Do large bushcrickets have more sensitive ears? Natural variation in hearing thresholds within populations of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae)

The auditory spiracle of tettigoniid Orthoptera influences hearing threshold and, for the most part, individuals with larger auditory spiracles have lower hearing thresholds; they are more sensitive. Hearing thresholds of both sexes of the bushcricket, Requena verticalis Walker (Orthoptera; Tettigoniidae; Listroscelidinae), were measured at the male call's carrier frequency and were found to correlate with spiracle dimension. In turn, spiracle dimension correlates with the size of the insect as measured by pronotum length. The best frequency of hearing is close to 16 kHz and this appears to be independent of size. Males show a higher variation in threshold than females and this was reflected in a trend toward lower variance in spiracle size in females.
To test the effects of size on sensitivity, spiracle size was manipulated by partially blocking it. Blocking the spiracle decreases sensitivity to high rather than low frequencies. As in other tettigoniids, the spiracle and associated auditory system act as a high-pass filter. Within and between sex differences in hearing sensitivity were compared with differences in male call intensity. It is argued that sensitivity to sounds associated with mating should be as much under sexual selection as the sexual calls of males.     

Sensory evolution of hearing in tettigoniids with differing communication systems

In Tettigoniidae (Orthoptera: Ensifera), hearing organs are essential in mate detection. Male tettigoniids usually produce calling songs by tegminal stridulation, whereas females approach the males phonotactically. This unidirectional communication system is the most common one among tettigoniids. In several tettigoniid lineages, females have evolved acoustic replies to the male calling song which constitutes a bidirectional communication system. The genus Poecilimon (Tettigoniidae: Phaneropterinae) is of special interest because the ancestral state of bidirectional communication, with calling males and responding females, has been reversed repeatedly to unidirectional communication. Acoustic communication is mediated by hearing organs that are adapted to the conspecific signals. Therefore, we analyse the auditory system in the Tettigoniidae genus Poecilimon for functional adaptations in three characteristics: (i) dimension of sound‐receiving structures (tympanum and acoustic spiracle), (ii) number of auditory sensilla and (iii) hearing sensitivity. Profound differences in the auditory system correlate with uni‐ or bidirectional communication. Among the sound‐receiving structures, the tympana scale with body size, whereas the acoustic spiracle, the major sound input structure, was drastically reduced in unidirectional communicating species. In the unidirectional P. ampliatus group, auditory sensilla are severely reduced in numbers, but not in the unidirectional P. propinquus group. Within the P. ampliatus group, the number of auditory sensilla is further reduced in P. intermedius which lost acoustic signalling due to parthenogenesis. The auditory sensitivity correlated with the size of the acoustic spiracle, as hearing sensitivity was better with larger spiracles, especially in the ultrasonic range. Our results show a significant reduction in auditory structures, shaped by the differing sex roles during mate detection.     

Directionality of the tympanal vibrations in a cicada: a biophysical analysis

1. Laser vibrometry and acoustic measurements were used to study the biophysics of directional hearing in males and females of a cicada, in which most of the male tympanum is covered by thick, water filled tissue “pads”. 2. In females, the tympanal vibrations are very dependent on the direction of sound incidence in the entire frequency range 1–20 kHz, and especially at the main frequencies of the calling song (3–7 kHz). At frequencies up to 10 kHz, the directionality disappears if the contralateral tympanum, metathoracic spiracle, and folded membrane are blocked with Vaseline. This suggests some pressure-difference receiver properties in the ear. 3. In males, the tympanal vibrations depend on the direction of sound incidence only within narrow frequency bands (around 1.8 kHz and at 6–7 kHz). At frequencies above 10–12 kHz, the directionality appears to be determined by diffraction, and the ear seems to work as a pressure receiver. The peak in directionality at 6–7 kHz disappears when the contralateral timbal, but not the tympanum, is covered. Covering the thin ventral abdominal wall causes the peak around 1.8 kHz to disappear. 4. Most observed tympanal directionalities, except around 1.8 kHz in males, are well predicted from measured transmissions of sound through the body and measured values of sound amplitude and phase at the ears at various directions of sound incidence. Accepted: 18 October 1996     

