Identification of candidate volatiles that affect the behavioural response of the malaria mosquitoAnopheles gambiae sensu strictoto an active kairomone blend: laboratory and semi‐field assays

Abstract

Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is the most important vector of human malaria in sub‐Saharan Africa, affecting the lives of millions of people. Existing tools such as insecticide‐treated nets and indoor‐residual sprays are not only effective, but also have limitations as a result of the development of resistance to insecticides and behavioural adaptations in biting time. Therefore, novel mosquito‐control tools are needed. Odour‐releasing traps have a potential for both trapping and surveillance purposes. Based on the outcome of ex vivo gene expression assays and in vivo electrophysiological assays on hundreds of volatile organic compounds, 29 ‘candidate behaviourally‐disruptive organic compounds' (cBDOCs) are selected, belonging to 10 chemical categories, to be assayed in the laboratory using dual‐choice olfactometers for the ability to modify the ‘attractiveness’ (i.e. significantly more insects being caught in the associated trap) of a basic volatile blend consisting of ammonia, lactic acid and tetradecanoic acid but without additional carbon dioxide. Compounds that either reduce or increase trap catches by the basic blend in the olfactometer experiments are tested under African conditions in choice experiments in a semi‐field facility in Kenya. The release rates of cBDOCs are determined gravimetrically to allow the calculation of aerial concentrations at the trap outlet. Aerial concentrations in the sub‐p.p.m. range are reported for the first time to influence mosquito behaviour. The results of the olfactometer and semi‐field assays generally correspond. Under semi‐field conditions, three compounds, 3‐heptanol (0.025 p.p.m.), 2‐methylpropanal (0.05 p.p.m.) and 4,5‐dimethylthiazole (0.73 p.p.m.), significantly increase trap catches relative to the basic blend consisting of ammonia, lactic acid, tetradecanoic acid and carbon dioxide. 2‐Acetylthiophene, 2‐nonanone and 2‐phenylethanol decrease the number of mosquitoes caught at all concentrations tested under semi‐field conditions. These compounds hold promise as attractants and spatial repellents to be applied in mosquito control programmes.

Mosquito Attraction: Crucial Role of Carbon Dioxide in Formulation of a Five-Component Blend of Human-Derived Volatiles

“…Mosquito rearing, preparation and the performance of the olfactometer experiments, as well as cleaning of the olfactometer parts, were done as described in Smallegange et al (2012). The air flowing into the flight chambers was maintained at a relative humidity above 70 % and had an average temperature of 26.6 ± 1.1 °C.…”

“…Recently, significant progress has been made in the identification of a number of these odorants, resulting in the creation of odor blends that are as attractive as a human host (Menger et al 2014; Mukabana et al 2012; Okumu et al 2010). These blends have been formulated during an iterative process involving molecular, physiological, and behavioral assays on anopheline mosquitoes in vitro and in vivo (Carey et al 2010; Carlson and Carey 2011; Qiu et al 2011; Rinker et al 2012; Smallegange et al 2010, 2012). …”

“…n. (renamed from An. gambiae sensu stricto molecular ‘M-form’; Coetzee et al 2013) 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 3-methyl-1-butanol, a volatile produced by microbiota on the human skin (Verhulst et al 2009, 2011a).…”

Chemosensory behaviors of parasites

“…In the case of An. gambiae , the discovery that human skin microbiota play an important role in host seeking [58] led to the finding that the addition of some skin microbiota-derived odorants enhance the effectiveness of existing traps [59, 103], and the large-scale decoding of the AgOR repertoire [77] led to the finding that some of the odorants that strongly activate AgORs can increase trap effectiveness [104]. In addition, a better understanding of insect odorant receptor function led to the finding that the broad-spectrum insect repellent DEET directly modulates the odorant receptor complex [105], paving the way for future studies aimed at designing alternative insect repellents.…”

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“…Some prefer to feed only on birds or mammals, or cold-blooded vertebrates such as reptiles and frogs. Consequently, various mosquito species use a wide variety of cues to find a suitable host, often involving a variety of complex interactions that are optimal for their host preference (Smallegange et al, 2012). The distance that mosquitoes can fly is difficult to generalize because mosquito species vary in their flight range.…”