Biology subjects

Cribellier, A.

Publications and source records attributed to Cribellier, A..

4 recordsLinked to original sources

bioRxiv2024

The complex swarming dynamics of malaria mosquitoes emerges from simple minimally-interactive behavioral rules

Swarming is a widespread collective behavior in animals, often thought to emerge from complex interactions among individuals. Here, we show that mating swarms of malaria mosquitoes can emerge from simple behavioral rules with minimal interaction between individuals. We analyzed two published experimental datasets with three-dimensional flight tracks of Anopheles coluzzii mosquitoes swarming above a visual marker under simulated sunset conditions. We found that individuals alternate between straight flight and rapid turning maneuvers known as saccades. These saccades are triggered at the edge of the swarm, and their directions are biased along the sunset direction. This behavior was found consistent between both datasets and across swarm sizes, including solitary individuals, indicating that inter-individual interactions play a limited role within the studied size range. We developed a simple agent-based model incorporating three behavioral rules: attraction to the swarm center, alignment normal to the sunset horizon, both driven by environmental cues, and repulsion through short-range collision avoidance. The model reproduced key features of natural mosquito swarms, including looping flight paths, central density peaks, and directional alignment. Even in the absence of direct inter-individual interactions, the model generated realistic emergent swarm dynamics, demonstrating that social coordination is not required for swarm emergence. Our findings suggest that mosquito swarming is primarily guided by environmental perception rather than social interaction. This minimal framework offers a new perspective on insect swarming and may apply broadly to the many other insect species that form mating swarms. Understanding these rules could inform strategies for vector control and improve the effectiveness of interventions targeting mosquito reproduction. Author SummaryMosquito swarms are a familiar sight in many parts of the world, but the rules that govern their movement have remained mysterious. In our study, we investigated how male malaria mosquitoes behave in mating swarms. Using high-speed videography and computer simulations, we discovered that these swarms do not rely on complex social interactions. Instead, each mosquito follows a few simple rules based on visual cues from the environment, like the position of the sunset and a ground marker. These rules are enough to produce the looping flight patterns and dense swarms observed in nature. Surprisingly, even a single mosquito can perform this behavior in isolation. This minimal approach challenges the idea that swarming requires strong social coordination. It also opens new possibilities for controlling malaria mosquito populations by targeting the environmental factors that influence mating behavior. Since many insects rely on swarming to reproduce, our findings may help explain similar behaviors across species and inform broader strategies for insect population management.

animal behavior and cognition↗

bioRxiv2024

Multisensory integration in Anopheles mosquito swarms: The role of visual and acoustic information in mate tracking and collision avoidance

Male mosquitoes form aerial aggregations, known as swarms, to attract females and maximize their chances of finding a mate. Within these swarms, individuals must be able to recognize potential mates and navigate the dynamic social environment to successfully intercept a mating partner. Prior research has almost exclusively focused on the role of acoustic cues in mediating the ability of male mosquitoes to recognize and pursue flying females. However, the role of other sensory modalities in this behavior has not been explored. Moreover, how males avoid collisions with one another in the dense swarm while pursuing females remains poorly understood. In this study, we combined free-flight and tethered flight simulator experiments to demonstrate that swarming Anopheles coluzzii mosquitoes integrate visual and acoustic information to track conspecifics and avoid collisions. Our tethered experiments revealed that acoustic stimuli gated mosquito steering responses to visual objects simulating nearby mosquitoes, especially in males that exhibited attraction to visual objects in the presence of female flight tones. Additionally, we observed that visual cues alone could trigger changes in wingbeat amplitude and frequency of mosquitoes. These findings were corroborated by our free-flight experiments, which revealed that mosquitoes modulate their flight responses to nearby conspecifics in a similar manner to tethered animals, allowing for collision avoidance within swarms. Together, these results demonstrate that both males and females integrate multiple sensory inputs to mediate swarming behavior, and for males, the change in flight kinematics in response to multimodal cues allows them to simultaneously track females while avoiding collisions.

neuroscience↗

bioRxiv2024

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

Anopheles mosquitoes mate at sunset in aerial swarms. The development of mating-based methods for effective malaria vector control requires a good knowledge of the flight behaviour of Anopheles species in mating swarms. However, the process of how swarms are formed and maintained remains poorly understood. Here, we characterized the three-dimensional spatial and temporal flight kinematics of Anopheles coluzzii males swarming above a ground marker. We observed that the location, shape and volume of swarms were highly stereotypic, consistent over the swarming duration, regardless of the number of individuals in the swarm. The swarm had an elliptical cone shape, and we observed a differential spatial distribution of flight kinematics parameters within the swarm volume. Among these parameters, only swarm density varied with swarm size. Using a sensory system-informed model, we show that swarm location and shape can accurately be modelled based on visual perception of the marker. To control swarm height, swarming individuals maintain an optical angle of the marker ranging from 24{degrees} to 55{degrees}. Limiting the viewing angle deviation to 4.5% of the maximum value results in the observed elliptical cone swarm shape. We discuss the implications of these finding in mating success, speciation and for vector control.

animal behavior and cognition↗

bioRxiv2023

Mosquitoes escape looming threats by actively flying with the bow-wave induced by the attacker

To detect and escape from a looming threat, night-flying insects must rely on other senses than vision alone. Nocturnal mosquitoes have been described to escape looming objects in the dark, but how they achieve this is still unknown. Here, we show how night-active female malaria mosquitoes escape from a rapidly looming object that simulates the defensive action of a blood-host. By combining videography-based automatic tracking with numerical simulations of the attacker-induced airflow, we first show that night-flying mosquitoes use airflow-sensing to detect the danger and trigger their escape. Secondly, by combining these data with mechanistic movement modelling, we unravelled how mosquitoes control their escape manoeuvres: they actively steer away from the danger, and passively travel with the bow-wave produced by the attacker. Our results demonstrate that night-flying mosquitoes escaping from a looming object use the object-induced airflow both to detect the danger, and as fluid medium to move with for avoiding collision. This shows that the escape strategy of flying insects is more complex than previous visually-induces escape flight studies suggest. As mosquitoes are average-sized insects, a combined airflow-induced and visual-induced escape strategy is expected to be common amongst millions of flying insect species. Also, our research helps explain the high escape performance of mosquitoes from counterflow-based odour-baited mosquito traps. It can therefore provide new insights for the development of novel trapping techniques for integrative vector management.

zoology↗