Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T06:04:14.591Z Has data issue: false hasContentIssue false
  • English
  • Français

Competitive exclusion in human schistosomes: the restricted distribution of Schistosoma intercalatum

Published online by Cambridge University Press:  06 April 2009

L. A. Tchuem Tchuenté ,
S. Morand ,
D. Imbert-Establet ,
B. Delay  and
J. Jourdane
L. A. Tchuem Tchuenté
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France Laboratoire de Biologie Générale, Faculté des Sciences, Université de Yaoundé I, B.P. 812 Yaoundé, Cameroun Department of Zoology, The Natural History Museum, Cromwell Road, South Kensingston, London, UK
S. Morand
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
D. Imbert-Establet
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
B. Delay
Affiliation:
Laboratoire de Génétique et Environnement, Institut des Sciences de l'Evolution, Université de Montpellier II, place E. Bataillon, 34095 Monpellier Cedex 5, France
J. Jourdane*
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
*
*Corresponding author. Laboratoire de Biologie Animale, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France. Tel: +33 68 66 21 82. Fax: + 33 68 66 22 81. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

A study on the immune and mating interactions between Schistosoma intercalatum and S. mansoni has been carried out. The immunologically mediated interactions and mating patterns observed between the two species demonstrate that S. mansoni is competitively dominant over S. intercalatum. When S. mansoni females are absent, S. mansoni males are more competitive than S. intercalatum males at pairing with S. intercalatum females. The use of a mathematical model shows how the abundance of S. mansoni worms per host could dramatically affect the mating probability of S. intercalatum females with their homologous males. It appears that the competitive exclusion between these two species of schistosomes may probably be an important factor restricting the distribution of S. intercalatum in Africa.

Keywords

competitive exclusionSchistosoma mansoniSchistosoma intercalatumgeographic distributionimmunitymating competitionsex ratio
Type
Research Article
Information
Parasitology , Volume 113 , Issue 2 , August 1996 , pp. 129 - 136
Copyright
Copyright © Cambridge University Press 1996

