American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Prey exploits the auditory illusions of eavesdropping predators”

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Henry D. Legett, Claire T. Hemingway, and Ximena E. Bernal (May 2020)

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A male pug-nosed treefrog (<i>Smilisca sila</i>) being bitten by eavesdropping frog-biting midges (<i>Corethrella</i> spp.).<br />(Credit: Henry D. Legett)
A male pug-nosed treefrog (Smilisca sila) being bitten by eavesdropping frog-biting midges (Corethrella spp.).
(Credit: Henry D. Legett)

Animals often use flashy signals to attract mates. The colorful plumage of birds or the night-time songs of frogs and crickets are examples of these so-called mating signals. Usually, more conspicuous mating signals, like brighter colors and louder songs, attract more mates. Conspicuousness, however, also attracts predators. This study investigates how pug-nosed treefrogs balance this tradeoff of attracting mates without also attracting predators. In this treefrog, groups of males simultaneously produce calls in near-perfect synchrony. These synchronized calls exploit an auditory illusion to reduce the call’s attractiveness to their predators, frog-eating bats and frog-biting midges. This auditory illusion results when two sounds are closely synchronized (a leading sound is produced closely followed by another sound), as both sounds are perceived as originating from the source of the leading sound. To examine how producing synchronized signals could create this illusion and obscure the location of the following mating signal from predators, field experiments were performed with two speakers playing pug-nosed frog calls mimicking a male producing a leading call closely followed by a call produced by a second male. These experiments revealed that both bats and midges are vulnerable to this auditory illusion, preferring to attack calls from the leading rather than following males. In contrast, female pug-nosed treefrogs have no preference, and choose either male at random. Male pug-nosed treefrogs, therefore, synchronize their calls to deceive predators with an illusion to avoid them but without reducing the attraction of mates.


Abstract

Mating signals have evolved to attract target receivers, even to the point of exploiting receivers through perceptual manipulation. Signals, however, can also expose signalers to non-target receivers, including predators and parasites, and thus have also evolved to decrease enemy attraction. Here we show that male treefrogs (Smilisca sila) reduce their attractiveness to eavesdropping enemies (bats and midges) by overlapping their calls at near-perfect synchrony with the calls of neighboring conspecifics. By producing calls that closely follow those of other males, synchronizing S. sila take advantage of an auditory illusion where enemies are more attracted to the leading call. Female S. sila, however, are not as susceptible to this illusion. Thus, synchronization among signaling males can result in acoustic crypsis from predators without affecting female attraction. Given the widespread use of conspicuous mating signals and eavesdropping enemies, perceptual exploitation of eavesdroppers is likely a common driver of signal evolution.

Presa explota las ilusiones auditivas de los depredadores que usan su sistema de comunicación

Para atraer hembras, las señales de apareamiento han evolucionado hasta el punto de explotar el mecanismo de percepción de los receptores de estas señales. Sin embargo, estas señales también exponen a sus emisores a ataques por depredadores y parásitos, y por tanto, han evolucionado para disminuir su atracción a dichos enemigos. Demonstramos que los machos de ranas arborícolas (Smilisca sila) sobreponen sus llamadas con llamadas de machos vecinos de la misma especie, produciendolas en sincronía y reduciendo que tan atractivas son sus señales para sus enemigos (murciélagos y mosquitos). Al producir su llamada justo después de la de otros machos, la sincronización de cantos en S. sila toma ventaja de una ilusión auditiva en la que los enemigos son atraídos hacia la llamada del macho que canta primero. Las hembras de S. sila, sin embargo, no son susceptibles a esta ilusión. Por lo tanto, la sincronización de producción de señales entre los machos puede dar lugar a cripsis acústica de los depredadores, sin afectar la atracción de las hembras. Dado el uso generalizado de las señales de apareamiento exageradas y el uso de dichas señales por enemigos, la explotación de la percepción de señales por enemigos es probablemente una fuerza común de selección en la evolución de señales de comunicación.