Mammalian ear specializations in arid habitats: structural and functional evidence from sand cat (Felis margarita)

To test whether structural specializations of sand-cat ears are adaptations to their desert habitats we measured structural and acoustic features of their ears. The area of the external ear's pinna flange is similar to that of domestic cat. The dimensions of the ear canal are about twice domestic cat's, as is the volume of the middle-ear air space. The magnitude of the acoustic input-admittance at the tympanic membrane is about five times larger than that of domestic cat; both the middle-ear cavities and the ossicular chain contribute to the increase. Structure-based models suggest the acoustic admittance looking outward through the external ear is generally larger for sand cat than for domestic cat; the radiation power-efficiency is also larger in sand cat for frequencies below 2 kHz. Hearing sensitivity (estimated from measurements and model calculations) in sand cat is predicted to be about 8 dB greater than in domestic cat for frequencies below 2 kHz. Analysis of attenuation of sound in deserts implies that the increased sensitivity extends sand cat's hearing range beyond domestic cat by 0.4 km at 0.5 kHz. Thus, the structural specializations may provide habitat-specific survival value.     

Acoustic communication and the evolution of hearing in fishes

Fishes have evolved a diversity of sound-generating organs and acoustic signals of various temporal and spectral content. Additionally, representatives of many teleost families such as otophysines, anabantoids, mormyrids and holocentrids possess accessory structures that enhance hearing abilities by acoustically coupling air-filled cavities to the inner ear. Contrary to the accessory hearing structures such as Weberian ossicles in otophysines and suprabranchial chambers in anabantoids, sonic organs do not occur in all members of these taxa. Comparison of audiograms among nine representatives of seven otophysan families from four orders revealed major differences in auditory sensitivity, especially at higher frequencies (> 1 kHz) where thresholds differed by up to 50 dB. These differences showed no apparent correspondence to the ability to produce sounds (vocal versus non-vocal species) or to the spectral content of species-specific sounds. In anabantoids, the lowest auditory thresholds were found in the blue gourami Trichogaster trichopterus, a species not thought to be vocal. Dominant frequencies of sounds corresponded with optimal hearing bandwidth in two out of three vocalizing species. Based on these results, it is concluded that the selective pressures involved in the evolution of accessory hearing structures and in the design of vocal signals were other than those serving to optimize acoustic communication.     

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.     

The active space of blue monkey and grey-cheeked mangabey vocalizations

The audible distance of 11 primate vocalizations uttered by blue monkeys, Cercopithecus mitis, and grey-cheeked mangabeys, Cercocebus albigena, and the human utterance ‘hey’ were determined experimentally. Calculations were based on measurements of (1) sound power of vocal signals (Brown: Bioacoustics, in press), (2) the attenuation rates of sound of different frequencies in East African forests (Waser & Brown: Am. J. Primatol., 1986, 10, 135–154), and (3) sensitivity of conspecific listeners to vocal signals presented in forest noise. Calculations were made of the active space, the area over which a call is audible, and the expected number of recipients of signals in nature. Masked thresholds for test vocalizations ranged from 21·1 dB for the mangabey ‘staccato bark’ call to 41·3 dB for the blue monkey ‘boom’ vocalization. The audible distance of the test signals ranged from 79 m for the blue monkey ‘chirp’ call to 1951 m for the mangabey ‘chorused grunt’ vocalization. Calls could be grouped into short- and long-range signals. The audible distance of primate long-range calls varied between 2·4 and nine times that of a typical yell given by human subjects. The active space of the test signals ranged from 1·4 to 1031·8 ha. The mean active space of monkey long-range calls (445·4 ha) was more than an order of magnitude greater than the loudest human yell. The average blue monkey long-range call was audible for 870 m, while the average mangabey long-range call was audible for 1800 m. The typical mangabey home range is four times that of the blue monkey, and in both species the average long-range call had an audible distance twice the diameter of the median home range of each species.     