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

Agnew, A. M., Murare, H. M. & Doenhoff, M. J. (1989). Specific cross-protection between Schistosoma bovis and S. haematobium induced by highly irradiated infections in mice. Parasite Immunology 11, 341–349.Google Scholar
Amin, M. A., Nelson, G. S. & Saoud, M. F. A. (1968). Studies on heterologous immunity on schistosomiasis. 2. Heterologous schistosome immunity in rhesus monkeys. Bulletin of the World Health Organization 38, 19–27.Google Scholar
Arène, F. O. I., Ukeibo, E. T. & Nwawze, E. A. (1989). Studies on Schistosomatidae in the Nigeria Delta: Schistosoma intercalatum in the Urban city of Port Harcourt, Nigeria. Public Health 103, 295–301.CrossRefGoogle ScholarPubMed
Basch, P. F. & Basch, N. (1984). Intergeneric reproductive stimulation and parthenogenesis in Schistosoma mansoni. Parasitology 89, 369–376.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. & Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301–312.CrossRefGoogle ScholarPubMed
Bjorneboe, A. & Frandsen, F. (1979). A comparison of the characteristics of two strains of Schistosoma intercalatum Fisher, 1934 in mice. Journal of Helminthology 53, 195–203.Google Scholar
Brown, D. S. (1994). Freshwater Snails of Africa and their Medical Importance. Taylor and Francis, London.Google Scholar
Brown, D. S., Sarfati, C., Southgate, V. R., Ross, G. C. & Knowles, R. J. (1984). Observations on Schistosoma intercalatum in southeast Gabon. Zeitschrift für Parasitenkunde 70, 243–253.Google Scholar
Burchard, G. D. & Kern, P. (1985). Probable hybridization between S. intercalatum and S. haematobium in western Gabon. Tropical and Geographical Medicine 37, 119–123.Google Scholar
Christensen, N. O., Frandsen, F. & Kristensen, T. K. (1986). African Schistosomes Weinland, 1858 (Digenea: Schistosomatidae) and the intermediate snail host genera Bulinus Müller, 1781 and Biomphalaria Preston, 1910 (Pulmonata; Planorbidae). A review. Revue zoologique africaine. 100, 137–152.Google Scholar
Combes, C. (1991). The schistosomes scandal. Acta Oecologica 12, 165–173.Google Scholar
Corachan, M., Escosa, R., Mas, J., Ruiz, L. & Campo, E. (1987). Clinical presentation of Schistosoma intercalatum infestation. Lancet 1, 1139–1140.CrossRefGoogle ScholarPubMed
Corachan, M., Romero, R., Mas, J., Palacin, A. & Knowles, R. (1988). A case of Schistosoma intercalatum infection from São Tomé. Tropical and Geographical Medicine 40, 147–150.Google Scholar
Damian, R. T. & Chapman, R. W. (1983). The fecundity of Schistosoma haematobium in baboons, with evidence for a sex ratio effect. Journal of Parasitology 69, 987–989.CrossRefGoogle Scholar
Dean, D. A. (1983). Schistosoma and related genera: acquired resistance in mice. Experimental Parasitology 55, 1–104.CrossRefGoogle ScholarPubMed
Doumenge, J. P., Mott, K. E., Cheung, C., Villenave, D., Chapuis, O., Perrin, M. F. & Reaud-Thomas, G. (1987). Atlas of the global distribution of schistosomiasis. CEGET-CNRS-OMS-WHO. Presses Universitaires de Bordeaux, France.Google Scholar
Duvall, R. H. & Dewitt, W. B. (1967). An improved perfusion technique for recovering adult schistosomes from laboratory animals. American Journal of Tropical Medicine and Hygiene 16, 483–486.Google Scholar
Eveland, L. K., Hsu, S. Y. L. & Hsu, H. F. (1969). Cross-immunity of Schistosoma japonicum, S. mansoni and S. bovis in rhesus monkeys. Journal of Parasitology 55, 279–288.CrossRefGoogle ScholarPubMed
Hussein, M. F., Saeed, A. A. & Nelson, G. S. (1970). Studies on heterologous immunity in schistosomiasis. 4. Heterologous schistosome immunity in cattle. Bulletin of the World Health Organization 42, 745–749.Google ScholarPubMed
Hussein, M. F. & Bushara, H. O. (1976). Investigations on the development of an irradiated vaccine for animal schistosomiasis. In: Nuclear Techniques in Animal Production and Health, pp. 421–432. International Atomic Energy Agency, Vienna.Google Scholar
Imbert-establet, D. & Combes, C. (1992). Relocation of Schistosoma mansoni in the lungs and resistance to reinfection in Rattus rattus. Parasitology 104, 51–57.CrossRefGoogle ScholarPubMed
Imbert-Establet, D., Xia, M. Y. & Jourdane, J. (1994). Parthenogenesis in the genus Schistosoma: electrophoretic evidence for this reproduction system in S. japonicum and S. mansoni. Parasitology Research 80, 186–191.Google Scholar
Jourdane, J. & Théron, A. (1980). Schistosoma mansoni: Cloning by microsurgical transplantation of sporocysts. Experimental Parasitology 50, 349–357.CrossRefGoogle ScholarPubMed
Kruger, F. J., Schutte, C. H. J., Visser, P. S. & Evans, R. J. (1986). Scanning electron microscopy of the tegument of males from five populations of Schistosoma mattheei. Onderstepoort Journal of Veterinary Research 53, 103–107.Google ScholarPubMed
Liberatos, J. D. (1987). Schistosoma mansoni: male-biased sex ratios in snails and mice. Experimental Parasitology 64, 165–177.Google Scholar
Loker, E. S. (1983). A comparative study of the life-history of mammalian schistosomes. Parasitology 87, 343–369.Google Scholar
May, R. M. & Woolhouse, M. E. J. (1993). Biased sex ratios and parasite mating probabilities. Parasitology 107, 287–295.Google Scholar