The spectral structure of vocalizations match hearing sensitivity but imprecisely in Philautus odontotarsus

It is generally thought that for species using vocal communication the spectral properties of the sender’s calls should match the frequency sensitivity of the receiver’s auditory system. Nevertheless, few studies have investigated both sender and receiver characteristics in anuran species. In the present study, auditory brainstem responses (ABRs) were recorded in the serrate legged treefrog, Philautus odontotarsus, in order to determine if male call spectral structure and hearing sensitivity in males and females have co-evolved in this species. The results showed that the spectral structures of male vocalization match both male and female hearing sensitivity, even though the dominant frequencies of male calls (2.5 kHz) are mismatched with the regions of best frequency sensitivity (1.4 and 2.8 kHz). In addition, the results show that, in contrast with most previous ABR studies in non-human animals, but consistent with human studies, there are noticeable sex differences in peripheral auditory sensitivity in Philautus insofar as females exhibit lower auditory thresholds than males across the entire 1.8–18 kHz frequency range. The results also show that the dominant frequency of male calls is negatively correlated with body size, indicating that call characteristics reflect body size in this species which may be used by females during mate choice.     

An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog

The matched filter hypothesis proposes that the tuning of auditory sensitivity and the spectral character of calls will match in order to maximize auditory processing efficiency during courtship. In this study, we analyzed the acoustic structure of male calls and both male and female hearing sensitivities in the little torrent frog (Amolops torrentis), an anuran species who transmits acoustic signals across streams. The results were in striking contradiction to the matched filter hypothesis. Auditory brainstem response results showed that the best hearing range was 1.6–2 kHz consistent with the best sensitive frequency of most terrestrial lentic taxa, yet completely mismatched with the dominant frequency of conspecific calls (4.3 kHz). Moreover, phonotaxis tests show that females strongly prefer high‐frequency (4.3 kHz) over low‐frequency calls (1.6 kHz) regardless of ambient noise levels, although peripheral auditory sensitivity is highest in the 1.6–2 kHz range. These results are consistent with the idea that A. torrentis evolved from nonstreamside species and that high‐frequency calls evolved under the pressure of stream noise. Our results also suggest that female preferences based on central auditory system characteristics may evolve independently of peripheral auditory system sensitivity in order to maximize communication effectiveness in noisy environments.     

Thresholds of cat cochlear nucleus neurons to microwave pulses

Action potentials of neurons in cat dorsal and posteroventral cochlear nuclei were recorded extracellularly with glass microelectrodes while the head of the cat was exposed to microwave pulses at 915 MHz using a diathermy applicator. Response thresholds to acoustic tones, acoustic clicks, and microwave pulses were determined for auditory units with characteristic frequencies (CFs) from 278 Hz to 39.2 kHz. Tests with pulsatile stimuli were performed for durations of 20-700 mus, principally 20, 70, and 200 mus. Brainstem midline specific absorption rate (SAR) threshold was as small as 11.1 mW/g per pulse, and specific absorption (SA) threshold was a small as 0.6 muJ/g per pulse. Microwave thresholds were generally lower for CF less than 9 kHz, as were most acoustic thresholds. However, microwave threshold was only weakly related to click threshold and CF-tone threshold of each unit.     

Frequency sensitivity and directional hearing in the gleaning bat,Plecotus auritus (Linnaeus 1758)

