Attraction of mosquitoes to primate odours and implications for zoonotic Plasmodium transmission

Abstract

Vector-borne diseases often originate from wildlife and can spill over into the human population. One of the most important determinants of vector-borne disease transmission is the host preference of mosquitoes. Mosquitoes with a specialised host preference are guided by body odours to find their hosts in addition to carbon dioxide. Little is known about the role of mosquito host preference in the spillover of pathogenic agents from humans towards animals and vice versa. In the Republic of Congo, the attraction of mosquitoes to primate host odours was determined, as well as their possible role as malaria vectors, using odour-baited traps mimicking the potential hosts of mosquitoes. Most of the mosquito species caught showed a generalistic host preference. Anopheles obscurus was the most abundant Anopheles mosquito, with a generalistic host preference observed from the olfactory response and the detection of various Plasmodium parasites. Interestingly, Culex decens showed a much higher attraction towards chimpanzee odours than to human or cow odours. Human Plasmodium parasites were observed in both human and chimpanzee blood, although not in the Anopheles mosquitoes that were collected. Understanding the role of mosquito host preference for cross-species parasite transmission provides information that will help to determine the risk of spillover of vector-borne diseases.

Keywords: Anopheles; Congo; Plasmodium; bridge vectors; chimpanzee; mosquito host preference; transmission dynamics.

Figure 1

Trapping efficiency of two odour‐baited mosquito traps. Back‐transformed mean proportion [generalized linear model (GLM)] of caught mosquitoes per trap using the BG‐Sentinel (BGS) trap (n = 15) and the Suna trap (n = 15) baited with the five‐component odour blend odour blend (Menger et al., 2014) and CO₂. Numbers in the bars indicate the total number of mosquito spp. (A) and Anopheles spp. (B) trapped. Error bars represent the SEM. Location effect was significant for both total mosquito spp. and total Anopheles spp. and included in the GLM (P < 0.001). [Colour figure can be viewed at http://wileyonlinelibrary.com].

Figure 2

Attraction of mosquito species to different host odours trapped with odour baited Suna traps. Back‐transformed mean proportion [generalized linear model (GLM)] of mosquito genera caught using different host odour treatments: no odours, CO₂ only, chimpanzee odours with CO₂, human odours with CO₂ and cow odours with CO₂. Error bars represent the SEM. Numbers below the bars indicate the total number of mosquitoes caught per species (n = 35 trapping nights). Different uppercase letters indicate significant differences between odour baits within each genus (GLM with least significant difference post‐hoc test, P < 0.05). NS, non‐significant (P > 0.05). [Colour figure can be viewed at http://wileyonlinelibrary.com].

Figure 3

Evolutionary relationships of Plasmodium parasite sequences from chimpanzees and humans. A maximum likelihood tree of mitochondrial cytochrome b (cytB) sequences (956 bp) is shown. Sequences in green represent the Plasmodium sequences found in chimpanzee (Chimpanzee 1 and 2) and human (Human 1) blood samples. Sequences in white represent Plasmodiidae sequences obtained from Anopheles mosquitoes. Black sequences represent Plasmodium reference sequences. Coloured blocks indicate primate (yellow), bird and reptile (brown), and ungulate (purple) reference sequences. Bootstrap values (≥ 70%) are shown above and below the branch nodes. The scale bar represents 0.03 nucleotide substitutions per site. [Colour figure can be viewed at http://wileyonlinelibrary.com].