Audio and 3D flight-track recordings of mosquito responses to opposite-sex sound-stimuli

Roux

Journal of Experimental Biology

2022

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Mosquitoes of many species mate in station-keeping swarms. Mating chases ensue as soon as a male detects the flight tones of a female with his auditory organs. Previous studies of hearing thresholds have mainly used electrophysiological methods that prevent the mosquito from flying naturally. The main aim of this study was to quantify behaviourally the sound-level threshold at which males can hear females. Free-flying male Anopheles coluzzii were released in a large arena (∼2 m high x 2 m x 1 m) with a conspicuous object on the ground that stimulates swarming behaviour. Males were exposed to a range of natural and synthetic played-back sounds of female flight. We monitored the responses of males and their distance to the speaker by recording changes in their wingbeat frequency and angular speed. We show that the mean male behavioural threshold of particle-velocity hearing lies between 13-20 dB SVL (95%-CI). A conservative estimate of 20 dB SVL (i.e.,<0.5 µm/s particle velocity) is already 12 to 26 dB lower than most of the published electrophysiological measurements from the Johnston's organ. In addition, we suggest that 1) the first harmonic of female flight-sound is sufficient for males to detect her presence, 2) males respond with a greater amplitude to single-female sounds than to the sound of a group of females and 3) the response of males to the playback of the flight sound of a live female is the same as that of a recorded sound of constant frequency and amplitude.

Section: Competing Interestsmentioning

confidence: 99%

Behavioural analysis of swarming mosquitoes reveals high hearing sensitivity in Anopheles coluzzii

Roux

Journal of Experimental Biology

2022

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“…Raw response files (sound and tracked flight trajectories) are available at: https://doi.org/10.5061/dryad.9cnp5hqhj (Feugère et al, 2021a). Sound stimuli (Audio S1 to S4), as well as the original sound recordings (Audio S5, Audio S6) are available as supplementary material.…”

Section: Competing Interestsmentioning

confidence: 99%

Behavioural analysis of swarming mosquitoes reveals higher hearing sensitivity than previously measured with electrophysiology methods

Roux

2021

Preprint

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Background: Male and female mosquitoes of many species mate in swarms consisting of males and uninseminated females; males form station-keeping swarms and mating chases ensue as soon as a male detects the flight tones of a female. The auditory organs of mosquitoes have been reported to be the most sensitive among arthropods, enabling them to track their flying mate by the sound of the female's flight tones during mating chases. Previous studies on hearing thresholds have mainly used electrophysiological methods, which unfortunately limit the natural behaviour of the mosquitoes. This study explores male auditory behavioural sensitivity to female flight tones. Methods: We developed a behavioural method for measuring hearing sensitivity in swarming male mosquitoes. Free-flying male Anopheles coluzzii mosquitoes were released in a large arena (~2 m high x 2 m x 1 m) with a visually conspicuous object on the ground that stimulates swarming behaviour consisting of elliptical flight pattern over the object. Males were exposed to a range of natural and synthetic played-back sounds of female flight emanating from a speaker located at the same height as the swarm centre and 0.9 m away from it. We monitored the responses of males to female sound by recording the flight-tone and flight-dynamic responses of males. Calibrated sound-levels were measured at the swarm centre; the changing distances between the speaker and the flying males as well as other measurement uncertainties were taken into account to estimate the sound levels that males were effectively exposed to. Results: We show that the mean male behavioural threshold of particle-velocity hearing lies between 13-20 dB SVL (95%-CI). A conservative estimate of 20 dB SVL (i.e., less than a particle velocity of 0.5e-6 m/s) is already 12 to 26 dB less than most of the published electrophysiological measurements on Johnston's organ sensilla. Our results confirm, under laboratory conditions, the high behavioural hearing-sensitivity of swarming mosquitoes recently found with swarming Aedes communis in the field, and suggest a hearing threshold at least two times lower than that of published results (26 dB SVL or 1e-6 m/s particle-velocity). In addition, we established that 1) the first harmonic of Anopheles coluzzii female flight sound is sufficient for males to detect her presence, 2) males respond with a greater amplitude to single-female sounds than to group-female sounds and 3) males respond to the playback of single-female sound as much as to pure-sound at a constant frequency and amplitude.

Mosquito sound communication: are male swarms loud enough to attract females?

Manoukis

et al. 2020

Preprint

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SUMMARYThe high-pitched whine of mosquitoes in flight is produced by their wingbeats, and is heard by conspecifics, who have unsurpassed sound sensitivity among arthropods. We investigated whether female mosquitoes might use the sound of a mating swarm at long-range (several meters) to identify species-specific cues. In the laboratory we exposed free-flying An. coluzzii females to pre-recorded male An. coluzzii and An. gambiae s.s. swarms to assess female response to male flight sounds over a range of ecologically-relevant sound-levels, based on our reference recording (70-male swarm producing 20 dB SPL 0.9m away). Sound-levels tested were related to equivalent distances between the female and the male swarm for a given number of males, enabling us to infer distances over which females can hear large male swarms. Females did not respond to swarm sounds at 36±3 dB, but their flight speed increased significantly at 48±3 dB, equivalent to a distance of 0.6±0.2 m from a point-source swarm-sound produced by 1,000 males. However, this distance is less than the 1,000-male swarm radius. We show that even for the loudest swarms of 10,000 males, a female will hear an individual male at the edge of the swarm sooner or more loudly than the swarm as a whole, due to the exponential increase of sound at close-range. Therefore, females highly unlikely cannot use swarm sound to locate swarms at long-range. We conclude that mosquito acoustic communication is restricted to close-range dyad interactions.