To escape hungry bats, these flying beetles create an ultrasound 'illusion'

MAY 22, 2024 6:00 AM ET
Ari Daniel



Harlan Gough holds a recently collected tiger beetle on a tether.
Lawrence Reeves

"Lots of things fly at night," says Harlan Gough, a wildlife biologist with the U.S. Fish and Wildlife Service. Nightfall can set the stage for an acrobatic high-stakes drama in the air — a swirl of bats and their prey each trying to outmaneuver the other in aerial pursuit and escape.

"It is life or death for a lot of these insects to get across the sky," says Gough. Bats are skilled nocturnal hunters that use echolocation to find, track, and catch their prey. "When [bats are] cruising through the night sky," he says, "they're sending out a pulse, listening for a response."

These ultrasound pulses are like an acoustic strobe light: They "illuminate" the night air with a sonic search beam that allows bats to home in on their next snack. But insects have evolved an array of strategies to avoid a bat's attack.

In the latest twist in our understanding of this arms race, Gough and his colleagues describe in new research published in Biology Letters that tiger beetles — big-eyed, long-legged insects with pincer-like jaws — produce their own ultrasound in response to a bat's ultrasound. The beetles, they suggest, do it to trick their predators into thinking they're toxic, allowing them to fly away, unharmed.

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Open Access

Tiger beetles produce anti-bat ultrasound and are probable Batesian moth mimics

Harlan M. Gough, Juliette J. Rubin, Akito Y. Kawahara† and Jesse R. Barber†

Published:15 May 2024https://doi.org/10.1098/rsbl.2023.0610

Review history

Abstract
Echolocating bats and their eared insect prey are in an acoustic evolutionary war. Moths produce anti-bat sounds that startle bat predators, signal noxiousness, mimic unpalatable models and jam bat sonar. Tiger beetles (Cicindelidae) also purportedly produce ultrasound in response to bat attacks. Here we tested 19 tiger beetle species from seven genera and showed that they produce anti-bat signals to playback of authentic bat echolocation. The dominant frequency of beetle sounds substantially overlaps the sonar calls of sympatric bats. As tiger beetles are known to produce defensive chemicals such as benzaldehyde and hydrogen cyanide, we hypothesized that tiger beetle sounds are acoustically advertising their unpalatability. We presented captive big brown bats (Eptesicus fuscus) with seven different tiger beetle species and found that 90 out of 94 beetles were completely consumed, indicating that these tiger beetle species are not aposematically signalling. Instead, we show that the primary temporal and spectral characteristics of beetle warning sounds overlap with sympatric unpalatable tiger moth (Arctinae) sounds and that tiger beetles are probably Batesian mimics of noxious moth models. We predict that many insect taxa produce anti-bat sounds and that the acoustic mimicry rings of the night sky are hyperdiverse.

1. Introduction
Insects that fly at night must defend against echolocating bats. This intense selective pressure has helped refine ultrasonically sensitive ears [1], auditory sensors that are capable of providing advance warnings of bat sonar attacks [2]. Bat-detecting ears are found in at least seven orders of insects (Orthoptera, Mantodea, Hemiptera, Coleoptera, Neuroptera, Lepidoptera and Diptera; [3]). In response to hearing the sonar cries of hunting bats, these insects commonly flee or initiate evasive manoeuvers [4,5]. Many moth species take this acoustic battle a step further and produce ultrasonic clicks in response to bat attacks that can startle bat predators [6], signal noxiousness [4], mimic unpalatable models, [7] and jam bat sonar [8]. A recent study revealed that anti-bat ultrasound production is widespread across the lepidopteran phylogeny and around the globe [9]. There are more than 10 independent origins of ultrasound production and Barber et al. [9] estimated that perhaps 20% of large-bodied moths (Macroheterocera) produce ultrasound in response to bat sonar attack with the primary function of advertising noxiousness (aposematism) and mimicking unpalatable models.

Several species of tiger beetles (Cicindelidae) in the tribe Cicindelini possess ultrasonically sensitive ears and purportedly produce ultrasound in response to bat attacks [10]. Yager & Spangler [11] showed that some tiger beetles emit ultrasonic clicks as part of a motoric behavioural response when queried with synthetic pulses (40 kHz tones at 100 ms intervals) intended to mimic sonar attack. Upon hearing ultrasound, tiger beetles swing their elytra backwards contacting the leading edge of their beating hindwings producing ultrasonic clicks in time with their wingbeat frequency. These researchers hypothesized that this acoustic response functions as an aposematic warning of chemical protection [11].

Defensive chemicals that tiger beetles produce include benzaldehyde and hydrogen cyanide [12,13]. Benzaldehyde is the most widely studied compound produced by tiger beetles and is known from 13 genera, while hydrogen cyanide has been found in two [14,15]. Using a reduced paradigm, chicks (Gallus gallus domesticus) have been shown to reject prey coated with benzaldehyde and hydrogen cyanide [16]. Other work using model tiger beetles has demonstrated that the conspicuous orange abdomens of some beetles, in conjunction with benzaldehyde chemical protection, can reduce the frequency of attacks by robber flies (Asilidae) [17]. We propose that just as bright orange colouring warns visual predators of chemical defence, tiger beetle ultrasonic clicks may be a warning to acoustically specialized bat predators.

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