Listening to the environment: hearing differences from an epigenetic effect in solitarious and gregarious locusts

Locusts display a striking form of phenotypic plasticity, developing into either a lone-living solitarious phase or a swarming gregarious phase depending on population density. The two phases differ extensively in appearance, behaviour and physiology. We found that solitarious and gregarious locusts have clear differences in their hearing, both in their tympanal and neuronal responses. We identified significant differences in the shape of the tympana that may be responsible for the variations in hearing between locust phases. We measured the nanometre mechanical responses of the ear's tympanal membrane to sound, finding that solitarious animals exhibit greater displacement. Finally, neural experiments signified that solitarious locusts have a relatively stronger response to high frequencies. The enhanced response to high-frequency sounds in the nocturnally flying solitarious locusts suggests greater investment in detecting the ultrasonic echolocation calls of bats, to which they are more vulnerable than diurnally active gregarious locusts. This study highlights the importance of epigenetic effects set forth during development and begins to identify how animals are equipped to match their immediate environmental needs.

Time-resolved tympanal mechanics of the locust

A salient characteristic of most auditory systems is their capacity to analyse the frequency of sound. Little is known about how such analysis is performed across the diversity of auditory systems found in animals, and especially in insects. In locusts, frequency analysis is primarily mechanical, based on vibrational waves travelling across the tympanal membrane. Different acoustic frequencies generate travelling waves that direct vibrations to distinct tympanal locations, where distinct groups of correspondingly tuned mechanosensory neurons attach. Measuring the mechanical tympanal response, for the first time, to acoustic impulses in the time domain, nanometre-range vibrational waves are characterized with high spatial and temporal resolutions. Conventional Fourier analysis is also used to characterize the response in the frequency domain. Altogether these results show that travelling waves originate from a particular tympanal location and travel across the membrane to generate oscillations in the exact region where mechanosensory neurons attach. Notably, travelling waves are unidirectional; no strong back reflection or wave resonance could be observed across the membrane. These results constitute a key step in understanding tympanal mechanics in general, and in insects in particular, but also in our knowledge of the vibrational behaviour of anisotropic media.

How well are FREQUENCY SENSITIVITIES OF grasshopper ears tuned to species-specific song spectra?

Grasshoppers of 20 acridid species were examined using spectral analysis, laser vibrometry and electrophysiology to determine whether the song spectra, the best frequencies of tympanal-membrane vibrations and the threshold curves of the tympanal nerves are adapted to one another. The songs of almost all species have a relatively broad-band maximum in the region between 20 and 40 kHz and a narrower peak between 5 and 15 kHz. There are clear interspecific differences in the latter, which are not correlated with the length of the body or of the elytra. At the site of attachment of the low-frequency receptors (a-cells), the tympanal membrane oscillates with maximal amplitude in the region from 5 to 10 kHz. At the attachment site of the high-frequency receptors (d-cells), there is also a maximum in this region as well as another around 15-20 kHz. The tympanal nerve is most sensitive to tones between 5 and 10 kHz, with another sensitivity maximum between 25 and 35 kHz. The species may differ from one another in the position of the low-frequency peaks of the membrane oscillation, of the nerve activity and of the song spectra. No correlation was found between the characteristic frequency of the membrane oscillation and the area of the tympanal membrane. Within a given species, the frequency for maximal oscillation of the membrane at the attachment site of the low-frequency receptors and the frequency for maximal sensitivity of the tympanal nerve are in most cases very close to the low-frequency peak in the song spectrum. In the high-frequency range, the situation is different: here, the position of the peak in the song spectrum is not correlated with the membrane oscillation maximum at the attachment site of the high-frequency receptors, although there is a correlation between the song spectrum and the sensitivity of the tympanal nerve. On the whole, therefore, hearing in acridid grasshoppers is quite well adjusted to the frequency spectra of the songs, partly because the tympanal membrane acts as a frequency filter in the low-frequency range.

The influence of tracheal pressure changes on the responses of the tympanal membrane and auditory receptors in the locust Locusta migratoria L.

In resting tethered locusts, the effect of slow changes in tracheal air pressure on peripheral auditory information processing was analysed. The tympanal membrane vibrations, the pressure inside the tracheal system and the summed activity of the auditory receptors were measured simultaneously. With the membrane in the resting position, laser vibrometry and Fast Fourier Transformation analysis of sound-induced membrane vibrations demonstrated characteristic power spectra at the attachment sites of the high-frequency and low-frequency receptors. The spectra were different above 9 kHz, but very similar in the range 2­9 kHz. During ventilation, tracheal pressure changed between -500 and 1500 Pa. This caused tympanal membrane peak-to-peak displacements in the range 70­90 µm outwards and 20­30 µm inwards, as measured by means of laser interferometry. For a quantitative analysis, sinusoidal tympanal membrane displacements with amplitudes such as those during natural ventilation could be induced by applying pressure to the tracheal system. There was a sigmoid relationship between the tracheal pressure and the corresponding membrane displacement. Outward displacements of the tympanal membrane at the attachment site of the elevated process (a-cells) attenuated sound-induced membrane vibrations in the ranges 2­10 kHz and 14­22 kHz and increased them in the ranges 10­14 kHz and 22­25 kHz. At the pyriform vesicle (d-cells), the vibration sensitivity was reduced in the frequency range 2­14 kHz. Sensitivity was enhanced in the range 14­25 kHz. As a consequence, the detection of acoustic signals was also influenced at the auditory receptor level. Tympanal membrane displacements during acoustic stimulation with 4 kHz sound pulses decreased the summed receptor response by approximately 15 dB. At 16 kHz, an increase of the response equivalent to 7 dB occurred. The effect on the response to white noise was intermediate.