Moloney, N. A., Garcia, E. G. & Webbe, G. (1985). The strain specificity of vaccination with ultra-violet attenuated cercariae of the Chinese strain of Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 245–247.Google Scholar
Moloney, N. A., Webbe, G. & Hinchcliffe, P. (1987). The induction of species-specific immunity against Schistosoma japonicum by exposure of rats to ultraviolet attenuated cercariae. Parasitology 94, 49–54.Google Scholar
Morand, S., Pointier, J. P., Borel, G. & Théron, A. (1993). Pairing probability of schistosomes related to their distribution among the host population. Ecology 74, 2444–2449.CrossRefGoogle Scholar
Navarrete, S., Rollinson, D. & Agnew, A. M. (1994). Cross-protection between species of the Schistosoma haematobium group induced by vaccination with irradiated parasites. Parasite Immunology 16, 19–25.CrossRefGoogle ScholarPubMed
Nelson, G. S., Amin, M. A., Saoud, M. F. A. & Teesdale, C. (1968). Studies on heterologous immunity in schistosomiasis. 1. Heterologous schistosome immunity in mice. Bulletin of the World Health Organization 38, 9–17.Google ScholarPubMed
Pitchford, F. J. (1961). Observations on a possible hybrid between the two schistosomes S. haematobium and S. mattheei. Transactions of the Royal Society of Tropical Medicine and Hygiene 55, 44–51.Google Scholar
Ratard, R. C., Kouemeni, L. E., Ekani, Bessala M., Ndamkou, C. N., Greer, G. J., Spilsbury, J. & Cline, B. L. (1990). Human schistosomiasis in Cameroon. I Distribution of schistosomiasis. American Journal of Tropical Medicine and Hygiene 42, 561–572.CrossRefGoogle ScholarPubMed
Ratcliffe, E. C. & Wilson, R. A. (1991). The magnitude and kinetics of delayed-type hypersensitivity responses in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 103, 65–75.CrossRefGoogle ScholarPubMed
Rollinson, D., Imbert-establet, D. & Ross, G. C. (1986). Schistosoma mansoni from naturally infected Rattus rattus in Guadeloupe: identification, prevalence and enzyme polymorphism. Parasitology 93, 39–53.Google Scholar
Rollinson, D., Southgate, V. R., Vercruysse, J. & Moore, P. J. (1990). Observations on natural and experimental interactions between Schistosoma bovis and S. curassoni from West Africa. Acta Tropica 47, 101–114.CrossRefGoogle ScholarPubMed
Simarro, P. P., Sima, F. O. & Mia, M. (1989). African trypanosomiasis and S. intercalatum infection in Equatorial Guinea: comparative epidemiology and feasibility of integrated control. Tropical Medicine and Parasitology 40, 159–162.Google ScholarPubMed
Smith, M. A., Clegg, J. A. & Webbe, G. (1976). Cross-immunity to Schistosoma mansoni in the hamster. Parasitology 73, 53–64.Google Scholar
Smithers, S. R. & Terry, R. J. (1967). Naturally acquired resistance to experimental infections of Schistosoma mansoni in the rhesus monkey (Macaco mulatta). Parasitology 55, 701–710.CrossRefGoogle Scholar
Southgate, V. R. (1978). On factors possibly restricting the distribution of Schistosoma intercalatum, Fisher 1934. Zeitschrift für Parasitenkunde 56, 183–193.Google Scholar
Southgate, V. R., Rollinson, D., Ross, G. C. & Knowles, R. J. (1982). Mating behaviour in mixed infections of Schistosoma haematobium and S. intercalatum. Journal of Natural History 16, 491–496.Google Scholar
Southgate, V. R., Rollinson, D., Kaukas, A., Almeda, J., Sousa, A. M., Castro, F., Scares, E. & Corachan, M. (1994). Schistosomiasis in the Republic of Sáo Tomé and Principe: characterization of Schistosoma intercalatum. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 479–486.CrossRefGoogle ScholarPubMed
Taylor, M. G. (1970). Hydridization experiments on five species of African schistosomes. Journal of Helminthology 44, 253–314.CrossRefGoogle Scholar
Tchuem, Tchuenté L. A., Imbert-establet, D., Delay, B. & Jourdane, J. (1993). Choice of mate, a reproductive isolating mechanism between Schistosoma intercalatum and S. mansoni in mixed infections. International Journal for Parasitology 23, 179–185.Google Scholar
Tchuem, Tchuenté L. A., Imbert-establet, D., Southgate, V. R. & Jourdane, J. (1994). Interspecific stimulation of parthenogenesis in Schistosoma intercalatum and S. mansoni. Journal of Helminthology 68, 167–173.Google Scholar
Tchuem, Tchuenté L. A., Southgate, V. R., Imbert-establet, D. & Jourdane, J. (1995). Change of mate and mating competition between males of Schistosoma intercalatum and S. mansoni. Parasitology 110, 45–52.Google Scholar
Webbe, G., James, E. R., Nelson, G. S., Ismail, M. M. & Shaw, J. R. (1979). Cross resistance between Schistosoma haematobium and S. mansoni in the baboon. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 42.CrossRefGoogle ScholarPubMed
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. & Muller, R.). Symposium of the British Society of Parasitology 14, 55–86.Google 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, 28–64.Google Scholar
Wright, C. A., Southgate, V. R. & Ross, G. C. (1979). Enzymes in Schistosoma intercalatum and the relative status of the Lower Guinea and Zaire strains of the parasite. International Journal for Parasitology 9, 523–528.Google Scholar