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Malaria parasites enhance blood-feeding of their naturally infected vector Anopheles punctulatus

Published online by Cambridge University Press:  06 April 2009

J. C. Koella*
Affiliation:
Department of Zoology, Universitetsparken B135, DK-8000 Aarhus C, Denmark
M. J. Packer
Affiliation:
Papua New Guinea Institute of Medical Research, Madang, Papua New Guinea
*
*Corresponding author. Tel. +45 89 422721. Fax: + 45 86 125175. E-mail: koella@aau.dk.

Summary

We investigated the blood-feeding behaviour of a natural population of the human-feeding mosquito Anopheles punctulatus in Iguruwe, Papua New Guinea. In particular we investigated the relationship between the mosquitoes' blood-feeding behaviour and their infection by the malaria parasites Plasmodium falciparum and P. vivax. Female mosquitoes were caught at 4 times of the night, the amount of blood they had obtained was measured and their status of infection was evaluated. Among uninfected mosquitoes the bloodmeal size steadily increased through the night, possibly because they were progressively less likely to be disturbed by human activity as the night drew on. Infected mosquitoes, on the other hand, tended to feed maximally at all times of the night. This suggests that infected mosquitoes were more tenacious in their blood-feeding behaviour, being either less readily disturbed during a bout of feeding (and thus feeding longer) or more likely to return to continue their feed following disturbance (and thus feeding several times). Either change would increase the parasites' rate of transmission. We conclude that in this natural situation the two species of malaria parasites modified the mosquitoes' behaviour with the effect of increasing their own transmission.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Anderson, R. A. & Brust, R. A. (1995). Field evidence for multiple host contacts during blood feeding by Culex tarsalis, Cx. restuans, and Cx. nigripalpus (Diptera: Culicidae). Journal of Medical Entomology 32, 705710.CrossRefGoogle ScholarPubMed
Beier, J. C., Onyango, F. K., Koros, J. K., Ramadhan, M., Ogwang, R., Wirtz, R. A., Koech, D. K. & Roberts, C. R. (1991). Quantitation of malaria sporozoites transmitted in vitro during salivation by wild Afrotropical Anopheles. Medical and Veterinary Entomology 5 7179.CrossRefGoogle ScholarPubMed
Briegel, H., Lea, A. O. & Klowden, M. J. (1979). Hemoglobinometry as a method for measuring bloodmeal sizes of mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 15, 235238.CrossRefGoogle Scholar
Burkot, T. R., Graves, P. M., Paru, R. & Lagog, M. (1988). Mixed blood feeding by the malaria vectors in the Anopheles punctulatus complex (Diptera, Culicidae). Journal of Medical Entomology 25, 205213.CrossRefGoogle ScholarPubMed
Burkot, T. R., Williams, J. L. & Schneider, I. (1984). Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 33, 783788.CrossRefGoogle ScholarPubMed
Cavanaugh, D.C. (1971). Specific effect of temperature upon transmission of the plague bacillus by the Oriental rat flea, Xenopsylla cheopis. American Journal of Tropical Medicine and Hygiene 20, 264273.CrossRefGoogle ScholarPubMed
Dye, C. (1986). Vectorial capacity: must we measure all its components? Parasitology Today 2, 203209.CrossRefGoogle ScholarPubMed
Dye, C. (1992). The analysis of parasite transmission by bloodsucking insects. Annual Review of Entomology 37, 119.CrossRefGoogle ScholarPubMed
Edman, J. D. (1974). Host-feeding patterns of Florida mosquitoes III. Culex (Culex) and Culex (Neoculex). Journal of Medical Entomology 2, 95104.CrossRefGoogle Scholar
Edman, J. D. & Downe, A. E. R. (1964). Host-blood sources and multiple-feeding habits of mosquitoes in Kansas. Mosquito News 24, 155160.Google Scholar
Grimstad, P. R., Ross, Q. E. & Craig, G. B. Jr. (1980). Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. II. Modification of mosquito feeding behaviour by virus infection. Journal of Medical Entomology 17, 17.CrossRefGoogle ScholarPubMed
