Aerial hearing thresholds and detection of hearing loss in male California sea lions (Zalophus californianus) using auditory evoked potentials

Auditory evoked potential (AEP) measurements are useful for describing the variability of hearing among individuals in marine mammal populations, an important consideration in terms of basic biology and the design of noise mitigation criteria. In this study, hearing thresholds were measured for 16 male California sea lions at frequencies ranging from 0.5 to 32 kHz using the auditory steady state‐response (ASSR), a frequency‐specific AEP. Audiograms for most sea lions were grossly similar to previously reported psychophysical data in that hearing sensitivity increased with increasing frequency up to a steep reduction in sensitivity between 16 and 32 kHz. Average thresholds were not different from AEP thresholds previously reported for male and female California sea lions. Two sea lions from the current study exhibited abnormal audiograms: a 26‐yr‐old sea lion had impaired hearing with a high‐frequency hearing limit (HFHL) between 8 and 16 kHz, and an 8‐yr‐old sea lion displayed elevated thresholds across most tested frequencies. The auditory brainstem responses (ABRs) for these two individuals and an additional 26‐yr‐old sea lion were aberrant compared to those of other sea lions. Hearing loss may have fitness implications for sea lions that rely on sound during foraging and reproductive activities.     

TEMPORARY THRESHOLD SHIFTS AFTER NOISE EXPOSURE IN THE BOTTLENOSE DOLPHIN (TURSIOPS TRUNCATUS) MEASURED USING EVOKED AUDITORY POTENTIALS

The time course of recovery from temporary threshold shift (TTS) was measured in a bottlenose dolphin, Tursiops truncatus , using an evoked-potential procedure. The envelope-following response (EFR), which is a rhythmic train of auditory brainstem responses (ABR) to sinusoidally amplitude-modulated tones, was used as an indicator of the sound reception by the animal. Variation of the intensity of the stimulus allowed us to measure the animal's hearing via EFR thresholds. During each session, following an initial measure of threshold, the trained animal voluntary positioned itself within a hoop 1 m underwater while a 160 dB re 1 μPa noise of a 4–11 kHz bandwidth was presented for 30 min. After the noise exposure, thresholds were measured again at delays of 5, 10, 15, 25, 45, and 105 min. Measurements were made at test frequencies of 8, 11.2, 16, 22.5, and 32 kHz. The maximum TTS occurred 5 min after exposure and rapidly recovered with a rate of around 1.5 dB per doubling of time. TTS occurred at test frequencies from 8 to 16 kHz, with the maximum at 16 kHz. TTS was negligible at 22.5 kHz and absent at 32 kHz.     

Audiogram of the chicken (Gallus gallus domesticus) from 2 Hz to 9 kHz

The pure-tone thresholds of four domestic female chickens were determined from 2 Hz to 9 kHz using the method of conditioned suppression/avoidance. At a level of 60 dB sound pressure level (re 20 μN/m²), their hearing range extends from 9.1 Hz to 7.2 kHz, with a best sensitivity of 2.6 dB at 2 kHz. Chickens have better sensitivity than humans for frequencies below 64 Hz; indeed, their sensitivity to infrasound exceeds that of the homing pigeon. However, when threshold testing moved to the lower frequencies, the animals required additional training before their final thresholds were obtained, suggesting that they may perceive frequencies below 64 Hz differently than higher frequencies.     

Behavioral audiogram of two Arctic foxes (Vulpes lagopus)

With increased polar anthropogenic activity, such as from the oil and gas industry, there are growing concerns about how Arctic species will be affected. Knowledge of species’ sensory abilities, such as auditory sensitivities, can be used to mitigate the effects of such activities. Herein, behavioral audiograms of two captive adult Arctic foxes (Vulpes lagopus) were measured using a yes/no paradigm and descending staircase method of signal presentation. Both foxes displayed a typical mammalian U-shaped audiometric curve, with a functional hearing range of 125 Hz–16 kHz (sensitivity ≤ 60 dB re: 20 μPa) and average peak sensitivity of 24 dB re: 20 μPa at 4 kHz. The foxes had a lower frequency range and sensitivity than would be expected when compared to previous audiograms of domestic dogs (Canis familiaris) and other carnivores. These differences indicate Arctic foxes (V. lagopus) may have a lower frequency range than previously expected, which was similar to the only other fox species tested to date, kit foxes (Vulpes macrotis). Alternatively, differences may be due to testing constraints, such as masking of test signals by ambient noise and/or an unintentionally trained conservative response bias, which most likely resulted in underestimated hearing curves. While results of this study should be interpreted with caution due to its limitations, findings indicate that foxes have a narrower frequency range than formerly presumed. Anthropogenic activities near fox habitats can mitigate their impacts by reducing noise at frequencies within the functional hearing range and peak sensitivities of this species.     

Comparative assessment of amphibious hearing in pinnipeds

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.     

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 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.     