1. The neural audiogram of the common long-eared bat, Plecotus auritus was recorded from the inferior colliculus (IC). The most sensitive best frequency (BF) thresholds for single neurones are below 0 dB SPL between 7-20 kHz, reaching a best value of -20 dB SPL between 12-20 kHz. The lower and upper limits of hearing occur at 3 kHz and 63 kHz, respectively, based on BF thresholds at 80 dB SPL. BF threshold sensitivities are about 10 dB SPL between 25-50 kHz, corresponding to the energy band of the sonar pulse (26-78 kHz). The tonotopic organization of the central nucleus of the IC (ICC) reveals that neurones with BFs below 20 kHz are disproportionately represented, occupying about 30% of ICC volume, occurring in the more rostral and lateral regions of the nucleus. 2. The acoustical gain of the external ear reaches a peak of about 20 dB between 8-20 kHz. The gain of the pinna increases rapidly above 4 kHz, to a peak of about 15 dB at 7-12 kHz. The pinna gain curve is similar to that of a simple, finite length acoustic horn; expected horn gain is calculated from the average dimensions of the pinna. 3. The directional properties of the external ear are based on sound diffraction by the pinna mouth, which, to a first approximation, is equivalent to an elliptical opening due to the elongated shape of the pinna. The spatial receptive field properties for IC neurones are related to the directional properties of the pinna. The position of the acoustic axis of the pinna and the best position (BP) of spatial receptive fields are both about 25 degrees from the midline between 8-30 kHz but approach the midline to 8 degrees at 45 kHz. In elevation, the acoustic axis and the BP of receptive fields move upwards by 20 degrees between 9-25 kHz, remaining stationary for frequencies up to 60 kHz. 4. The extremely high auditory sensitivity shown by the audiogram and the directionality of hearing are discussed in terms of the adaptation of the auditory system to low frequencies and the role of a large pinna in P. auritus. The functional significance of low frequency hearing in P. auritus is discussed in relation to hunting for prey by listening and is compared to other gleaning species.     

Ultrasound hearing and male–male communication in Australian katydids (Tettigoniidae: Zaprochilinae) with sexually dimorphic ears

The genus Kawanaphila (Tettigoniidae: Zaprochilinae) is unusual among the Tettigoniidae in the possession of sexually dimorphic auditory organs. We examined the auditory system and acoustic behaviour of two previously unstudied species in this genus to test whether reduced hearing in males is consistently associated with reduced male–male competition. Kawanaphila yarraga (Rentz, 1993) and K. mirla (Rentz, 1993) are both sexually dimorphic with respect to their auditory system, but to different degrees. Males of both species produce songs consisting of trains of brief (< 1 ms) pure-tone sound pulses at ultrasonic frequencies (K. yarraga, 40 kHz;K. mirla, 70 kHz). In both species, female hearing is more sensitive than that of males by 10 dB. In addition, male K. mirla are most sensitive at lower frequencies than females. Male and female K. yarraga differed only in sensitivity, not in tuning. The two species also differ in their degree of sexual dimorphism in auditory anatomy. Kawanaphila mirla males lack some auditory specializations of the prothoracic tracheal system, which are present in the normal tettigoniid condition in females. In K. yarraga males these structures are present, but reduced in size relative to females. The acoustic behaviour of males of the two species is consistent with this pattern of relative auditory sensitivity. Males of both species interact acoustically by altering the timing of their sound output to synchronize with neighbouring males. However, K. mirla males only interact in this way over very short distances (< 5 m), whereas K. yarraga males interact with neighbours up to at least 10 m distant. These results indicate that, although males of the two species differ in hearing sensitivity, the nature of their responses to conspecific calls are similar to one another and to those of other acoustic insects. This suggests that acoustically mediated male–male competition may be maintained even while selection favours a reduction in male auditory sensitivity.     

Directional characteristics of the auditory system of cicadas: is the sound producing tymbal an integral part of directional hearing?

Abstract. Directional hearing is investigated in males of two species of cicadas, Tympanistalna gastrica (Stål) and Tettigetta josei Boulard, that are similar in size but show different calling song spectra. The vibrational response of the ears is measured with laser vibrometry and compared with thresholds determined from auditory nerve recordings. The data are used to investigate to what extent the directional characteristic of the tympanal vibrations is encoded by the activity of auditory receptors. Laser measurements show complex vibrations of the tympanum, and reveal that directional differences are rather high (>15 dB) in characteristic but limited frequency ranges. At low frequencies, both species show a large directional difference at the same frequency (3–5 kHz) whereas, above 10 kHz, the directional differences correspond to the different resonant frequencies of the respective tymbals. Consequently, due to the mechanical resonance of the tymbal, the frequency range at which directional differences are high differs between the two species that otherwise show similar dimensions of the acoustic system. The directional differences observed in the tympanal vibrations are also observed in the auditory nerve activity. These recordings confirm that the biophysically determined directional differences are available within the nervous system for further processing. Despite considerable intra as well as interindividual variability, the ears of the cicadas investigated here exhibit profound directional characteristics, because the thresholds determined from recordings of the auditory nerve at 30° to the right and left of the longitudinal axis differ by more than 5 dB.     

