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Waiting with Bated Breath: Opportunistic Orientation to Human Odor in the Malaria Mosquito, Anopheles gambiae, is Modulated by Minute Changes in Carbon Dioxide Concentration

Abstract

Females of the malaria mosquito, Anopheles gambiae, predominantly obtain blood meals within human dwellings. Being highly anthropophilic, human skin odor offers a reliable, host-specific cue, but the challenge posed by pervasive human odor found indoors from used clothing, bedding etc. remains unclear. Anopheles gambiae spends much of its adult life indoors, constantly exposed to human odor even when dwellings are unoccupied. In landing assays, we found that female mosquitoes respond very weakly to human skin odor alone, suggesting that, alone, it is an ineffective landing cue. Landing, however, was dramatically increased by addition of carbon dioxide at a range of concentrations above ambient. Indeed, this effect was seen even when carbon dioxide was just 0.015 % above ambient within the assay cage. The synergistic effect of added carbon dioxide quickly waned, thereby facilitating a highly adaptive “sit-and-wait” ambush strategy, wherein females ignore persistent human odor until a living human is present. Unexpectedly, landing rates in the presence of added carbon dioxide were almost as robust during daytime, when An. gambiae has previously been assumed inactive, possibly facilitating opportunistic feeding at times of day when human dwellings are occupied intermittently. We suggest earlier studies that showed strong upwind flight behavior toward human odor alone could, in fact, have been demonstrating orientation toward a human dwelling rather than toward a living human. This new interpretation of how human odors mediate upwind orientation and landing in An. gambiae is discussed.

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Acknowledgments

This work was funded by an R56AI099778 (National Institute of Allergy and Infectious Diseases) grant to Anandasankar Ray and Ring Cardé. The granting agencies had no role in experimental design or analysis. We are grateful to Anandasankar Ray for his comments and Bradley White for our colony of An. gambiae.

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Correspondence to Ring T. Cardé.

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Webster, B., Lacey, E.S. & Cardé, R.T. Waiting with Bated Breath: Opportunistic Orientation to Human Odor in the Malaria Mosquito, Anopheles gambiae, is Modulated by Minute Changes in Carbon Dioxide Concentration. J Chem Ecol 41, 59–66 (2015). https://doi.org/10.1007/s10886-014-0542-x

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Keywords

  • Anopheles gambiae
  • Olfaction
  • Landing
  • Behavior
  • Carbon dioxide
  • Skin odor