Deaf moths employ acoustic Müllerian mimicry against bats using wingbeat-powered tymbals

Abstract

Emitting ultrasound upon hearing an attacking bat is an effective defence strategy used by several moth taxa. Here we reveal how Yponomeuta moths acquire sophisticated acoustic protection despite being deaf themselves and hence unable to respond to bat attacks. Instead, flying Yponomeuta produce bursts of ultrasonic clicks perpetually; a striated patch in their hind wing clicks as the beating wing rotates and bends. This wing structure is strikingly similar to the thorax tymbals with which arctiine moths produce their anti-bat sounds. And indeed, Yponomeuta sounds closely mimic such arctiine signals, revealing convergence in form and function. Because both moth taxa contain noxious compounds, we conclude they are mutual Müllerian acoustic mimics. Yponomeuta's perpetual clicking would however also attract bat predators. In response, their click amplitude is reduced and affords acoustic protection just as far as required, matching the distance over which bat biosonar would pick up Yponomeuta echoes anyway - advanced acoustic defences for a deaf moth.

Figure 1

Hyaline (translucent) patch of Yponomeuta (A) Yponomeuta evonymella exposing the hyaline patch on its hindwing (in white box; see B). (B) Scanning electron micrograph (SEM) of the ventral side of the hyaline patch (white box corresponds to that in A), with the striations numbered from left to right and the Cu_1b and Cu₂ veins labelled.

Figure 2

Synchronisation of click bursts with wing beats in Yponomeuta evonymella. (A) Spectrogram (FFT size 256, window Hamming, overlap 25%) and waveform showing an example of the two bursts of ultrasonic clicks produced during one wingbeat. Red and blue boxes represent the frequency range of arctiine anti-bat sounds and the hearing range of Eptesicus fuscus (an insectivorous bat) respectively. (B) Histogram of click timing over five consecutive wingbeats from one individual, time bins each show click counts for 2% of a full wingbeat cycle. (C) Histogram of the timing of twisting at the wing joint for the same wingbeats and bin size as panel B, a value of 1 was assigned for the occurrence and 0 for absence of twisting. All plots represent one full wingbeat.

Figure 3

Source level directionality of Yponomeuta evonymella clicks Mean source level (in dB peSPL re 0.1 m) of eight Yponomeuta evonymella, recorded from four different directions, 0° corresponds to the microphone positioned anteriorly to the moth, 180° posteriorly, 90° laterally, and 45° anterio-laterally. Asterisks indicate significant differences of a nested ANOVA using a mixed effect model with a Bonferroni-corrected Tukey post-hoc test. Error bars show standard deviation.

Figure 4

Echo strength and detection distances (A) Spectral target strength (black line: mean, grey area: SD, n = 5) of five dried Y. evonymella with the wings in an upright position to represent a mid-flight moth. (B) Directionality of detection distance of the right-hand side of Yponomeuta evonymella based on echo target strengths over 180° in 0.5° steps (black line: mean, grey area: SD, n = 5), and sound produced by the moth’s wing-based tymbal during tethered flight in four orientations; 0°, 45°, 90°, and 180° (red circles: mean, error bars SD, n = 8, 80). Photograph (c) L. O’Reilly.