Mosquitoes Use Vision to Associate Odor Plumes with Thermal Targets

Abstract

All moving animals, including flies [1, 2 and 3], sharks [4], and humans [5], experience a dynamic sensory landscape that is a function of both their trajectory through space and the distribution of stimuli in the environment. This is particularly apparent for mosquitoes, which use a combination of olfactory, visual, and thermal cues to locate hosts [6, 7, 8, 9 and 10]. Mosquitoes are thought to detect suitable hosts by the presence of a sparse CO2 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, 13, 14 and 15]. Recent evidence suggests that thermal attraction is gated by the presence of CO2 [6], although this conclusion was based experiments in which the actual flight trajectories of the animals were unknown and visual cues were not studied. Using a three-dimensional tracking system, we show that rather than gating heat sensing, the detection of CO2 actually activates a strong attraction to visual features. This visual reflex guides the mosquitoes to potential hosts where they are close enough to detect thermal cues. By experimentally decoupling the olfactory, visual, and thermal cues, we show that the motor reactions to these stimuli are independently controlled. Given that humans become visible to mosquitoes at a distance of 5–15 m [16], visual cues play a critical intermediate role in host localization by coupling long-range plume tracking to behaviors that require short-range cues. Rather than direct neural coupling, the separate sensory-motor reflexes are linked as a result of the interaction between the animal's reactions and the spatial structure of the stimuli in the environment.

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