The conduction of tonal and compound sounds through the body of a bottlenose dolphin

The peculiarities of underwater sound conduction through the body of the Black Sea bottlenose dolphin (Tursiops truncatus p.) were investigated to elucidate the mechanisms of acoustic orientation of marine mammals. By using the method of instrumental conditioned reflexes with food reinforcement, underwater hearing thresholds in the bottlenose dolphin depending on signal parameters (tonal pulses and various noises) and sound conduction pathways were measured under conditions of full and partial (with the head out of water and sound being conducted through the body tissues) submergence of the animal into water. The underwater hearing thresholds increased by 6-27 dB upon sound conduction through the body tissues (to the least extent for tonal pulses of 10 and 20 kHz). The hearing thresholds for tonal pulses and narrow-band noises were very similar both under conditions of full and partial submergence of the animal into water.     

Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls

Absolute thresholds and critical masking ratios were determined behaviorally for the European barn owl (Tyto alba guttata). It shows an excellent sensitivity throughout its hearing range with a minimum threshold of −14.2 dB sound pressure level at 6.3 kHz, which is similar to the sensitivity found in the American barn owl (Tyto alba pratincola) and some other owls. Both the European and the American barn owl have a high upper-frequency limit of hearing exceeding that in other bird species. Critical masking ratios, that can provide an estimate for the frequency selectivity in the barn owl's hearing system, were determined with a noise of about 0 dB spectrum level. They increased from 19.1 dB at 2 kHz to 29.2 dB at 8 kHz at a rate of 5.1 dB per octave. The corresponding critical ratio bandwidths were 81, 218, 562 and 831 Hz for test-tone frequencies of 2, 4, 6.3 and 8 kHz, respectively. These values indicate, contrary to expectations based on the spatial representation of frequencies on the basilar papilla, increasing bandwidths of auditory filters in the region of the barn owl's auditory fovea. This increase, however, correlates with the increase in the bandwidths of tuning curves in the barn owl's auditory fovea. Accepted: 27 November 1997     

Ample active acoustic space of a frog from the South American temperate forest

The efficiency of acoustic communication depends on the power generated by the sound source, the attributes of the environment across which signals propagate, the environmental noise and the sensitivity of the intended receivers. Eupsophus emiliopugini, an anuran from the temperate austral forest communicates by means of an advertisement call of moderate intensity within the range for anurans. To estimate the range over which these frogs communicate effectively, we conducted measurements of call sound levels and of auditory thresholds to pure tones and to synthetic conspecific calls. The results show that E. emiliopugini produces advertisement calls of about 84 dB SPL at 0.25 m from the caller. The signals are affected by attenuation as they propagate, reaching average values of about 47 dB SPL at 8 m from the sound source. Midbrain multi-unit recordings show quite sensitive audiograms within the anuran range, with thresholds of about 44 dB SPL for synthetic imitations of conspecific calls, which would allow communication at distances beyond 8 m. This is an extended range as compared to E. calcaratus, a related syntopic species for which a previous study has shown to be restricted to active acoustic spaces shorter than 2 m. The comparison reveals divergent strategies for related taxa communicating amid the same environment.     

Severe constraints for sound communication in a frog from the South American temperate forest

The efficiency of acoustic communication depends on the power generated by the sound source, the quality of the environment across which signals propagate, the environmental noise and the sensitivity of the intended receivers. Eupsophus calcaratus, an anuran from the temperate austral forest, communicates by means of an advertisement call of weak intensity in a sound-attenuating environment. To estimate the range over which these frogs communicate effectively, we conducted measurements of sound level and degradation patterns of propagating advertisement calls in the field, and measurements of auditory thresholds to pure tones and to natural calls in laboratory conditions. The results show that E. calcaratus produces weak advertisement calls of about 72 dB sound pressure level (SPL) at 0.25 m from the caller. The signals are affected by attenuation and degradation patterns as they propagate in their native environment, reaching average values of 61 and 51 dB SPL at 1 and 2 m from the sound source, respectively. Midbrain multi-unit recordings show a relatively low auditory sensitivity, with thresholds of about 58 dB SPL for conspecific calls, which are likely to restrict communication to distances shorter than 2 m, a remarkably short range as compared to other anurans.     

AUDIOMETRIC ASSESSMENT OF NORTHERN FUR SEALS, CALLORHINUS URSINUS

Aerial and underwater audiograms for two young female northern fur seals ( Callorhinus ursinus ) and one young female California sea lion (Zalophus californianus) were obtained with the same procedure and apparatus. Callorhinus hears over a larger frequency range and is more sensitive to airborne sounds than Zalophus or any other pinniped thus far tested in the frequency range of 500 Hz to 32 kHz. Sensitivity of Callorhinus to waterborne pure tones, ranging from 2 to 28 kHz, is equal or superior to all other pinnipeds tested in this same frequency range. Like Zalophus , the upper frequency limit for underwater hearing (as defined by Masterton et al. 1969) in Callorhinus is about one-half octave lower than the three phocid species thus far tested. Callorhinus' upper frequency limit in air is about 36 kHz and under water it is about 40 kHz. Comparison of air and water audiograms shows Callorhinus is no exception to previous behavioral findings demonstrating that the „pinniped ear” is more suitable for hearing in water than in air. Similar to Zalophus and Phoca vitulina, Callorhinus shows an anomalous hearing loss at 4 kHz in air. The basis for this insensitivity to airborne sounds at 4kHz and not at lower or higher frequencies is presumably caused by specialized middle ear mechanisms matching impedance for waterborne sounds. Critical ratio curves for Callorhinus are similarly shaped to ones obtained for humans but are shifted upwards in frequency. Compared to all other marine mammals thus far evaluated, the critical ratios for Callorhinus are the smallest yet reported.     