Hearing Range of White-Tailed Deer as Determined by Auditory Brainstem Response

Abstract: Basic knowledge of white-tailed deer (Odocoileus virginianus) hearing can improve understanding of deer behavior and may assist in the development of effective deterrent strategies. Using auditory brainstem response testing, we determined that white-tailed deer hear within the range of frequencies we tested, between 0.25–30 kilohertz (kHz), with best sensitivity between 4–8 kHz. The upper limit of human hearing lies at about 20 kHz, whereas we demonstrated that white-tailed deer detected frequencies to at least 30 kHz. This difference suggests that research on the use of ultrasonic (frequencies >20 kHz) auditory deterrents is justified as a possible means of reducing deer—human conflicts.     

Size, peripheral auditory tuning and target strength in noctuid moths

We investigated relationships among body size, the frequency of peak auditory sensitivity (best frequency) and acoustic conspicuousness (measured as target strength) to simulated bat echolocation calls in a range of tympanate moths (Lepidoptera: Noctuidae). Audiograms of Amphipyra pyramidea Linnaeus, Agrotis exclamationis Linnaeus, Omphaloscelis lunosa Haworth and Xestia xanthographa Denis and Schiffermüller are described for the first time. Best frequency was inversely related to forewing length, an index of body size. Models predict that target strength falls off rapidly once wavelength (1/frequency) exceeds some defined feature of target size (e.g. circumference for spheres). We investigated how target strength varies in relation to target size and emitted frequency for simple targets (paper discs) and for moths. Target strength fell rapidly when target radius/wavelength < 2 for paper discs of similar size to many noctuid moths. Target strength fell rapidly below wing‐length/wavelength ratios of 2 in relatively small (O. lunosa, wing‐length = 15.2 ± 0.4 mm, best frequency = 45 kHz) and large (N. pronuba, wing‐length = 24.6 ± 0.8 mm, best frequency = 15 kHz) noctuid species, and decreased rapidly at frequencies below 25 kHz in both species. These target strengths were used to predict the detection distance of the moths by bat sonar between 10 and 55 kHz. Predicted detection distances of both species were maximal for fictive call frequencies of 20 kHz, and were reduced at lower frequencies due to decreased target strength and at higher frequencies by excess atmospheric attenuation. Both relatively large and small noctuid moths are therefore strong acoustic targets to bats that echolocate at relatively low frequencies. Bats may emit allotonic calls at low frequency because the costs of reduced detection range are smaller than the benefits of reduced audibility to moths. Because best frequency scales with body size and maximum detection distance is not very sensitive to body size, noctuid moths in the size range examined do not necessarily have best frequencies that would match the call frequencies of bats that may detect the moths at greatest distance precisely. Hence, best frequency may be constrained in part by body size.     

Development of the auditory sensitivity and formation of the acoustically guided defensive behavior in nestlings of the pied flycatcher Ficedula hypoleuca

Age dynamics of generation of the evoked potentials (EP) in the field L of caudal nidopallium (the higher integrative center of the avian auditory system) and development of the auditory-guided defensive behavior were studied in control and visually deprived pied flycatcher Ficedula hypoleuca nestlings. It was shown that the rhythmically organized monofrequency signals with sound frequency 3.5 kHz and higher produced the defensive behavior as the auditory sensitivity to these frequencies matured. After 9 days, the species-specific alarm signal produced more effectively the defensive behavior than the tonal signals. The rhythmically organized sound with filling frequency 0.5 kHz, occupying the less low-frequency diapason than the feeding signal, produced the effect opposite to the alarm signal to increase the nestling mobility. At the initial stage of the defensive behavior development the auditory threshold fell markedly in the frequency diapason corresponding to the frequency diapason of the alarm signal (5–6 kHz), which seemed to facilitate involvement of this diapason signals in the defensive integration. The auditory EP generation thresholds in the whole studied diapason were lower in the visually deprived nestlings than in the normally developing one; however, the ability of the acoustic signals to suppress alimentary reactions fell significantly.     

