Evolution of directional hearing in moths via conversion of bat detection devices to asymmetric pressure gradient receivers

Abstract

Small animals typically localize sound sources by means of complex internal connections and baffles that effectively increase time or intensity differences between the two ears. However, some miniature acoustic species achieve directional hearing without such devices, indicating that other mechanisms have evolved. Using 3D laser vibrometry to measure tympanum deflection, we show that female lesser waxmoths (Achroia grisella) can orient toward the 100-kHz male song, because each ear functions independently as an asymmetric pressure gradient receiver that responds sharply to high-frequency sound arriving from an azimuth angle 30°contralat-eral to the animal's midline. We found that females presented with a song stimulus while running on a locomotion compensation sphere follow a trajectory 20°-40°to the left or right of the stimulus heading but not directly toward it, movement consistent with the tympanum deflections and suggestive of a monaural mechanism of auditory tracking. Moreover, females losing their track typically regain it by auditory scanning-sudden, wide deviations in their heading-and females initially facing away from the stimulus quickly change their general heading toward it, orientation indicating superior ability to resolve the front-rear ambiguity in source location. X-ray computer-aided tomography (CT) scans of the moths did not reveal any internal coupling between the two ears, confirming that an acoustic insect can localize a sound source based solely on the distinct features of each ear.

Toward a Bio-Inspired Acoustic Sensor: Achroia grisella’s Ear

“…This distance is insufficient to account for any phase, intensity, or time of arrival difference between their ears considering a 100 kilohertz signal has a wavelength of 3.8 millimeters. On the other hand, no connection has been detected between the tympana using X-ray scanning, no spiracles are found either [12], and the measurements of diffraction in the abdominal section of the moth do not provide enough intensity difference [13]. Furthermore, moths with one tympanum pierced and the other one in healthy condition were still able to locate the singing males, if only taking a longer time [14].…”

Neurophysiology goes wild: from exploring sensory coding in sound proof rooms to natural environments

“…In most experiments, the latency differences closely correlated with the maxima and minima of discharge differences, but at some distances, latency differences were large, whereas the discharge differences approached zero. Time bar in A and B 350 ms. (Kostarakos and Römer unpublished) comparison of the acoustic input, when binaural hearing is impaired, as has been suggested earlier for one-eared crickets (Schildberger and Kleindienst 1989), and experimental evidence provided for the moth Achroia grisella (Greenfield et al 2002;Reid et al 2016). Reichert (2015) performed a behavioural study with male grasshoppers on the effect of masking noise on their sound localisation abilities.…”

Directional hearing in insects: biophysical, physiological and ecological challenges

“…The same argument holds for a female katydid that uses branches or leaves to approach a singing male, thereby also constantly deviating from the target direction as a result of her own forced turns. Moreover, under conditions where binaural hearing is impaired or where directional cues are poor or missing, acoustic orientation could be based on the sequential comparison of the acoustic input, as has been suggested for the moth Achroia grisella (Greenfield et al, 2002;Reid et al, 2016). Note that the tilting behaviour displayed by the katydid L. punctatissima also indicates that it makes a sequential comparison of such acoustic input when directional cues are missing (see above).…”