Chicken volatiles repel host-seeking malaria mosquitoes

Abstract

Background: Anopheles arabiensis is a dominant vector of malaria in sub-Saharan Africa, which feeds indoors and outdoors on human and other vertebrate hosts, making it a difficult species to control with existing control methods. Novel methods that reduce human-vector interactions are, therefore, required to improve the impact of vector control programmes. Investigating the mechanisms underlying the host discrimination process in An. arabiensis could provide valuable knowledge leading to the development of novel control technologies. In this study, a host census and blood meal analysis were conducted to determine the host selection behaviour of An. arabiensis. Since mosquitoes select and discriminate among hosts primarily using olfaction, the volatile headspace of the preferred non-human host and non-host species, were collected. Using combined gas chromatography and electroantennographic detection analysis followed by combined gas chromatography and mass spectrometry, the bioactive compounds in the headspace collections were identified. The efficiency of the identified non-host compounds to repel host-seeking malaria mosquitoes was tested under field conditions.

Results: The host census and blood meal analyses demonstrated that An. arabiensis strongly prefers human blood when host seeking indoors, while it randomly feeds on cattle, goats and sheep when found outdoors. However, An. arabiensis avoids chickens despite their relatively high abundance, indicating that chickens are a non-host species for this vector. Eleven bioactive compounds were found in the headspace of the non-host species. Six of these were species-specific, out of which four were identified using combined gas chromatography and mass spectrometry. When tested in the field, the chicken-specific compounds, isobutyl butyrate, naphthalene, hexadecane and trans-limonene oxide, and the generic host compounds, limonene, cis-limonene oxide and β-myrcene, significantly reduced trap catches within the house compared to a negative control. A significant reduction in trap catch was also observed when suspending a caged chicken next to the trap.

Conclusions: Non-host volatiles repel host-seeking An. arabiensis and thus play a significant role in host discrimination. As such, this study demonstrates that non-host volatiles can provide protection to humans at risk of mosquito-vectored diseases in combination with established control programmes.

Keywords: Anopheles arabiensis; Blood meal analysis; Host discrimination; Host species abundance; Non-host volatiles.

Fig. 1

CDC suction traps used in the field experiment were placed at the foot of a bed with a volunteer sleeping under a bed net. Dispenser vials, releasing test compounds at a rate of 1 mg h⁻¹, were suspended next to the traps (a). As a control, a live caged chicken was used in lieu of the dispenser (b)

Fig. 2

The mean number (±SEM) of host-seeking Anopheles arabiensis caught in CDC suction traps baited with synthetic chicken-specific (hatched bars) and generic (solid bars) host compounds or a live chicken (hatched bar) compared to a CDC control trap (open bar). The mean mosquito catches per treatment sharing the same letter designation are not significantly different from one another (generalized linear model; P > 0.05)