980). Comparison of eggs and miracidia of Schistosoma mekongi and S. japonicum. In The Mekong Schistosome (ed. Bruce, J. I. and Sornmani, S.), pp. 93103, Malacological Review, Suppl. 2, Whitmore Lake, Michigan.Google Scholar
Koura, M. (1970). The relation between egg production and worm burden in experimental schistosomiasis. I. Worm burden. Journal of the Egyptian Medical Association 53, 598602.Google ScholarPubMed
Koura, M. (1971). The relation between egg production and worm burden in experimental schistosomiasis. II. Duration of infection. Journal of the Egyptian Medical Association 54, 446–50.Google ScholarPubMed
Kruatrachue, M., Bhaibulaya, M. & Harinasuta, C. (1965). Ornithobilharzia harinasutai sp.n., a mammalian blood-fluke, its morphology and life cycle. Annals of Tropical Medicine and Parasitology 59, 181–8.CrossRefGoogle Scholar
Kuntz, R. E. & Malakatis, G. M. (1955 a). Susceptibility studies in schistosomiasis. IV. Susceptibility of wild mammals to infection by Schistosoma haematobium in Egypt, with emphasis on rodents. Journal of Parasitology 41, 467–75.CrossRefGoogle ScholarPubMed
Kuntz, R. E. & Malakatis, G. M. (1955 b). Susceptibility studies in schistosomiasis. II. Susceptibility of wild mammals to infection by Schistosoma mansoni in Egypt, with emphasis on rodents. American Journal of Tropical Medicine and Hygiene 4, 7589.CrossRefGoogle ScholarPubMed
Lawrence, J. A. (1973). Schistosoma mattheei in cattle: variations in parasite egg production. Research in Veterinary Science 14, 402–4.CrossRefGoogle ScholarPubMed
Lawrence, J. A. (1974). Schistosoma mattheei in sheep: the host–parasite relationship. Research in Veterinary Science 17, 263–4.CrossRefGoogle ScholarPubMed
Lee, H. F. (1962 a). Life history of Heterobilharzia americana Price 1929, a schistosome of the raccoon and other mammals in southeastern United States. Journal of Parasitology 48, 728–39.CrossRefGoogle ScholarPubMed
Lee, H. F. (1962 b). Susceptibility of mammalian hosts to experimental infection with Heterobilharzia americana. Journal of Parasitology 48, 740–5.CrossRefGoogle ScholarPubMed
Lengy, J. (1962). Studies on Schistosoma bovis (Sonsino, 1876) in Israel. I. Larval stages from egg to cercaria. Bulletin of the Research Council of Israel 10, 136.Google Scholar
Le Roux, P. L. (1929). Notes on the life cycle of Schistosoma mattheei and observations on the control and eradication of schistosomiasis in man and animals. 15th Annual Report of the Director of Veterinary Services,Union of South Africa, pp. 407–438.Google Scholar
Le Roux, P. L. (1955). A new mammalian schistosome (Schistosoma leiperi sp.nov.) from herbivora in Northern Rhodesia (Demonstration). Transactions of the Royal Society of Tropical Medicine and Hygiene 49, 293–4.Google Scholar
Liang, Y.-S. & Kitikoon, V. (1980). Susceptibility of Lithoglyphopsis aperta to Schistosoma mekongi and Schistosoma japonicum. In The Mekong Schistosome (ed. Bruce, J. I. and Sornmani, S.), pp. 5360, Malacological Review, Suppl. 2, Whitmore Lake, Michigan.Google Scholar
Loker, E. S. (1979). Effects of Schistosomatium douthitti infection on the growth, survival, and reproduction of Lymnaea catascopium. Journal of Invertebrate Pathology 34, 138–44.CrossRefGoogle ScholarPubMed
Machattie, C. (1936). A preliminary note on the life history of Schistosoma turkestanicum Skrjabin 1913. Transactions of the Royal Society of Tropical Medicine and Hygiene 30, 115–21.CrossRefGoogle Scholar
