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

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.