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The impact of variations in temperature on early Plasmodium falciparum development in Anopheles stephensi

Published online by Cambridge University Press:  06 April 2009

B. H. Noden ,
M. D. Kent  and
J. C. Beier
B. H. Noden
Affiliation:
Department of Molecular Microbiology and Immunology, School of Hygiene and Public Health, The Johns Hopkins University, 615 N. Wolfe St, Baltimore, MD 21205, USA
M. D. Kent
Affiliation:
Department of Molecular Microbiology and Immunology, School of Hygiene and Public Health, The Johns Hopkins University, 615 N. Wolfe St, Baltimore, MD 21205, USA
J. C. Beier
Affiliation:
Department of Molecular Microbiology and Immunology, School of Hygiene and Public Health, The Johns Hopkins University, 615 N. Wolfe St, Baltimore, MD 21205, USA
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Summary

The effect of temperature on early Plasmodium falciparum development was examined in Anopheles stephensi. The rates of both ookinete development and bloodmeal digestion were lengthened as temperatures decreased from 27 to 21 °. However, low temperatures (21–27 °) did not significantly influence infection rates or densities of either ookinetes or oocysts. In contrast, high temperatures (30 and 32 °) significantly impacted parasite densities and infection rates by interfering with developmental processes occurring between parasite fertilization and ookinete formation, especially during zygote and early ookinete maturation. This study demonstrates clearly that temperature affects the sporogonic development of P. falciparum in anophelines by altering the kinetics of ookinete maturation. These studies not only confirm the ookinete as the key development stage affecting the probability of vector infectivity, they provide new insights into the epidemiology of P. falciparum infections.

Keywords

Anopheles stephensiPlasmodium falciparumsporogonytemperature
Type
Research Article
Information
Parasitology , Volume 111 , Issue 5 , December 1995 , pp. 539 - 545
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Andrewartha, H. G. & Birch, L. C. (1954). The Distribution and Abundance of Animals. Chicago: University of Chicago Press.Google Scholar
Ball, C. H. & Chao, J. (1964). Temperature stresses on the mosquito phase of Plasmodium relictum. Journal of Parasitology 50, 748–52.CrossRefGoogle ScholarPubMed
Beier, J. C., Copeland, R. S., Mtalib, R. & Valghan, J. A. (1992). Ookinete rates in afrotropical anopheline mosquitoes as a measure of human malaria infectiousness. American Journal of Tropical Medicine and Hygiene 47, 41–6.CrossRefGoogle ScholarPubMed
Billincsley, P. F. & Hecker, H. (1991). Blood digestion in the mosquito, Anopheles stephensi Listen (Diptera: Culicidae): activity and distribution of trypsin, aminopeptidase, and α-glucosidase in the midgut. Journal of Medical Entomology 28, 865–71.CrossRefGoogle Scholar
Boyd, M. F. (1949). Epidemiology: factors related to the definitive host. In Malariology (ed. Boyd, M. F.), pp. 608–697. Philadelphia: W. B. Saunders.Google Scholar
Briegel, H. & Lea, A. O. (1975). Relationship between protein and proteolytic activity in the midgut of mosquitoes. Journal of Insect Physiology 21, 1597–604.CrossRefGoogle ScholarPubMed
Chao, J. & Ball, G. H. (1962). The effect of low temperature on Plasmodium relictum in Culex tarsalis. Journal of Parasitology 48, 252–4.CrossRefGoogle ScholarPubMed
Davidson, J. (1944). On the relationship between temperature and rate of development of insects at constant temperatures. Journal of Animal Ecology 13, 26–38.CrossRefGoogle Scholar
Detinova, T. S. (1962). Age-Grouping Methods in Diptera of Medical Importance. WHO monograph series No. 47. Geneva: WHO.Google ScholarPubMed
Gass, R. F. & Yeates, R. A. (1979). In vitro damage of cultured ookinetes of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Tropica 36, 243–52.Google ScholarPubMed
Loevinsohn, M. E. (1994). Climatic warming and increased malaria incidence in Rwanda. Lancet 343, 714–18.CrossRefGoogle ScholarPubMed
Macdonald, G. (1957). The Epidemiology and Control of Malaria. London: Oxford University Press.Google Scholar
Martens, W. J. M., Rotmans, J. & Niessen, L. W. (1994). Climate Change and Malaria Risk: an Integrated Modelling Approach. Global Dynamics and Sustainable Development Programme, GLOBO Report Series no. 3, National Institute of Public Health and Environmental Protection, RIVM report no. 4615020003, Bilthoven, The Netherlands.Google Scholar
Mitzmain, M. B. (1917). The malaria parasite in the mosquito. Public Health Report 32, 1400–13.CrossRefGoogle Scholar
Noden, B. H., Beadle, P. S., Vaughan, J. A., Pumpuni, C. B., Kent, M. D. & Beier, J. C. (1994). Plasmodium falciparum: the population structure of mature gametocyte cultures has little effect on their innate fertility. Acta Tropica 58, 13–19.CrossRefGoogle ScholarPubMed
Ogwan'g, R. A., Mwangi, J. K., Githure, J., Were, J. B. O., Roberts, C. R. & Martin, S. K. (1993). Factors affecting exflagellation of in vitro-cultivated Plasmodium falciparum gametocytes. American Journal of Tropical Medicine and Hygiene 49, 25–39.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Meuwissen, J. H. E. TH., Leeuwenberg, A. D. E. M., Verhave, J. P. & Lenen, A. H. W. (1982). The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 242–50.CrossRefGoogle ScholarPubMed
Shahabuddin, M., Criscio, M. & Kaslow, D. C. (1995). Unique specificity of in vitro inhibition of mosquito midgut trypsin-like activity correlates with in vitro inhibition of malaria parasite infectivity. Experimental Parasitology 80, 212–19.CrossRefGoogle ScholarPubMed
Shahabuddin, M. & Kaslow, D. C. (1994). Plasmodium: parasite chitinase and its role in malaria transmission. Experimental Parasitology 79, 85–8.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1984). The biology of Plasmodium in the mosquito. Experientia 40, 1330–43.CrossRefGoogle ScholarPubMed
Sinden, R. E. & Hartley, R. H. (1985). Identification of the meiotic division of malarial parasites. Journal of Protozoology 32, 742–4.CrossRefGoogle ScholarPubMed
Southwood, T. R. E. (1978). Ecological Methods. New York: John Wiley & Sons.Google Scholar
Stone, R. (1995). If the mercury rises, so may health hazards. Science 267, 957–8.CrossRefGoogle Scholar
Stratman-Thomas, W. K. (1940). The influence of temperature on Plasmodium vivax. American Journal of Tropical Medicine 20, 703–15.Google Scholar
Vanderberg, J. P. & Yoeli, M. (1966). Effects of temperature on sporogonic development of Plasmodium berghei. Journal of Parasitology 52, 559–64.CrossRefGoogle ScholarPubMed
Varley, G. C., Gradwell, G. R. & Hassell, M. P. (1973). Insect Population Ecology: an Analytical Approach. Berkeley: University of California Press.Google Scholar
Vaughan, J. A., Noden, B. H. & Beier, J. C. (1992). Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. Journal of Parasitology 78, 716–24.CrossRefGoogle ScholarPubMed
Vaughan, J. A., Noden, B. H. & Beier, J. C. (1994). Sporogonic development of cultured Plasmodium falciparum in six species of laboratory-reared Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 233–43.CrossRefGoogle ScholarPubMed