Skip to main content
×
×
Home

Host choice and penetration by Schistosoma haematobium miracidia

  • F. Allan (a1) (a2), D. Rollinson (a2), J.E. Smith (a1) and A.M. Dunn (a1)
Abstract
Abstract

Schistosome parasites commonly show specificity to their intermediate mollusc hosts and the degree of specificity can vary between parasite strains and geographical location. Here the role of miracidial behaviour in host specificity of Schistosoma haematobium on the islands of Zanzibar is investigated. In choice-chamber experiments, S. haematobium miracidia moved towards Bulinus globosus snail hosts in preference to empty chambers. In addition, miracidia preferred uninfected over patent B. globosus. This preference should benefit the parasite as patent snails are likely to have mounted an immune response to S. haematobium as well as providing poorer resources than uninfected snails. Miracidia also discriminated between the host B. globosus and the sympatric, non-host species Cleopatra ferruginea. In contrast, S. haematobium did not discriminate against the allopatric Bulinus nasutus. Penetration of the host by miracidia was investigated by screening snails 24 h after exposure using polymerase chain reaction (PCR) with S. haematobium specific DraI repeat primers. There was no difference in the frequency of penetration of B. globosus versus B. nasutus. These responses to different snail species may reflect selection pressure to avoid sympatric non-hosts which represent a transmission dead end. The distribution of B. nasutus on Unguja is outside the endemic zone and so there is less chance of exposure to S. haematobium, hence there will be little selection pressure to avoid this non-host snail.