Innovative biomechanics for directional hearing in small flies

In humans and animals alike, the localization of sound constitutes a fundamental processing task of the auditory system. Directional hearing relies on acoustic cues such as the interaural amplitude and time differences and also, sometimes, the signal spectral composition. In small animals, such as insects, the auditory receptors are forcibly set close together, a design constraint imposing very short interaural distances. Due to the physics of sound propagation, the close proximity of the sound receivers results in vanishingly small amplitude and time cues. Yet, because of their directionality, small auditory systems embed original and innovative solutions that can be of inspirational value to some acute problems of technological miniaturization. Such ears are found in a parasitoid fly that acoustically locates its singing cricket host. Anatomically rather unconventional, the fly's auditory system is endowed with a directional sensitivity that is based on the mechanical coupling between its two hemilateral tympanal membranes. The functional principle permitting this directionality may be of particular relevance for technological applications necessitating sensors that are low cost, low weight, and low energy. Based on silicon-etching technology, early prototypes of sub-millimeter acoustic sensors provide evidence for directional mechanical responses. Further developments hold the promise of applications in hearing aid technology, vibration sensors, and miniature video-acoustic surveillance systems.     

Ultrasonic startle behavior in bushcrickets (Orthoptera; Tettigoniidae)

1. In the present work, we show that in flight, bushcrickets not previously known to respond to ultrasound alter their flight course in response to ultrasonic stimuli. Such stimuli elicit in flying Neoconocephalus ensiger an extension of the front and middle legs along the body and a rapid closure of all 4 wings (Fig. 1). This is a short latency acoustic startle response to ultrasound, consistent with acoustic startle responses of other insects. 2. The percentage of trials on which acoustic startle responses were elicited was maximum (90%) for sound frequencies ranging from 25 to at least 60 kHz. No acoustic startle response was observed at frequencies of 5 or 10 kHz (Fig. 2). The threshold for the response was roughly 76 dB between 25 to 60 kHz (Fig. 2) and the behavioral latency was 45 ms (Fig. 3). Recordings from flight muscles show that they cease discharging during the acoustic startle response (Fig. 4). 3. The characteristics of the acoustic startle response match those of an auditory interneuron called the T-neuron. The frequency sensitivity of this neuron is greatest for sound frequencies ranging from 13 to 60 kHz (Fig. 6). Moreover, we found that the neuron produces many more spikes to ultrasound (30 kHz) of increasing intensities than to a conspecific communication sound, whose dominant frequency is 14 kHz (Fig. 7).     

Psychophysical and neurophysiological hearing thresholds in the bat <Emphasis Type="Italic">Phyllostomus </Emphasis><Emphasis Type="Italic">discolor</Emphasis>

Absolute hearing thresholds in the spear-nosed bat Phyllostomus discolor have been determined both with psychophysical and neurophysiological methods. Neurophysiological data have been obtained from two different structures of the ascending auditory pathway, the inferior colliculus and the auditory cortex. Minimum auditory thresholds of neurons are very similar in both structures. Lowest absolute thresholds of 0 dB SPL are reached at frequencies from about 35 to 55 kHz in both cases. Overall behavioural sensitivity is roughly 20 dB better than neural sensitivity. The behavioural audiogram shows a first threshold dip around 23 kHz but threshold was lowest at 80 kHz (−10 dB SPL). This high sensitivity at 80 kHz is not reflected in the neural data. The data suggest that P. discolor has considerably better absolute auditory thresholds than estimated previously. The psychophysical and neurophysiological data are compared to other phyllostomid bats and differences are discussed. S. Hoffmann, L. Baier, F. Borina contributed equally to this work.     

