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

Lionel Feugère,Gabriella Gibson,Nicholas C Manoukis,Olivier Roux

doi:10.1098/rsif.2021.0121

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.

Highlights

One-on-one male–female auditory interactions in mosquitoes have been shown to be related to pre-mating behaviour in at least four species of medical importance (Anopheles gambiae s.l., Anopheles albimanus, Aedes aegypti and Culex quinquefasciatus), plus Toxorhynchites brevipalpis and Culex pipiens [1,2,3,4,5,6,7,8,9,10], as well as in other dipteran flies [11]
Instead of changing the distance between the test female and the male swarm, we used a range of sound levels to mimic a range of distances between a female and swarming males, altering the apparent distance ri between the female and the sound source ‘image’ of the played-back swarm according to acoustic propagation theory
Previous studies estimated the hearing threshold of tethered An. gambiae s.l. females was in the range 44–52 dB and tethered Aedes aegypti females around 55 dB sound pressure level (SPL) (n = 10) by monitoring the activity of the Johnston’s organ nerve [4,16]

Summary

Introduction

One-on-one male–female auditory interactions in mosquitoes have been shown to be related to pre-mating behaviour in at least four species of medical importance (Anopheles gambiae s.l., Anopheles albimanus, Aedes aegypti and Culex quinquefasciatus), plus Toxorhynchites brevipalpis and Culex pipiens [1,2,3,4,5,6,7,8,9,10], as well as in other dipteran flies [11]. Species of mosquito that form mating swarms can produce a relatively loud sound, discernible to the human ear a few metres away [17], by forming relatively dense station-keeping aggregations [18], consisting of up to thousands of males [19,20,21]. This raises the hypothesis that a female can be attracted from a distance to swarm sounds produced by males in established swarms

Methods

Results

Conclusion