Malek, E. A. (1961). The biology of mammalian and bird schistosomes. Bulletin of the Tulane University Medical Faculty 20, 181207.Google ScholarPubMed
Malek, E. A. (1967). Experimental infection of several lymnaeid snails with Heterobilharzia americana. Journal of Parasitology 53, 700–2.CrossRefGoogle ScholarPubMed
Malek, E. A. (1969). Studies on bovine schistosomiasis in the Sudan. Annals of Tropical Medicine and Parasitology 63, 501–13.CrossRefGoogle ScholarPubMed
Malek, E. A. (1977). Geographical distribution, hosts, and biology of Schistosomatium douthitti (Cort, 1914) Price, 1931. Canadian Journal of Zoology 55, 661–71.CrossRefGoogle ScholarPubMed
Martins, A. V. (1958). Non-human vertebrate hosts of Schistosoma haematobium and Schistosoma mansoni. Bulletin of the World Health Organization 18, 931–44.Google ScholarPubMed
Massoud, J. (1973 a). Parasitological and pathological observations on Schistosomabovis Sonsino, 1876, in calves, sheep and goats in Iran. Journal of Helminthology 47, 155–64.CrossRefGoogle ScholarPubMed
Massoud, J. (1973 b). Studies on the schistosomes of domestic animals in Iran. I. Observations on Ornithobilharzia turkestanicum (Skrjabin, 1913) in Khuzestan. Journal of Helminthology 47, 165–80.CrossRefGoogle ScholarPubMed
Massoud, J. (1974). The effect of variation in miracidial exposure dose on laboratory infections of Ornithobilharzia turkestanicum in Lymnaea gedrosiana. Journal of Helminthology 48, 139–44.CrossRefGoogle ScholarPubMed
McClelland, W. J. F. (1965). The production of cercariae by Schistosoma mansoni and S. haematobium and methods for estimating the numbers of cercariae in suspension. Bulletin of the World Health Organization 33, 270–5.Google ScholarPubMed
McClelland, W. J. F. (1967). Production of Schistosoma haematobium and Schistosoma mansoni cercariae in Tanzania. Experimental Parasitology 20, 205–18.CrossRefGoogle ScholarPubMed
McCully, R. M., van Niekerk, J. W. & Kruger, S. P. (1967). Observations on the pathology of bilharziasis and other parasitic infections of Hippopotamus amphibius Linnaeus, 1758 from the Kruger National Park. Onderslepoort Journal of Veterinary Research 34, 563618.Google ScholarPubMed
McDonald, M. E. (1969). Catalogue of helminths of waterfowl (Anatidae). U.S. Department of the Interior Fish and Wildlife Service, Bureau of Sport Fisheries and Wildlife Special Scientific Report, Wildlife No. 126.Google Scholar
Moore, D. V. & Sandground, J. H. (1956). The relative egg producing capacity of Schistosoma mansoni and Schistosoma japonicum. American Journal of Tropical Medicine and Hygiene 5, 831–40.CrossRefGoogle ScholarPubMed
Morris, D. (1965). The Mammals. London: Hodder and Stoughton.Google Scholar
Mudaliar, S. V. & Ramanujachary, G. (1945). Schistosoma nairi n.sp. from an elephant. Indian Veterinary Journal 22, 14.Google Scholar
Nelson, G. S. & Saoud, M. F. A. (1968). A comparison of the pathogenicity of two geographical strains of Schistosoma mansoni in rhesus monkeys. Journal of Helminthology 42, 339–62.CrossRefGoogle ScholarPubMed
Pan American Health Organization. (1968). A guide for the identification of the snail intermediate hosts of schistosomiasis in the Americas. Scientific Publication No. 168.Google Scholar
Papasarathorn, T., Tongkoom, B., Hiraniramon, S. & ITO, J. (1963). On the discovery and prevalence of Schistosoma spindale (Montgomery, 1906) in Thailand. Japanese Journal of Medical Science and Biology 16, 3943.CrossRefGoogle ScholarPubMed