Hearing in the sea otter (Enhydra lutris): auditory profiles for an amphibious marine carnivore

In this study we examine the auditory capabilities of the sea otter (Enhydra lutris), an amphibious marine mammal that remains virtually unstudied with respect to its sensory biology. We trained an adult male sea otter to perform a psychophysical task in an acoustic chamber and at an underwater apparatus. Aerial and underwater audiograms were constructed from detection thresholds for narrowband signals measured in quiet conditions at frequencies from 0.125–40 kHz. Aerial hearing thresholds were also measured in the presence of octave-band masking noise centered at eight signal frequencies (0.25–22.6 kHz) so that critical ratios could be determined. The aerial audiogram of the sea otter resembled that of sea lions and showed a reduction in low-frequency sensitivity relative to terrestrial mustelids. Best sensitivity was ?1 dB re 20 µPa at 8 kHz. Under water, hearing sensitivity was significantly reduced when compared to sea lions and other pinniped species, demonstrating that sea otter hearing is primarily adapted to receive airborne sounds. Critical ratios were more than 10 dB higher than those measured for pinnipeds, suggesting that sea otters are less efficient than other marine carnivores at extracting acoustic signals from background noise, especially at frequencies below 2 kHz.     

Auditory evoked potentials in the Japanese monkey.

Auditory sensitivity based on auditory brain stem response (ABR), whole nerve action potential (AP), and cochlear microphonics (CM) to tone bursts of 0.5-8 kHz were compared with behavioral audiometry in the Japanese monkeys. Although sensitivity loss at 4-6 kHz was observed in these potentials, an increase in sensitivity at 8 kHz was obtained only in the ABR. Thus the sensitivity loss at 4-6 kHz originates at the peripheral system and the increased sensitivity at 8 kHz originates at the central.     

Effects of Boat Engine Noise on the Auditory Sensitivity of the Fathead Minnow, Pimephales promelas

Fishes are constantly exposed to various sources of noise in their underwater acoustic environment. Many of these sounds are from anthropogenic sources, especially engines of boats. Noise generated from a small boat with a 55 horsepower outboard motor was played back to fathead minnows, Pimephales promelas, for 2 h at 142 dB (re: 1 Pa), and auditory thresholds were measured using the auditory brainstem response (ABR) technique. The results demonstrate that boat engine noise significantly elevate a fish's auditory threshold at 1 kHz (7.8 dB), 1.5 kHz (13.5 dB), and 2.0 kHz (10.5 dB), the most sensitive hearing range of this species. Such a short duration of noise exposure leads to significant changes in hearing capability, and implies that man-made noise generated from boat engines can have far reaching environmental impacts on fishes.     

Hearing conspecific vocal signals alters peripheral auditory sensitivity

We investigated whether hearing advertisement calls over several nights, as happens in natural frog choruses, modified the responses of the peripheral auditory system in the green treefrog, Hyla cinerea. Using auditory evoked potentials (AEP), we found that exposure to 10 nights of a simulated male chorus lowered auditory thresholds in males and females, while exposure to random tones had no effect in males, but did result in lower thresholds in females. The threshold change was larger at the lower frequencies stimulating the amphibian papilla than at higher frequencies stimulating the basilar papilla. Suprathreshold responses to tonal stimuli were assessed for two peaks in the AEP recordings. For the peak P1 (assessed for 0.8–1.25 kHz), peak amplitude increased following chorus exposure. For peak P2 (assessed for 2–4 kHz), peak amplitude decreased at frequencies between 2.5 and 4.0 kHz, but remained unaltered at 2.0 kHz. Our results show for the first time, to our knowledge, that hearing dynamic social stimuli, like frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.     

Evoked potential audiometry of 13 Pacific bottlenose dolphins (Tursiops truncatus gilli)

Evoked potential audiograms were measured in 13 Pacific bottlenose dolphins (Tursiops truncatus gilli) to determine the variability in hearing sensitivity and range of hearing. The auditory evoked potential system used a transducer embedded in a suction cup to deliver sinusoidal amplitude modulated tones to each dolphin through the pan region of the lower right jaw. Evoked potentials were recorded noninvasively using surface electrodes, and hearing thresholds were estimated by tracking the amplitude of the envelope following response, an evoked potential that is phase‐locked to the stimulus modulation rate. Frequencies tested ranged from 10 to 180 kHz in each animal. Variability in the range of hearing and age‐related reductions in hearing sensitivity and range of hearing were consistent with those observed in Atlantic bottlenose dolphins. Comparison of audiograms to a captive population of Atlantic bottlenose dolphins demonstrated that the Pacific bottlenose dolphins tested in this study had significantly lower thresholds at frequencies of 40 and 60–115 kHz. Differences in thresholds between the groups are unlikely to be due to methodological factors.