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Spatial and temporal characteristics of laboratory-induced Anopheles coluzzii swarms: shape, structure and flight kinematics

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Oct 11, 2024 version files 12.65 MB

Abstract

Anopheles mosquitoes mate at sunset in aerial swarms formed by males near a visual ground marker, and where females come into to find a mate. However, the process of how swarms are formed and maintained remains poorly understood. In the context of effective malaria vector control, the development of mating-based control methods such as sterile, incompatible, or genetically modified insect techniques, require a good knowledge of the flight behaviour of Anopheles gambiae s.l. in mating swarms. Here, we used a stereoscopic videography-based tracking system, to study the flight behaviour of swarming Anopheles coluzzii males under laboratory conditions. Using this approach, we characterized the three-dimensional spatial and temporal flight kinematics of male mosquitoes swarming above a visual ground marker. We observed that the location, shape, and volume of swarms were highly stereotypic, consistent over the duration of the swarming activity, regardless the number of individuals in the swarm. In contrast, the distance to the nearest neighbour in the swarm did vary with decreased with swarm size, as it reduced on average 7 mm per mosquito recruited into the swarm, and was thus minimal at peak swarming (~10 cm). Regardless of swarm size, the stereotypic mosquito swarm has an elliptical cone shape, with the major and minor ellipse axes perpendicular and parallel to the sunset horizon, respectively. More precisely, we found that swarm width and flight speeds in the swarm were 1.7 and 1.6 times higher perpendicular to the sunset horizon than parallel to it, respectively. Using a sensory system-informed model, we show that swarm location and shape can accurately be modelled on visual perception of the ground marker. To control swarm height, swarming individuals maintain an optical angle of the marker ranging from 24° to 55°. Limiting the deviation of the viewing angle to 4.5% of the maximum value at a given height, results in the elliptical cone swarm shape. Based on these experimental and modelling results, we discuss the implications of these finding in mating success, speciation and for vector control.