Moths produce extremely quiet ultrasonic courtship songs by rubbing specialized scales

Abstract

Insects have evolved a marked diversity of mechanisms to produce loud conspicuous sounds for efficient communication. However, the risk of eavesdropping by competitors and predators is high. Here, we describe a mechanism for producing extremely low-intensity ultrasonic songs (46 dB sound pressure level at 1 cm) adapted for private sexual communication in the Asian corn borer moth, Ostrinia furnacalis. During courtship, the male rubs specialized scales on the wing against those on the thorax to produce the songs, with the wing membrane underlying the scales possibly acting as a sound resonator. The male's song suppresses the escape behavior of the female, thereby increasing his mating success. Our discovery of extremely low-intensity ultrasonic communication may point to a whole undiscovered world of private communication, using "quiet" ultrasound.

Fig. 1.

Synchronicity of ultrasonic song production and wing strokes in O. furnacalis. Gray line represents the oscillogram of six sound pulses recorded with a microphone during courtship. Black line with dots shows a trace of distances between distal edges of the right and left forewings, calculated from a frame-by-frame analysis of high-speed video (Movie S2) at 2-ms intervals (31 frames in 60 ms), which indicates up and down strokes of the wings (white and black arrows, respectively).

Fig. 2.

Sex-specific scales on forewings and mesothoraxes. (A) Drawing of a male moth showing the positions of sex-specific scales (indicated by arrowheads) on the right of the notum (dorsal plate of mesothorax) and basal part of the right forewing. The left tegula (indicated by an asterisk) is shown intact, but the right tegula is removed to show the male-specific scales. (Scale bar: 2 mm.) (B) Photograph showing areas bearing the male-specific scales (indicated by a dotted box in A). Left and right arrowheads indicate the male-specific scales on the mesothorax and forewing, respectively. (Scale bar: 1 mm.) (C) Scanning electron micrograph of the right mesothorax of a male with the sex-specific scales (a) and ordinary scales (b). (D) The female mesothorax with scales corresponding to the male-specific scales (c) and ordinary scales (d). (E) The right forewing of a male with the sex-specific scales (e) and ordinary scales (f). A scaleless area is found adjacent to the sound scales. (F) The female forewing with scales corresponding to the male-specific scales (g) and ordinary scales (h). (Scale bars: C–F, 200 μm.) (G) Surface ultrastructure of individual scales: a, male-specific mesothoracic scale; c, female mesothoracic scale; e, male-specific forewing scale; g, female forewing scale. (Scale bar: 2 μm.) (H–K) Morphology of ridges on the male-specific scales and ordinary scales. Box-and-whisker plots show the median, lower and upper quartiles, and adjacent values within 1.5 × interquartile ranges from the quartiles. (H) The interridge distance is significantly shorter in the mesothoracic sound scale a than in ordinary scales b (t = 4.65, P < 0.001), c (t = 5.32, P < 0.001), and d (t = 5.08, P < 0.001) (Dunnett's test, n = 5). (I) The ridge is significantly thicker in scale a than in scale b (t = 8.79, P < 0.0001), c (t = 8.24, P < 0.0001), and d (t = 4.97, P < 0.001) (n = 5). (J) The interridge distance is significantly shorter in the forewing male-specific scale e than in ordinary scales f (t = 3.71, P < 0.01), g (t = 3.06, P < 0.05), and h (t = 4.11, P < 0.01) (n = 5). (K) The ridge is significantly thicker in scale e than scales f (t = 11.00, P < 0.0001), g (t = 8.30, P < 0.0001), and h (t = 10.70, P < 0.0001) (n = 5).

Fig. 3.

Effects of sound scale treatments on sound production. (A) Sound level (dB SPL at 1 cm) diminished when either or both of the male-specific scales on the mesothorax and forewing were ablated or covered with Vaseline. n = numbers of males tested. (B) Vibration characteristics of the male-specific scales and the cuticle underlying them measured using a laser Doppler vibrometer. Relative vibration amplitudes (dB) of objects in response to excitation by pulsed sound sweeps (10–70 kHz) are shown. The amplitude spectrum of each object was normalized to that of thoracic male-specific scales, which exhibited the weakest response among the objects examined.

Fig. 4.

Physiological and behavioral responses of moths. (A) Hearing threshold curves and sound level spectra of male songs. Red thin lines denote hearing threshold curves obtained from tympanal nerves of six females, and the red bold line shows the average. Blue line shows a hearing threshold curve of a male. Black bold line shows an average power spectrum of 20 male songs, and black dotted lines show the range. The songs were recorded at a distance of 1 cm, which corresponds to the distance between a female and a courting male. (B–D) Effect of male songs on the number of copulation attempts a courting male with damaged genital claspers can repeat before the female escapes. Males with damaged genital claspers cannot copulate and repeat copulation attempts over and over. The number of copulation attempts thus reflects the male's success in suppressing the escape behavior of the female. (B) Effect of male song (Control, no treatment on the sound scales; Muted, sound scales covered with Vaseline; Sham, ordinary scales covered with Vaseline). A significant difference in the number of copulation attempts is found among the male treatments [generalized linear model (GLM), errors: negative binomial; link: log, ANOVA χ²_2,57 = 24.1, P < 0.0001]. (C) Effect of different sound stimuli (Natural song, the song produced by sham-operated males; Playback song, playback of recorded male songs at original sound level, ≈46 dB SPL; Noise, playback of recorded background noises; Silence, no sound broadcast). Males in the “Natural song” test group were sham-operated, and males in the other test groups were muted by covering the sound scales with Vaseline. In addition, all males were deafened to eliminate the influence of sound stimuli on their behavior. A significant difference in the number of copulation attempts is found among the sound stimuli groups (GLM, ANOVA χ²_3,76 = 23.6, P < 0.0001). (D) Effect of sound level. All males were muted and deafened. Male song playbacks with different sound intensities (26, 38, 46, 62, and 74 dB SPL) were broadcast to the females. A significant difference in the number of copulation attempts is found among the sound level groups (GLM, ANOVA χ²_4,95 = 17.8, P < 0.0014).