Copyright
Corresponding author
*E-mail: a.dunn@leeds.ac.uk
References
Hide All
Adema C.M. & Loker E.S. (1997) Specificity and immunobiology of larval digenean-snail associations. pp. 229263in Fried B. & Graczyk T.K. (Eds) Advances in trematode biology. Boca Raton, CRC Press.
Brown D. (1994) Freshwater snails of Africa and their medical importance. 608 pp. London, Taylor & Francis.
Chitsulo L., Loverde R. & Engels D. (2004) Schistosomiasis. Nature Reviews Microbiology 2, 1213.
Combes C. & Moné H. (1987) Possible mechanisms of the decoy effect in Schistosoma mansoni transmission. International Journal for Parasitology 17, 971975.
Crawley M.J. (1993) GLIM for ecologists. 379 pp. Oxford, Blackwell Scientific Publications.
Haas W. & Haberl B. (1997) Host recognition by trematode miracidaia and cercariae. pp. 196227in Fried B. & Graczyk T.K. (Eds) Advances in trematode biology. Boca Raton, CRC Press.
Haas W., Haberl B., Kalbe M. & Korner M. (1995) Snail host-finding by miracidia and cercariae: chemical host cues. Parasitology Today 11, 468472.
Haberl B., Kalbe M., Fuchs H., Strobel M., Schmalfuss G. & Haas W. (1995) Schistosoma mansoni and Schistosoma haematobium miracidial host finding behavior is stimulated by macromolecules. International Journal for Parasitology 25, 551560.
Hamburger J., He-Na, Abassi I., Ramzy R.M., Jourdane J. & Ruppel A. (2001) Polymerase chain reaction assay based on a highly repeated sequence of Schistosoma haematobium: a potential tool for monitoring schistosome-infested water. American Journal of Tropical Medicine and Hygiene 65, 907911.
Hamburger J., Hoffman O., Kariuki H.C., Muchiri E.M., Ouma J.H., Koech D.K., Sturrock R.F. & King C.H. (2004) Large-scale, polymerase chain reaction-based surveillance of Schistosoma haematobium DNA in snails from transmission sites in coastal Kenya: a new tool for studying the dynamics of snail infection. American Journal of Tropical Medicine and Hygiene 71, 765773.
Hertel J., Holweg A., Haberl B., Kalbe M. & Haas W. (2006) Snail odour-clouds: spreading and contribution to the transmission success of Trichobilharzia ocellata (Trematoda, Digenea) miracidia. Oecologia 147, 173180.
Jørgensen A., Jørgensen L.V.G., Kristensen T.K., Madsen H. & Stothard J.R. (2007) Molecular phylogenetic investigations of Bulinus (Gastropoda: Planorbidae) in Lake Malawi with comments on the topological incongruence between DNA loci. Zoologica Scripta 36, 577585.
Kalbe M., Haberl B. & Haas W. (1996) Schistosoma mansoni miracidial host-finding: species specificity of an Egyptian strain. Parasitology Research 82, 813.
Kalbe M., Haberl B. & Haas W. (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitology Research 83, 806812.
Kalbe M., Haberl B., Hertel J. & Haas W. (2004) Heredity of specific host-finding behaviour in Schistosoma mansoni miracidia. Parasitology 128, 635643.
Kane R.A., Stothard J.R., Emery A.M. & Rollinson D. (2008) Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasites and Vectors 1, 15.
Kariuki H.C., Clennon J.A., Brady M.S., Kitron U., Sturrock R.F., Ouma J.H., Ndzovu S.T.M., Mungai P., Hoffman O., Hamburger J., Pellegrini C., Muchiri E.M. & King C.H. (2004) Distribution patterns and cercarial shedding of Bulinus nasutus and other snail species in the Msambweni area, Coast Province, Kenya. American Journal of Tropical Medicine and Hygiene 70, 449456.
Lively C.M. & Dybdahl M.F. (2000) Parasite adaptation to locally common host genotypes. Nature 405, 679681.
Magalhães L.A., Zanotti-Magalhães E.M. & de Carvalho J.F. (1997) Observations on the miraxonal attraction exercised by sexually immature or adult Biomphalaria glabrata infected or not by Schistosoma mansoni. Revista de Saúde Pública 31, 121124.
Munoz-Antoli C., Trelis M., Toledo R. & Esteban J.G. (2006) Infectivity of Echinostoma friedi miracidia to different snail species under experimental conditions. Journal of Helminthology 80, 323325.
Rollinson D., Stothard J.R. & Southgate V.R. (2001) Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group. Parasitology 123, S245S260.
Rudge J.W., Stothard J.R., Basanez M.-G., Mgeni A.F., Khamis I.S., Kharmis A.N. & Rollinson D. (2008) Micro-epidemiology of urinary schistosomiasis in Zanzibar: local risk factors associated with distribution of infections among school children and relevance for control. Acta Tropica 105, 4554.
Sapp K.K. & Loker E.S. (2000) Mechanisms underlying digenean-snail specificity: role of miracidial attachment and host plasma factors. Journal of Parasitology 86, 10121019.
Sire C., Rognon A. & Theron A. (1998) Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism? Parasitology 117, 117122.
Stothard J.R. & Rollinson D. (1997) Molecular characterization of Bulinus globosus and Bulinus nasutus on Zanzibar, and an investigation of their roles in the epidemiology of Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 353357.
Stothard J.R., Loxton N., Rollinson D., Mgeni A.F., Khamis S., Ameri H., Ramsan M. & Savioli L. (2000) The transmission status of Bulinus on Zanzibar Island (Unguja), with implications for control of urinary schistosomiasis. Annals of Tropical Medicine and Parasitology 94, 8794.
Stothard J.R., Llewellyn-Hughes J., Griffin C.E., Hubbard S.J., Kristensen T.K. & Rollinson D. (2002) Identification of snails within the Bulinus africanus group from East Africa by multiplex SNaPshot (TM) analysis of single nucleotide polymorphisms within the cytochrome oxidase subunit I. Memorias Do Instituto Oswaldo Cruz 97, 3136.
Stothard J.R., Mook P., Mgeni A.F., Khamis S., Khamis A.N. & Rollinson D. (2006) Control of urinary schistosomiasis on Zanzibar (Unguja Island): a pilot evaluation of the educational impact of the Juma na Kichocho health education booklet within primary schools. Memórias do Instituto Oswaldo Cruz 101, 119124.
Théron A., Rognon A. & Pagès J.R. (1998) Host choice by larval parasites: a study of Biomphalaria glabrata snails and Schistosoma mansoni miracidia related to host size. Parasitology Research 84, 727732.
Toledo R., Munoz-Antoli C., Perez M. & Esteban J.G. (1999) Miracidial infectivity of Hypoderaeum conoideum (Trematoda: Echinostomatidae): differential susceptibility of two lymnaeid species. Parasitology Research 85, 212215.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Helminthology
  • ISSN: 0022-149X
  • EISSN: 1475-2697
  • URL: /core/journals/journal-of-helminthology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 21 *
Loading metrics...

Abstract views

Total abstract views: 113 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 16th December 2017. This data will be updated every 24 hours.