Japanese macaques form a cross-modal representation of their own species in their first year of life

We tested whether infant Japanese macaques (Macaca fuscata) have a cross-modal representation of their own species. We presented monkeys with a photograph of either a monkey or a human face on an LCD monitor after playing back a vocalization of one of those two species. The subjects looked at the monitor longer when a human face was presented after the monkey vocalization than when the same face was presented after human vocalization. This suggests that monkeys recall and expect a monkey’s face upon hearing a monkey’s voice.     

Hearing in Cichlid Fishes under Noise Conditions

Background

Hearing thresholds of fishes are typically acquired under laboratory conditions. This does not reflect the situation in natural habitats, where ambient noise may mask their hearing sensitivities. In the current study we investigate hearing in terms of sound pressure (SPL) and particle acceleration levels (PAL) of two cichlid species within the naturally occurring range of noise levels. This enabled us to determine whether species with and without hearing specializations are differently affected by noise.

Methodology/Principal Findings

We investigated auditory sensitivities in the orange chromide Etroplus maculatus, which possesses anterior swim bladder extensions, and the slender lionhead cichlid Steatocranus tinanti, in which the swim bladder is much smaller and lacks extensions. E. maculatus was tested between 0.2 and 3kHz and S. tinanti between 0.1 and 0.5 kHz using the auditory evoked potential (AEP) recording technique. In both species, SPL and PAL audiograms were determined in the presence of quiet laboratory conditions (baseline) and continuous white noise of 110 and 130 dB RMS. Baseline thresholds showed greatest hearing sensitivity around 0.5 kHz (SPL) and 0.2 kHz (PAL) in E. maculatus and 0.2 kHz in S. tinanti. White noise of 110 dB elevated the thresholds by 0–11 dB (SPL) and 7–11 dB (PAL) in E. maculatus and by 1–2 dB (SPL) and by 1–4 dB (PAL) in S. tinanti. White noise of 130 dB elevated hearing thresholds by 13–29 dB (SPL) and 26–32 dB (PAL) in E. maculatus and 6–16 dB (SPL) and 6–19 dB (PAL) in S. tinanti.

Conclusions

Our data showed for the first time for SPL and PAL thresholds that the specialized species was masked by different noise regimes at almost all frequencies, whereas the non-specialized species was much less affected. This indicates that noise can limit sound detection and acoustic orientation differently within a single fish family.     

褐菖鲉的听觉阈值研究

利用听觉诱发电位记录技术研究了褐菖鲉(Sebasticus marmoratus)的听觉阈值。通过采用听觉生理系统记录和分析了8尾褐菖鲉对频率范围在100—1000 Hz的7种不同频率的声音刺激的诱发电位反应。结果表明, 褐菖鲉的听觉阈值在整体上随着频率增加而增加, 对100—300 Hz的低频声音信号敏感, 最敏感频率为150 Hz, 对应的听觉阈值为70 dB re 1 μPa。褐菖鲉的听觉敏感区间与其发声频率具有较高的匹配性, 表明其声讯交流的重要性。同时, 人为低频噪声可能对其声讯交流造成影响。     

Audio–vocal interactions during vocal communication in squirrel monkeys and their neurobiological implications

Several strategies have evolved in the vertebrate lineage to facilitate signal transmission in vocal communication. Here, I present a mechanism to facilitate signal transmission in a group of communicating common squirrel monkeys (Saimiri sciureus sciureus). Vocal onsets of a conspecific affect call initiation in all other members of the group in less than 100 ms. The probability of vocal onsets in a range of 100 ms after the beginning of a vocalization of another monkey was significantly decreased compared to the mean probability of call onsets. Additionally, the probability for vocal onsets of conspecifics was significantly increased just a few hundreds of milliseconds after call onset of others. These behavioral data suggest neural mechanisms that suppress vocal output just after the onset of environmental noise, such as vocalizations of conspecifics, and increase the probability of call initiation of group mates shortly after. These findings add new audio–vocal behaviors to the known strategies that modulate signal transmission in vocal communication. The present study will guide future neurobiological studies that explore how the observed audio–vocal behaviors are implemented in the monkey brain.     