Pesigan, T. P., Farooq, M., Hairston, N. G., Jauregui, J. J., Garcia, E. G., Santos, A. T., Santos, B. C. & Besa, A. A. (1958 a). Studies on Schistosoma japonicum infection in the Philippines. 1. General consideration and epidemiology. Bulletin of the World Health Organization 18, 345455.Google ScholarPubMed
Pesigan, T. P., Hairston, N. G., Jauregui, J. J., Garcia, E. G., Santos, A. T., Santos, B. C. & Besa, A. A. (1958 b). Studies on Schistosoma japonicum infection in the Philippines. 2. The molluscan host. Bulletin of the World Health Organization 18, 481578.Google ScholarPubMed
Pitchford, R. J. (1977). A check list of definitive hosts exhibiting evidence of the genus Schistosoma Weinland, 1858 acquired naturally in Africa and the Middle East. Journal of Helminthology 51, 229–52.CrossRefGoogle ScholarPubMed
Pitchford, R. J. & Visser, P. S. (1981). Schistosoma Weinland, 1858 from Hippopotamus amphibius Linnaeus, 1758 in the Kruger National Park. Onderstepoort Journal of Veterinary Research 48, 181–4.Google ScholarPubMed
Powers, K. G. & Cheever, A. W. (1972). Comparison of geographical strains of Schistosoma mansoni in the rhesus monkey. Bulletin of the World Health Organization 46, 295300.Google ScholarPubMed
Price, H. F. (1931). Life history of Schistosomatium douthitti (Cort). American Journal of Hygiene 13, 685727.Google Scholar
Rao, M. A. N. (1934). A comparative study of Schistosoma spindalis, Montgomery, 1906 and S. nasalis n.sp. Indian Journal of Veterinary Science and Animal Husbandry 4, 128.Google Scholar
Richards, C. S. (1963). Infectivity of Schistosoma mansoni for Puerto Rican mollusks, including a new potential intermediate host. American Journal of Tropical Medicine and Hygiene 12, 2633.CrossRefGoogle ScholarPubMed
Sadun, E. H., von Lichtenberg, F., Hickman, R. L., Bruce, J. I., Smith, J. H. & Schoenbechler, M. J. (1966). Schistosomiasis mansoni in the chimpanzee: parasitologic, clinical, serologic, pathologic and radiologic observations. American Journal of Tropical Medicine and Hygiene 15, 496506.CrossRefGoogle ScholarPubMed
Sadun, E. H., von Lichtenberg, F., Cheever, A. W., Erickson, D. G. & Hickman, R. L. (1970). Experimental infection with Schistosoma haematobium in chimpanzees. American Journal of Tropical Medicine and Hygiene 19, 427–58.CrossRefGoogle ScholarPubMed
Saoud, M. F. A. (1965). Comparative studies on the characteristics of some geographical strains of Schistosoma mansoni in mice and hamsters. Journal of Helminthology 39, 101–12.CrossRefGoogle Scholar
Saoud, M. F. A. (1966). On the morphology of Schistosoma rodhaini from Kenya. Journal of Helminthology 40, 147–54.CrossRefGoogle ScholarPubMed
Schwetz, J. (1954). On two schistosomes of wild rodents of the Belgian Congo: Schistosoma rodhaini Brumpt, 1931; and Schistosoma mansoni var. rodentorum Schwetz, 1953; and their relationship to S. mansoni of man. Transactions of the Royal Society of Tropical Medicine and, Hygiene 48, 89100.CrossRefGoogle Scholar
Schwetz, J. (1956). Some new comparative investigations on three Physopsis borne schistosomes: Schistosoma haematobium, S. bovis, and S. intercalatum. American Journal of Tropical Medicine and Hygiene 5, 1071–85.CrossRefGoogle ScholarPubMed
Short, R. B. (1952 a). Sex studies on Schistosomatium douthitti, Cort, 1914, Price, 1931, Trematoda, Schistosomatidae. American Midland Naturalist 47, 154.CrossRefGoogle Scholar
Short, R. B. (1952 b). Uniparental miracidia of Schistosomatium douthitti and their progeny (Trematoda, Schistosomatidae). American Midland Naturalist 48, 5568.CrossRefGoogle Scholar
Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85, 1350.Google Scholar
Sinha, P. K. & Srivastava, H. D. (1956). Studies on Schistosoma incognitum Chandler, 1926. I. On the synonymy and morphology of the blood fluke. Parasitology 46, 91100.CrossRefGoogle ScholarPubMed
Sinha, P. K. & Srivastava, H. D. (1960). Studies on Schistosoma incognitum Chandler, 1926. II. On the life history of the blood fluke. Journal of Parasitology 46, 629–41.CrossRefGoogle Scholar
Smithers, S. R. (1956). On the ecology of schistosome vectors in the Gambia, with the evidence of their role in transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene 50, 354–65.CrossRefGoogle ScholarPubMed
Sornmani, S., Kitikoon, V., Schneider, C. R., Harinasuta, C. & Pathammauong, O. (1973) Mekong schistosomiasis. 1. Life cycle of Schistosoma japonicum, Mekong strain in the laboratory. Southeast Asian Journal of Tropical Medicine and Public Health 4, 218–25.Google ScholarPubMed
Southern, H. N. (1979 a). Population processes in small mammals. In Ecology of Small Mammals (ed. Stoddert, D. M.), pp. 63101. London: Chapman and Hall.CrossRefGoogle Scholar
Southern, H. N. (1979 b). The stability and instability of small mammal populations. In Ecology of Small Mammals (ed. Stoddert, D. M.), pp. 103134. London: Chapman and Hall.CrossRefGoogle Scholar
Southgate, V. R. & Knowles, R. J. (1975). Observations on Schistosoma bovis Sonsino, 1876. Journal of Natural History 9, 273314.CrossRefGoogle Scholar
Southgate, V. R. & Knowles, R. J. (1977). On Schistosoma margrebowiei Le Roux, 1933: the morphology of the egg, miracidium and cercaria, the compatibility with species of Bulinus, and development in Mesocricetus auratus. Zeitschrift für Parasitenkunde 54, 233–50.CrossRefGoogle Scholar
Southgate, V. R., Ross, G. C. & Knowles, R. J. (1981). On Schistosoma leiperi Le Roux, 1955: scanning electron microscopy of adult worms, compatibility with species of Bulinus, development in Mesocricetus auratus, and isoenzymes. Zeitschrift für Parasitenkunde 66, 6381.CrossRefGoogle Scholar
Srivastava, H. D. & Dutt, S. C. (1962). Studies on Schistosoma indicum. Research Series. Indian Council of Agricultural Research 34, 91 pp.Google Scholar
Standen, O. D. (1949). Experimental schistosomiasis. II. Maintenance of Schistosoma mansoni in the laboratory, with some notes on experimental infection with S. haematobium. Annals of Tropical Medicine and Parasitology 43, 268–83.CrossRefGoogle Scholar
Tanabe, B. (1923). The life history of a new schistosome, Schistosomatium patholocopticum Tanabe, found in experimentally infected mice. Journal of Parasitology 9, 183–98.CrossRefGoogle Scholar
Taylor, M. G. (1970). Hybridization experiments on five species of African schistosomes. Journal of Helminthology 44, 253314.CrossRefGoogle ScholarPubMed
Taylor, M. G., Amin, M. B. A. & Nelson, G. S. (1969). ‘Parthenogenesis’ in Schistosoma mattheei. Journal of Helminthology 43, 197206.CrossRefGoogle ScholarPubMed
Taylor, M. G., Nelson, G. S., Smith, M. & Andrews, B. J. (1973). Comparison of the infectivity and pathogenicity of six species of African schistosomes and their hybrids. 2. Baboons. Journal of Helminthology 47, 455–85.CrossRefGoogle ScholarPubMed
Thurston, J. P. (1963). Schistosomes from Hippopotamus amphibius L. I. The morphology of Schistosoma hippopotami sp.nov. Parasitology 53, 4954.CrossRefGoogle Scholar
