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

Abstract

Given the unsurpassed sound sensitivity of mosquitoes among arthropods and the sound source power required for long-range hearing, we investigated the distance over which female mosquitoes detect species-specific cues in the sound of station-keeping mating swarms. A common misunderstanding, that mosquitoes cannot hear at long range because their hearing organs are ‘particle-velocity’ receptors, has clouded the fact that particle velocity is an intrinsic component of sound whatever the distance to the sound source. We exposed free-flying Anopheles coluzzii females to pre-recorded sounds of male An. coluzzii and An. gambiae s.s. swarms over a range of natural sound levels. Sound levels tested were related to equivalent distances between the female and the swarm for a given number of males, enabling us to infer distances over which females might hear large male swarms. We show that females do not respond to swarm sound up to 48 dB sound pressure level (SPL) and that louder SPLs are not ecologically relevant for a swarm. Considering that swarms are the only mosquito sound source that would be loud enough to be heard at long range, we conclude that inter-mosquito acoustic communication is restricted to close-range pair interactions. We also showed that the sensitivity to sound in free-flying males is much enhanced compared to that of tethered ones.

Harmonic convergence coordinates swarm mating by enhancing mate detection in the malaria mosquito Anopheles gambiae

“…Artificial flight tone stimuli have been used to examine acoustic mating behavior in mosquitoes 16 , 30 , 33 , 34 , 39 , 43 , 45 , 53 , 67 , 71 as well as in midges 80 . To further dissect acoustic mating interactions during swarming, we tested swarming male flight responses to artificial female swarm tone audio playback emitted from a speaker (Fig.…”

“…Numerous studies have reported mosquito flight tones from single, pairs, or groups of tethered adults 30 , 32 – 35 , 49 , 84 , 87 – 89 , free-flying adults 28 , 36 , 39 – 41 , 54 , 71 , 90 , or a combination of tethered and free-flying adults 15 , 25 , 29 , 43 – 46 , 51 , 52 , 67 , 72 , 85 . Fewer studies have examined mating activity in swarms 6 , 12 , 91 or performed audio recordings of swarming individuals in free flight 15 , 39 , 40 , 43 , 51 , 53 – 55 , 67 , 71 , 90 , and none prior to the present study have done so simultaneously over an entire swarm sequence. Overall, the findings presented in this study, along with other recent mosquito acoustics work 15 , 43 , 51 – 53 , 55 , 71 , underscore the importance of examining mosquito flight tones and mating activity in free-flying individuals, ideally during their swarming period.…”

“…Despite these discoveries, much of the previous work on harmonic convergence has examined tethered, rather than free-flying males and females. Although tethered flight analysis offers an experimentally tractable means of dissecting the mechanics and biological significance of this behavior, tethering can alter flight tones 15 , 25 , 48 – 52 and lower sensitivity to sound 53 by restricting natural flight patterns. Analysis on flight tone acoustics and harmonic convergence over the course of a complete swarm sequence would therefore provide valuable insights and context for these phenomena, as studies examining convergence in free-flight are limited 15 , 43 , 51 , 54 , 55 .…”

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

“…Hearing is a key sensory modality for mosquito mating; it enables males to detect females at a distance through the combined sounds of their respective flapping wings (01) (02) (03). The more sensitive males are, the further away they can hear a female and the sooner they detect and close in on a nearby female in the context of highly-competitive mating-swarms.…”

“…Indeed, male responsiveness to sound was found to be reduced when they were not flying (15). Second, Feugère et al (03) measured the flight and wingbeat frequency response of free-flying, swarming male An. coluzzii to a range of sound levels of a played-back group of females and found a response at 33±3 dB SPL.…”