Hearing of old world monkeys (Cercopithecinae)

The characteristics of normal hearing were examined in the laboratory for seven species of Old World monkeys. Operant conditioning procedures, coupled with standard audiometric testing methods, were used to assess thresholds of hearing, frequency range of hearing, and differential sensitivity to auditory intensity and frequency. To produce tonal stimulation, an animal was trained to touch and maintain manual contact with a contact-sensitive key and to report hearing the tone by lifting his hand from the key; this response was followed by food reinforcement. When the reporting response occurred without the auditory signal, the animal was punished by a short suspension from the experiment. Additional contingencies were added to ensure stable and reliable responding, and threshold and differential acuity determinations were then made. Threshold was defined as the stimulus value responded to correctly 50% of the time. The frequency range of hearing of all the cercopithecoids tested extended from 60 to 40,000 Hz, an octave above the upper bound of 20,000 Hz for man but well below the 60–70,000 Hz limit for some prosimians. Absolute sensitivity for tonal stimulation in the most sensitive frequency range (1–8 kHz) was about 2 × 10^?4 microbars, comparable to that of other primates tested, including man. Thus, the Old World monkey appears only slightly less sensitive than man to small changes in intensity and frequency of acoustic stimulation. At 1000 Hz at 60 dB above the threshold of audibility, his limit of resolution is about 5 Hz for frequency and 2 dB for intensity.     

Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae)

Thresholds for evoked vocal responses and thresholds of multiunit midbrain auditory responses to pure tones and synthetic calls were investigated in males of Pleurodema thaul, as behavioral thresholds well above auditory sensitivity have been reported for other anurans. Thresholds for evoked vocal responses to synthetic advertisement calls played back at increasing intensity averaged 43 dB RMS SPL (range 31–52 dB RMS SPL), measured at the subjects’ position. Number of pulses increased with stimulus intensities, reaching a plateau at about 18–39 dB above threshold and decreased at higher intensities. Latency to call followed inverse trends relative to number of pulses. Neural audiograms yielded an average best threshold in the high frequency range of 46.6 dB RMS SPL (range 41–51 dB RMS SPL) and a center frequency of 1.9 kHz (range 1.7–2.6 kHz). Auditory thresholds for a synthetic call having a carrier frequency of 2.1 kHz averaged 44 dB RMS SPL (range 39–47 dB RMS SPL). The similarity between thresholds for advertisement calling and auditory thresholds for the advertisement call indicates that male P. thaul use the full extent of their auditory sensitivity in acoustic interactions, likely an evolutionary adaptation allowing chorusing activity in low-density aggregations.     

Efficiency of body conduction of underwater sounds in the bottlenose dolphin

Hearing thresholds of the Black Sea bottlenose dolphin Tursiops truncatus for tonal and composite underwater sounds within 50 kHz were ascertained in fully or partly submerged (head out of water) animals (trained by operant conditioning with food reinforcement). Perception of sounds conducted through the body deteriorated in all cases (thresholds for 75%-correct response rose typically by 6-24 dB); the least changes were observed for 10 and 20 kHz tones. The aggregate data also suggested significant individual variations.     

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko,Gekko subpalmatus

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects’ vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.     

Hearing in coruros (<Emphasis Type="Italic">Spalacopus cyanus</Emphasis>): special audiogram features of a subterranean rodent

Learning curves and behavioural audiograms of subterranean, socially living coruros (Spalacopus cyanus) were obtained using a positive reinforcement conditioning procedure. The individually varying audiograms revealed best hearing at frequencies between 1.25 and 1.6 kHz, which corresponds with the common pattern established in subterranean rodents studied so far. However, the broad hearing range covering frequencies at least between 0.25 and 20 kHz coupled with the high sensitivity (average minimum 7 dB) that is found in coruros are atypical features for audiograms of subterranean rodents, which usually show restricted high-frequency hearing ranges and very poor sensitivity. Hearing at low frequencies (peaks at frequencies <1 kHz), which may be related to sound transmission in underground burrows, and high sensitivity at 1.25/1.6 kHz are discussed in relation to vocalization. In addition to these peaks, a third peak at 8 kHz—probably a plesiomorphic feature of mammals—may be of significance in aboveground communication.     

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.     

