Moment-to-moment flight manoeuvres of the female yellow fever mosquito (Aedes aegyptiL.) in response to plumes of carbon dioxide and human skin odour

Abstract

Odours are crucial cues enabling female mosquitoes to orient to prospective hosts. However, their in-flight manoeuvres to host odours are virtually unknown. Here we analyzed in 3-D the video records of female Aedes aegypti mosquitoes flying in a wind tunnel in response to host odour plumes that differed in spatial structure and composition. Following a brief (~0.03 s) encounter with CO(2), mosquitoes surged upwind and, in the absence of further encounters, counterturned without displacing upwind. These patterns resemble moth responses to encounter and loss of a filament of pheromone. Moreover, CO(2) encounters induced a highly regular pattern of counterturning across the windline in the horizontal (crosswind) and vertical planes, causing the mosquito to transect repeatedly the area where CO(2) was previously detected. However, despite the rapid changes across all three axes following an encounter with CO(2), the angular velocities remained remarkably constant. This suggests that during these CO(2)-induced surges mosquitoes stabilize flight through sensors, such as the halteres and Johnston organs, sensitive to Coriolis forces. In contrast to the instantaneous responses of the mosquito CO(2), a brief encounter with a filament of human skin odour did not induce a consistent change in mosquito flight. These differential responses were reflected in further experiments with broad plumes. A broad homogeneous plume of skin odour induced rapid upwind flight and source finding, whereas a broad filamentous plume of skin odour lowered activation rates, kinetic responses and source finding compared with homogeneous plumes. Apparently, yellow fever mosquitoes need longer continuous exposure to complex skin-odour blends to induce activation and source finding.

Mosquitoes Use Vision to Associate Odor Plumes with Thermal Targets

“…In control experiments, in which we injected clean air instead of CO 2 , the female mosquitoes did not exhibit plume-tracking behavior (Figures 1c and 2a, Figure S1). In the presence of the CO 2 plume, the female mosquitoes showed stereotypical cast and surge behavior in response to CO 2 concentrations greater than 500–600 ppm (Figure S2), as has been reported previously [11, 18]. …”

“…This is particularly apparent for mosquitoes, which use a combination of olfactory, visual, and thermal cues to locate hosts [6–10]. Mosquitoes are thought to detect suitable hosts by the presence of a sparse CO 2 plume, which they track by surging upwind and casting crosswind [11]. Upon approach, local cues such as heat and skin volatiles help them identify a landing site [12–15].…”

Impact of elevated CO2 background levels on the host-seeking behaviour of Aedes aegypti

“…Carbon dioxide activates and modulates the host-seeking behaviour of insects, including mosquitoes, in a concentration-dependent manner (Dekker et al, 2001;Guerenstein and Hildebrand, 2008;Dekker and Cardé, 2011). We have shown that a transient elevation of the background level of CO 2 significantly affects the behavioural response of the mosquitoes.…”

Reception of odors and repellents in mosquitoes

“…When a female mosquito in flight or resting on a walls inside a house comes in contact with a turbulent plume of CO 2 , she immediately turns upwind and increases speed or takes off in a process described as activation [12]. The CO 2 -receptor (Gr1, Gr2, Gr3) in the cpA neurons of the maxillary palps also detects whole-skin odor weakly [13], so when a female Aedes aegypti enters a plume of undiluted skin odor, she turns upwind and increases flight speed just as she does in a plume of CO 2 [12,14].…”

“…The CO 2 -receptor (Gr1, Gr2, Gr3) in the cpA neurons of the maxillary palps also detects whole-skin odor weakly [13], so when a female Aedes aegypti enters a plume of undiluted skin odor, she turns upwind and increases flight speed just as she does in a plume of CO 2 [12,14]. Diluted skin odor however is not sufficient to activate a mosquito or induce an upwind surge however it is highly attractive after a mosquito is activated by a momentary pulse of CO 2 , through mechanisms that are not well understood [12,14]. After activating upwind navigation the mosquito surges forward every time it contacts a CO 2 plume, closer towards the emitting source, and when contact is lost she casts across the direction of airflow maximizing chances of encountering another plume from the source [12].…”