Parasitology

Research Article

Density-dependent processes in the transmission of human onchocerciasis: relationship between the numbers of microfilariae ingested and successful larval development in the simuliid vector

M. G. Basáñeza1a7*, J. H. F. Remmea2, E. S. Alleya3, O. Baina4, A. J. Shelleya5, G. F. Medleya6 and R. M. Andersona7

a1 Department of Biology, Imperial College of Science, Technology and Medicine, Prince Consort Road, London SW7 2BB, UK

a2 UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases, World Health Organization, 20 Av. Appia, CH-1211 Geneva 27, Switzerland

a3 Onchocerciasis Control Programme in West Africa, P.O. Box 549, Ouagadougou, Burkina Faso

a4 Muséum d 'Histoire Naturelle, 61 rue Buff on 75231, Paris Cedex 05, France

a5 Natural History Museum, Cromwell Road, London SW7 5BD, UK

a6 Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK

a7 Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

SUMMARY

A previous paper reported that the intake of Onchocerca volvulus microfilariae (mff) by different species of Simulium is essentially proportional to the parasite load in the skin of infected carriers. This paper examines the fate of the ingested mff in susceptible vectors to assess the relationship between parasite intake and infective larval output in blackfly species with and without well-developed cibarial armatures. Analysis is based on data from 3 onchocerciasis endemic areas: Guatemala (S. ochraceum s.l.), West Africa (S. damnosum s.l./S. sirbanum) and the Amazonian focus between South Venezuela and Northern Brazil (S. guianense and S. oyapockense s.l.). The data, which include published and unedited information collected in the field, record experimental studies of parasite uptake by wild flies maintained in captivity until the completion of the extrinsic incubation period. The relationship between L3 output (measured as the mean number of successful larvae/fly or, as the proportion of flies with infective larvae) and average microfilarial intake, was strongly non-linear. This non-linearity was best represented by a sigmoid function in case of armed simuliids (S. ochraceum s.l., S. oyapockense s.l.), or by a hyperbolic expression in that of unarmed flies (S. damnosum s.l., S. guianense). These results are compatible, respectively, with the patterns of ‘initial facilitation’ and ‘limitation’ described in culicid vectors of lymphatic filariases. A maximum mean number of 1–3 L3/fly was observed in all 4 vectors. It is concluded that O. volvulus larval development to the infective stage is regulated by density-dependent mechanisms acting at the early phase of microfilarial migration out of the blackfly's bloodmeal. Damage by the bucco-pharyngeal armature may also be density dependent. A hypothesis, based on this density dependence is forwarded to explain initial facilitation, so far only recorded in vectors with well-developed cibarial teeth. Our results provide quantitative support for the conjecture that chemotherapy alone is likely to have a greater impact on reducing onchocerciasis transmission in endemic areas where the main vector has a toothed fore-gut than in foci where the vectors have unarmed cibaria.

(Received July 27 1994)

(Revised October 07 1994)

(Accepted October 07 1994)

Footnotes

* Reprint requests to María-Gloria Basáñez, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS.

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