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Answer by Tirumalai Kamala:

This question has two aspects, first, does Plasmodium alter an infected mosquito’s feeding behavior, and if so, how?

Plasmodium alters an infected mosquito’s feeding behavior under experimental conditions. It’s difficult to generalize since different studies used different mosquito and malaria species, and examined different aspects of mosquito feeding behavior pre- and post-infection.

After taking an infectious blood meal. the most striking behavior change is between a pre-infectious (oocyst) and infectious (sporozoite; infectious for mammals) mosquito. Pre-infectious females show less attraction to hosts, are less persistent in their feeding attempts, probe less frequently and for less duration, activities that are reversed in infectious female mosquitoes, except in one case of birds and bird-specific mosquito and malaria parasite. A caveat to many of these studies is lack of matched control mosquitos.

My summation of key data from peer-reviewed publications:


How does Plasmodium induce such changes?

  1. When an infected mosquito takes a blood meal on a mammalian host, it transmits the sporozoite stage malaria parasite. How? After it develops inside the mosquito gut, the malaria sporozoite invades the salivary glands. When the infected mosquito bites to take a blood meal, it reflexively deposits a bolus of malaria sporozoites from its salivary glands. Now in the process of invading, sporozoites damage mosquito salivary glands (1). Mosquitos with damaged salivary glands have less salivary apyrase (2). Mosquitos deficient in salivary apyrase have difficulty in locating and feeding on host blood. They thus tend to probe more often and to feed on several hosts successively (1, 3, 4). One caveat to this hypothesis is that scientists have observed at least one outlier, Plasmodium berghei sporozoite invasion of the mosquito Anopheles stephensi salivary glands did not affect mosquito probing time (5).
  2. Another hypothesis is that malaria parasites manipulate infected mosquitos’ satiation threshold, making them take smaller and more frequent blood meals (6).
  3. The most recent hypothesis is that the malaria sporozoite specifically induces changes in the sensitivity of odorant receptors in the mosquito’s maxillary palps, changes that correlate with changes in the short- and long-range attraction of mosquitos to hosts (7). Supporting this hypothesis, a proteomic analysis of the head proteins in female Anopheles mosquitos infected or not with Plasmodium berghei also showed infection-specific upregulation of insect Central Nervous System (CNS) proteins (8). Unfortunately, similar changes in the sensitivity of odorant receptors were induced in the mosquito by simply injecting E. coli into it, suggesting that this pathway is not uniquely stimulated by the Plasmodium parasite alone.

Bibliography

  1. Rossignol, P. A., J. M. Ribeiro, and A. Spielman. “Increased intradermal probing time in sporozoite-infected mosquitoes.” The American journal of tropical medicine and hygiene 33.1 (1984): 17-20.
  2. Ribeiro, J. M. C., P. A. Rossignol, and A. Spielman. “Salivary gland apyrase determines probing time in anopheline mosquitoes.” Journal of insect physiology 31.9 (1985): 689-692.
  3. Rossignol, P. A., J. M. Ribeiro, and A. N. D. A. Spielman. “Increased biting rate and reduced fertility in sporozoite-infected mosquitoes.” The American journal of tropical medicine and hygiene 35.2 (1986): 277-279.
  4. Ribeiro, J. M. C., P. A. Rossignol, and A. Spielman. “Salivary gland apyrase determines probing time in anopheline mosquitoes.” Journal of insect physiology 31.9 (1985): 689-692.
  5. Li, X., Sina, B., and Rossignol, P.A.. “Probing behaviour and sporozoite delivery by Anopheles stephensi infected with Plasmodium berghei.” Medical and veterinary entomology 6.1 (1992): 57-61.
  6. Koella, Jacob C., Linda Rieu, and Richard EL Paul. “Stage-specific manipulation of a mosquito’s host-seeking behavior by the malaria parasite Plasmodium gallinaceum.” Behavioral Ecology 13.6 (2002): 816-820. Stage-specific manipulation of a mosquito’s host-seeking behavior by the malaria parasite Plasmodium gallinaceum
  7. Cator, Lauren J., et al. “‘Manipulation’without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites.” Proceedings of the Royal Society of London B: Biological Sciences 280.1763 (2013): 20130711. Page on royalsocietypublishing.org
  8. Lefevre, Thierry, et al. “Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host.” Proteomics 7.11 (2007): 1908-1915. Page on psu.edu

How does Plasmodium alter mosquito feeding habits?

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