Auditory sexual difference in the large odorous frog Odorrana graminea

Acoustic communication is an important behavior in frog courtship. Male and female frogs of most species, except the concave-eared torrent frog Odorrana tormota, have largely similar audiograms. The large odorous frogs (Odorrana graminea) are sympatric with O. tormota, but have no ear canals. The difference in hearing between two sexes of the frog is unknown. We recorded auditory evoked near-field potentials and single-unit responses from the auditory midbrain (the torus semicircularis) to determine auditory frequency sensitivity and threshold. The results show that males have the upper frequency limit at 24 kHz and females have the upper limit at 16 kHz. The more sensitive frequency range is 3–15 kHz for males and 1–8 kHz for females. Males have the minimum threshold at 11 kHz (58 dB SPL), higher about 5 dB than that at 3 kHz for females. The best excitatory frequencies of single units are mostly between 3 and 5 kHz in females and at 7–8 kHz in males. The underlying mechanism of auditory sexual differences is discussed.     

Ranging Behavior of Two Species of Guenons (Cercopithecus lhoesti and C. mitis doggetti) in the Nyungwe Forest Reserve,Rwanda

I studied the ranging behavior of one group of L'Hoest's monkeys (Cercopithecus lhoesti) and one group of blue monkeys (C. mitis doggetti) in the Nyungwe Forest Reserve, Rwanda. This study is the first to examine the ranging behavior of the more terrestrial L'Hoest's monkeys. Fruits composed 47% of blue monkey diet and 24% of the L'Hoest's monkey diet; terrestrial herbaceous vegetation composed 35% of the diet of the latter. While overall abundance of fruit resources in the home range and overall proportion of fruit in the diet were not related to ranging behavior in either group, temporal and spatial availability of specific fruit species was related. Measures of ranging behavior indicated a more concentrated ranging pattern when fruit resources were scarce and dietary diversity increased and when fruit resources were abundant and the groups focused on a few abundant fruit species. Current hypotheses concerning primate ranging behavior suggest that frugivorous species are expected to have greater day ranges and larger home ranges than folivorous species, and invertebrate consumption is expected to produce a more wide-ranging pattern. However, the L'Hoest's monkey group, which was more folivorous and consumed fewer invertebrates, traveled greater daily distances, had a more diverse and longer ranging pattern, and had larger home range areas than the blue monkey group in every month of the study. Both species were highly selective of forest habitats; L'Hoest's monkeys used secondary forest, while blue monkeys preferred primary forest.     

Processing of simple and complex acoustic signals in a tonotopically organized ear

Processing of complex signals in the hearing organ remains poorly understood. This paper aims to contribute to this topic by presenting investigations on the mechanical and neuronal response of the hearing organ of the tropical bushcricket species Mecopoda elongata to simple pure tone signals as well as to the conspecific song as a complex acoustic signal. The high-frequency hearing organ of bushcrickets, the crista acustica (CA), is tonotopically tuned to frequencies between about 4 and 70 kHz. Laser Doppler vibrometer measurements revealed a strong and dominant low-frequency-induced motion of the CA when stimulated with either pure tone or complex stimuli. Consequently, the high-frequency distal area of the CA is more strongly deflected by low-frequency-induced waves than by high-frequency-induced waves. This low-frequency dominance will have strong effects on the processing of complex signals. Therefore, we additionally studied the neuronal response of the CA to native and frequency-manipulated chirps. Again, we found a dominant influence of low-frequency components within the conspecific song, indicating that the mechanical vibration pattern highly determines the neuronal response of the sensory cells. Thus, we conclude that the encoding of communication signals is modulated by ear mechanics.     

Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec.