Thurston, J. P. (1964). Schistosomes from Hippopotamus amphibius L. II. The morphology of Schistosoma edwardiense sp.nov. Parasitology 54, 6772.CrossRefGoogle ScholarPubMed
Vogel, H. (1948). Maintenance of Oncomelania hupensis and experimental infection of it with Bilharzia japonicum. Zeitschrift für Parasitenkunde 14, 7091.CrossRefGoogle Scholar
Vogel, H. & Minning, W. (1940). Bilharziose bei Elefanten. Archiv für Schiffs und Tropen Hygiene 44, 562–74.Google Scholar
von Lichtenberg, F., Sadun, E. H., Cheever, A. W., Erickson, D. G., Johnson, A. J. & Boyce, H. W. (1971). Experimental infection with Schistosoma japonicum in chimpanzees. Parasitologic, clinical, serologic, and pathological observations. American Journal of Tropical Medicine and Hygiene 20, 850–93.CrossRefGoogle Scholar
Wallerstein, R. S. (1949). Longevity of Schistosoma mansoni: observations based on a case. American Journal of Tropical Medicine and Hygiene 29, 717–22.CrossRefGoogle Scholar
Warren, K. S. (1973). The pathology of schistosome infections. Helminthological Abstracts 42, 591633.Google Scholar
Warren, K. S., Mahmoud, A. A. F., Cummings, P., Murphy, D. J. & Mouser, D. B. (1974). Schistosomiasis mansoni in Yemeni in California: duration of infection, presence of disease and therapeutic management. American Journal of Tropical Medicine and Hygiene 23, 902–9.CrossRefGoogle ScholarPubMed
Webbe, G. & James, C. (1971). A comparison of two geographical strains of Schistosoma haematobium. Journal of Helminthology 45, 271–84.CrossRefGoogle ScholarPubMed
Wright, C. A. (1963). Schistosomiasis in the Western Aden Protectorate. A preliminary study. Transactions of the Royal Society of Tropical Medicine and Hygiene 57, 142–7.CrossRefGoogle ScholarPubMed
Wright, C. A. & Bennett, M. S. (1967 a). Studies on Schistosoma haematobium in the laboratory. I. A strain from Durban, Natal, South Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 221–7.CrossRefGoogle Scholar
Wright, C. A. & Bennett, M. S. (1967 b). Studies on Schistosoma haematobium in the laboratory. II. A strain from South Arabia. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 228–33.CrossRefGoogle Scholar
Wright, C. A. & Knowles, R. J. (1972). Studies on Schistosoma haematobium in the laboratory. III. Strains from Iran, Mauritius and Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 108–18.CrossRefGoogle Scholar
Wright, C. A. & Southgate, V. R. (1976). Hybridization of schistosomes and some of its implications. In Symposium of the British Society for Parasitology, vol. 14 (ed. Taylor, A. E. R. and Muller, R.), pp. 5586.Google Scholar
Wright, C. A., Southgate, V. R. & Howard, G. W. (1979). Observations on the life-cycle of Schistosoma margrebowiei and its possible interactions with S. leiperi in Zambia. Journal of Natural History 13, 499506.CrossRefGoogle Scholar
Wright, C. A., Southgate, V. R. & Knowles, R. J. (1972). What is Schistosoma intercalatum, Fisher 1934? Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 2864.CrossRefGoogle ScholarPubMed
Wright, W. H. (1973). Geographical distribution of schistosomes and their intermediate hosts. In Epidemiology and Control of Schistosomiasis (ed. Ansari, N.), pp. 32249. Basel: Karger and Baltimore: University Park Press.Google Scholar
Yamaguti, S. (1971). Synopsis of Digenetic Trematodes of Vertebrates. Vol. 1 and 2. Kyoto, Japan.Google Scholar
Yamaguti, S. (1975). A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates. Kyoto, Japan.Google Scholar