Abstract

Behavioral responses of the malaria mosquito Anopheles coluzzii (An. gambiae sensu stricto molecular ‘M form’) to an expanded blend of human-derived volatiles were assessed in a dual-port olfactometer. A previously documented attractive three-component blend consisting of NH3, (S)-lactic acid, and tetradecanoic acid served as the basis for expansion. Adding 4.5 % CO2 to the basic blend significantly enhanced its attractiveness. Expansion of the blend with four human-derived C4-volatiles was then assessed, both with and without CO2. Only when CO2 was offered simultaneously, did addition of a specific concentration of 3-methyl-1-butanol or 3-methyl-butanoic acid significantly enhance attraction. The functional group at the terminal C of the 3-methyl-substituted C4 compounds influenced behavioral effectiveness. In the absence of CO2, addition of three concentrations of butan-1-amine caused inhibition when added to the basic blend. In contrast, when CO2 was added, butan-1-amine added to the basic blend strongly enhanced attraction at all five concentrations tested, the lowest being 100,000 times diluted. The reversal of inhibition to attraction by adding CO2 is unique in the class Insecta. We subsequently augmented the three-component basic blend by adding both butan-1-amine and 3-methyl-1-butanol and optimizing their concentrations in the presence of CO2 in order to significantly enhance the attractiveness to An. coluzzii compared to the three- and four-component blends. This novel blend holds potential to enhance malaria vector control based on behavioral disruption.

Highlights

  • Mosquitoes belong to a group of blood-feeding insects that contribute to transmission of serious infectious diseases like dengue, malaria, chikungunya, and Rift Valley fever

  • We re-assessed the role of carbon dioxide in attraction of the African malaria mosquito An. coluzzii Coetzee & Wilkerson sp. n. to odor blends composed of C4-compounds, which have previously been reported to be attractive or inhibitory in the absence of carbon dioxide (Smallegange et al 2012; Verhulst et al 2011a). This finding led us to augment the three-component blend of ammonia, lactic acid, and tetradecanoic acid that we reported before as an effective kairomone blend mimicking the attraction of human subjects (Smallegange et al 2009, 2012) with butan-1-amine and 3methyl-1-butanol, a volatile produced by microbiota on the human skin (Verhulst et al 2009, 2011a)

  • When the basic blend was prepared with 0.01 % 3-methyl-1-butanol, the addition of 0.01, 0.004, or 0.001 % butan-1-amine resulted in higher trap catches (χ2-test, P≤0.001)

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Summary

Introduction

Mosquitoes belong to a group of blood-feeding insects that contribute to transmission of serious infectious diseases like dengue, malaria, chikungunya, and Rift Valley fever. Malaria mosquitoes in the genus Anopheles are the most important species because of their high prevalence and incidence of infection with malaria parasites, Plasmodium spp. Anopheline mosquitoes feed on humans as blood hosts, enabling the transmission of Plasmodium parasites from infected to uninfected hosts. Vector-host contact is achieved through chemoreception of volatile cues emitted by the blood host (Zwiebel and Takken 2004). Host volatiles are perceived by olfactory organs located on the head of the mosquito, in particular the antennae and maxillary palps (Qiu and Van Loon 2010).

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