James, A. A. & Rossignol, P. A. (1991). Mosquito salivary glands: parasitological and molecular aspects. Parasitology Today 7, 267271.CrossRefGoogle ScholarPubMed
Jenni, L., Molyneux, D. H., Livesey, J. L. & Galun, R. (1980). Feeding behaviour of tsetse flies infected with salivarian trypanosomes. Nature, London 283, 383385.CrossRefGoogle ScholarPubMed
Kelly, R. & Edman, J. D. (1989). Mosquito size and multiple transmission of avaian malaria in the laboratory. Journal of Medical Entomology 8, 386388.Google Scholar
Kelly, R. & Edman, J. D. (1992). Multiple transmission of Plasmodium gallinaceum (Eucoccida: Plasmodiidae) during serial probing by Aedes aegypti (Diptera: Culicidae) on several hosts. Journal of Medical Entomology 29, 329331CrossRefGoogle ScholarPubMed
Li, X., Sina, B. & Rossignol, P. A. (1992). Probing behaviour and sporozoite delivery by Anopheles stephensi infected with Plasmodium berghei. Medical and Veterinary Entomology 6, 5761.CrossRefGoogle ScholarPubMed
Lyimo, E. O. & Koella, J. C. (1992). Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 104, 233237.CrossRefGoogle ScholarPubMed
MacDonald, G. (1957). The Epidemiology and Control of Malaria. London: Oxford University Press.Google Scholar
Makumi, J. N. & Moloo, S. K. (1991). Trypanosoma Vivax in Glossina palpalis gambiensis do not appear to affect feeding behaviour, longevity or reproductive performance of the vector. Medical and Veterinary Entomology 5, 3542.CrossRefGoogle ScholarPubMed
Moloo, S. K. (1983). Feeding behaviour of Glossina morsitans morsitans infected with Trypanosoma vivax, T. congolense or T. brucei. Parasitology 86, 5156.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Lensen, A. H. W., Van Gemert, G. F. A., Bolmer, J. H. E. & Meuwissen, J. H. E. T. (1991). Feeding behaviour and sporozoite ejection by infected Anopheles stephensi. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 175180.CrossRefGoogle ScholarPubMed
Randolph, S. E. & Nuttall, P. A. (1994) Nearly right or precisely wrong? Natural versus laboratory studies of vector-borne diseases. Parasitology Today 10, 458462.CrossRefGoogle ScholarPubMed
Rosenberg, R., Wirtz, R. A., Schneider, I. & Burge, R. (1990). An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Transactions of the Royal Society Tropical Medicine and Hygiene 84, 209212.CrossRefGoogle ScholarPubMed
Rossignol, P. A. & Mackay, Rossignol A. (1988). Simulations of enhanced malaria transmission and host bias by modified vector blood location behaviour. Parasitology 97, 363372.CrossRefGoogle ScholarPubMed
Rossignol, P. A., Ribeiro, J. M. C. & Spielman, A. (1984). Increased intradermal probing time in sporozoite- infected mosquitoes. American Journal of Tropical Medicine and Hygiene 33, 1720.CrossRefGoogle ScholarPubMed
Rossignol, P. A., Ribeiro, J. M. C. & Spielman, A. (1986). Increased biting-rate and reduced fertility in sporozoite-infected mosquitoes. American Journal of Tropical Medicine and Hygiene 35, 277279.CrossRefGoogle ScholarPubMed
Schaub, G. A. (1992). The effects of trypanosomatids on insects. Advances in Parasitology 31, 255319.CrossRefGoogle ScholarPubMed
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. San Francisco: W. H. Freeman and Company.Google Scholar
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford: Oxford University Press.Google Scholar
Wekesa, J. W., Copeland, R. S. & Mwangi, R. W. (1992). Effect of Plasmodium falciparum on blood-feeding behaviour of naturally infected Anopheles mosquitoes in western Kenya. American Journal of Tropical Medicine and Hygiene 47, 484488.CrossRefGoogle ScholarPubMed
Wheeler, C. M. & Douglas, J. R. (1941). Transmission Studies of sylvatic plague. Proceedings of the Society of Experimental Biology and Medicine 47, 6566.CrossRefGoogle Scholar
Wirtz, R. A., Burkot, T. R., Andre, R. G., Rosenberg, R., Collins, w. E. & Roberts, D. R. (1985). Identification of Plasmodium vivax sporozoites in mosquitoes using enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 34, 10481054CrossRefGoogle ScholarPubMed