Aedes vector-host olfactory interactions in sylvatic and domestic dengue transmission environments

Abstract

Interactions between Aedes (Stegomyia) species and non-human primate (NHP) and human hosts govern the transmission of the pathogens, dengue, zika, yellow fever and chikungunya viruses. Little is known about Aedes mosquito olfactory interactions with these hosts in the domestic and sylvatic cycles where these viruses circulate. Here, we explore how the different host-derived skin odours influence Aedes mosquito responses in these two environments. In field assays, we show that the cyclic ketone cyclohexanone is a signature cue for Aedes mosquitoes to detect the NHP baboon, sykes and vervet, whereas for humans, it is the unsaturated aliphatic keto-analogue 6-methyl-5-hepten-2-one (sulcatone). We find that in the sylvatic environment, CO₂-baited traps combined with either cyclohexanone or sulcatone increased trap catches of Aedes mosquitoes compared to traps either baited with CO₂ alone or CO₂ combined with NHP- or human-derived crude skin odours. In the domestic environment, each of these odourants and crude human skin odours increased Aedes aegypti catches in CO₂-baited traps. These results expand our knowledge on the role of host odours in the ecologies of Aedes mosquitoes, and the likelihood of associated spread of pathogens between primates and humans. Both cyclohexanone and sulcatone have potential practical applications as lures for monitoring Aedes disease vectors.

Keywords: Aedes (Stegomyia) mosquitoes; cyclohexanone; non-human primate; skin odours; sulcatone; sylvatic and domestic environments.

Figure 1.

Mosquito abundance pattern in crude NHP and human skin odours in the sylvatic environment. (a) Aedes chaussieri abundance, (b) Ae. aegypti abundance and (c) Ae. pembaensis abundance. Boundaries of the dot plot whiskers represent the minimum and maximum of all the count data; closed dots represent data points and those outside the boundaries are outliers; replicate values as open dots are also indicated for each treatment; black bars represent the median number of catches; **significance at p < 0.01 from the control (CO₂ only); n.s. denotes non-significance from the control at p < 0.05; the host odours comprised skin volatiles trapped on cotton material (NHPs) or worn socks (humans); number of replicates, n = 24. All treatments were less attractive than the control. (Online version in colour.)

Figure 2.

Representative GC–EAD profiles using adult female Ae. aegypti to (a) baboon, (b) vervet, (c) sykes and (d) human, odours. Upper traces are flame ionization detector (chemical profile) of the respective host odours and lower traces are EAD responses; number of runs, n = 3; scale bar in all the GC–EAD runs, 5 mV div; red asterisks are unidentified compounds. (Online version in colour.)

Figure 3.

Comparison in mosquito abundance pattern in NHP and human signature cues and their crude skin odours in the sylvatic environment. (a) Aedes chaussieri abundance, (b) Ae. cumminsii abundance and (c) Ae. pembaensis abundance. Boundaries of the dot plot whiskers represent the minimum and maximum of all the count data; closed dots represent data points and those outside the boundaries are outliers; replicate values as open dots are also indicated for each treatment; black bars represent the median number of catches; *,** significance at p < 0.05 and p < 0.01, respectively, from the control (CO₂ only); the host odours comprised skin volatiles trapped on cotton material (NHPs) or worn socks (humans); number of replicates, n = 14. Sulcatone 1 mg ml⁻¹ (sulca1), sulcatone 0.1 mg ml⁻¹ (sulca0.1), sulcatone 0.01 mg ml⁻¹ (sulca0.01), cyclohexanone 2 mg ml⁻¹ (cyclo2), cyclohexanone 0.2 mg ml⁻¹ (cyclo0.2), cyclohexanone 0.02 mg ml⁻¹ (cyclo0.02), CS (a blend of cyclohexanone and sulcatone at optimum doses of 0.2 mg ml⁻¹ and 0.1 mg ml⁻¹, respectively). (Online version in colour.)

Figure 4.

Aedes aegypti abundance pattern in NHP and human signature cues and human-scented socks in the domestic environment. Boundaries of the dot plot whiskers represent the minimum and maximum of all the count data; closed dots represent data points and those outside the boundaries are outliers; replicate values as open dots are also indicated for each treatment; black bars represent the median number of catches; *, ** significance at p < 0.05 and p < 0.01, respectively, from the control (CO₂ only); human odours comprised skin volatiles trapped on worn socks; number of replicates, n = 12. Sulcatone 1 mg ml⁻¹ (sulca1), sulcatone 0.1 mg ml⁻¹ (sulca0.1), sulcatone 0.01 mg ml⁻¹ (sulca0.01), cyclohexanone 2 mg ml⁻¹ (cyclo2), cyclohexanone 0.2 mg ml⁻¹ (cyclo0.2), cyclohexanone 0.02 mg ml⁻¹ (cyclo0.02), CS (a blend of cyclohexanone and sulcatone at optimum doses of 0.2 mg ml⁻¹ and 0.1 mg ml⁻¹, respectively). (Online version in colour.)