The measurement of distortion-product otoacoustic emissions is a noninvasive method that can be used for assessing the sensitivity and the frequency tuning of nonlinear cochlear mechanics. During stimulation with two pure tones f1 and f2, the acoustic 2f1-f2 distortion was recorded in the ear canal of Cryptomys spec. to study specializations in cochlear mechanics that could be associated with the presence of a frequency expanded cochlear region between 0.8–1 kHz. In addition, a distortion threshold curve was obtained which describes relative threshold of nonlinear cochlear mechanics. Sensitive distortion thresholds could be measured for stimulus frequencies between 0.4 to 18 kHz with a broad minimum between 0.75 to 2.5 kHz. The distortion threshold curve extends to higher frequencies than previous neuronal data indicated.As a measure of mechanical tuning sharpness in the cochlea, suppression tuning curves of 2f1-f2 were recorded. The tuning curves reflected the typical mammalian pattern with shallow low frequency and steep high frequency slopes. Their tuning sharpness was poor with Q10dB values between 0.3 and 1.88. In the range of the frequency expanded region, the Q10dB values were below 0.5. This finding emphasizes that the presence of frequency expansion does not necessarily lead to enhanced mechanical tuning in the cochlea and one has to consider if in certain bat species with cochlear frequency expansion and particularly sharp cochlear tuning, the two phenomena may not be interlinked.Abbreviations CF constant frequency component of echolocation call - STC suppression tuning curve     

Acoustic irradiation produced by flying moths (Lepidoptera,Noctuidae)

Characteristics of acoustic waves accompanying the flight of noctuid moths (Noctuidae) were measured. The low-frequency part of the spectrum is formed of a series of up to 17 harmonics of the wingbeat frequency (30–50 Hz) with a general tendency toward the decrease in the spectral density and the increase in the sound frequency. The root-mean-square level of the sound pressure from flapping wings was found to be 70–78 dB SPL. Besides low-frequency components, the flight of moths was accompanied by short ultrasonic pulses, which appeared with every wingbeat. Most of the spectral energy was concentrated within a range of 7–150 kHz with the main peaks at 60–110 kHz. The short-term pulses were divided into two or more subpulses with different spectra. The high-frequency pulses were produced at two phases of the wingbeat cycle: during the pronation of the wings at the highest point and at the beginning of their upward movement from the lowest point. In most of the specimens tested, the peak amplitude of sounds varied from 55 to 65 dB SPL at a distance of 6 cm from the insect body. However, in nine noctuid species, no high-frequency acoustic components were recorded. In these experiments, the acoustic flow from the flying moth within a frequency range of 2 to 20 kHz did not exceed the self-noise level of the microphone amplifier (RMS 18 dB SPL). Probable mechanisms of the high frequency acoustic emission during flight, the effect of these sounds on the auditory sensitivity of moths, and the possibility of their self-revealing to insectivorous bats are discussed. In addition, spectral characteristics of the moth echolocation clicks were more precisely determined within the higher frequency range (>100 kHz).     

Effects of Temperature on Auditory Sensitivity in Eurythermal Fishes: Common Carp Cyprinus carpio (Family Cyprinidae) versus Wels Catfish Silurus glanis (Family Siluridae)

Background

In ectothermal animals such as fish, -temperature affects physiological and metabolic processes. This includes sensory organs such as the auditory system. The reported effects of temperature on hearing in eurythermal otophysines are contradictory. We therefore investigated the effect on the auditory system in species representing two different orders.

Methodology/Principal Findings

Hearing sensitivity was determined using the auditory evoked potentials (AEP) recording technique. Auditory sensitivity and latency in response to clicks were measured in the common carp Cyprinus carpio (order Cypriniformes) and the Wels catfish Silurus glanis (order Siluriformes) after acclimating fish for at least three weeks to two different water temperatures (15°C, 25°C and again 15°C). Hearing sensitivity increased with temperature in both species. Best hearing was detected between 0.3 and 1 kHz at both temperatures. The maximum increase occurred at 0.8 kHz (7.8 dB) in C. carpio and at 0.5 kHz (10.3 dB) in S. glanis. The improvement differed between species and was in particular more pronounced in the catfish at 4 kHz. The latency in response to single clicks was measured from the onset of the sound stimulus to the most constant positive peak of the AEP. The latency decreased at the higher temperature in both species by 0.37 ms on average.

Conclusions/Significance

The current study shows that higher temperature improves hearing (lower thresholds, shorter latencies) in eurythermal species from different orders of otophysines. Differences in threshold shifts between eurythermal species seem to reflect differences in absolute sensitivity at higher frequencies and they furthermore indicate differences to stenothermal (tropical) species.