Potential effects of underwater noise from wind turbines on the marbled rockfish (Sebasticus marmoratus)

Environmental assessments of underwater noise on marine species must be based on species-specific hearing abilities. This study was to assess the potential impact of underwater noise from the East China Sea Bridge wind farm on the acoustic communication of the marbled rockfish. Here, the 1/3 octave frequency band of underwater noise was 125 Hz with the level range of 78–96 dB re 1 μPa, recorded at distances between 15-20m from the foundation at wind speed of 3–5 m/s. Auditory evoked potential (AEP) and passive acoustic techniques were used to determine the hearing abilities and sound production of the fish. The resultes showed the lowest auditory threshold of Sebastiscus marmoratus was 70 dB at 150 Hz matching the disturbance sound ranging 140–180 Hz, which indicating the acoustic communication used in this species. However, the frequency and level of turbine underwater noise overlapped the auditory sensitivity and vocalization of Sebastiscus marmoratus. The wind turbine noise could be detected by fish and may have a masking effect on their acoustic communication. This result can be applied for further to the assessent of fish species released into offshore wind farm marine ranch.     

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.     

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.     

Cigarette Smoking Causes Hearing Impairment among Bangladeshi Population

Lifestyle including smoking, noise exposure with MP3 player and drinking alcohol are considered as risk factors for affecting hearing synergistically. However, little is known about the association of cigarette smoking with hearing impairment among subjects who carry a lifestyle without using MP3 player and drinking alcohol. We showed here the influence of smoking on hearing among Bangladeshi subjects who maintain a lifestyle devoid of using MP3 player and drinking alcohol. A total of 184 subjects (smokers: 90; non-smokers: 94) were included considering their duration and frequency of smoking for conducting this study. The mean hearing thresholds of non-smoker subjects at 1, 4, 8 and 12 kHz frequencies were 5.63±2.10, 8.56±5.75, 21.06±11.06, 40.79±20.36 decibel (dB), respectively and that of the smokers were 7±3.8, 13.27±8.4, 30.66±12.50 and 56.88±21.58 dB, respectively. The hearing thresholds of the smokers at 4, 8 and 12 kHz frequencies were significantly (p<0.05) higher than those of the non-smokers, while no significant differences were observed at 1 kHz frequency. We also observed no significant difference in auditory thresholds among smoker subgroups based on smoking frequency. In contrast, subjects smoked for longer duration (>5 years) showed higher level of auditory threshold (62.16±19.87 dB) at 12 kHz frequency compared with that (41.52±19.21 dB) of the subjects smoked for 1-5 years and the difference in auditory thresholds was statistically significant (p<0.0002). In this study, the Brinkman Index (BI) of smokers was from 6 to 440 and the adjusted odds ratio showed a positive correlation between hearing loss and smoking when adjusted for age and body mass index (BMI). In addition, age, but not BMI, also played positive role on hearing impairment at all frequencies. Thus, these findings suggested that cigarette smoking affects hearing level at all the frequencies tested but most significantly at extra higher frequencies.     

Frequency discrimination by the bottle-nosed dolphin and the Northern fur seal depending on sound parameters and sound conduction pathways

Underwater differential frequency hearing thresholds in the Black Sea bottle-nosed dolphin (Tursiops truncatus p.) and the northern fur seal (Callorhinus ursinus) were measured depending on signal frequency and sound conduction pathways. The measurements were performed by the method of instrumental conditioned reflexes with food reinforcement under conditions of full and partial (with heads out of water at sound conduction through body tissues) submergence of animals into water. It was shown that in a frequency range of 5-100 kHz, underwater differential frequency hearing thresholds of the bottle-nosed dolphin changed from 0.46-0.60% to 0.21-0.34% and depended little on sound conduction pathways. The minimum underwater differential frequency hearing thresholds of the northern fur seal corresponded to the frequencies of maximum hearing sensitivity, changed from 1.7% to 1-2.3% in a frequency range of 1-20 kHz, sharply increased at the edges of the frequency hearing perception range, and depended little (in a range of 5-40 kHz) on sound conduction pathways. Thus, underwater sounds propagating through the body tissues of dolphin and fur seal reach the inner ear.     

Characterization of beam patterns of bottlenose dolphin in the transversal plane

The characteristics of the absolute auditory sensitivity of the bottlenose dolphin (Tursiops truncatus p.) in the transverse plane have been measured using short broad-band stimuli simulating dolphin clicks (with energy maximum at frequencies 8, 16, 30, 50 and 100 kHz). Experiments were performed using the method of conditioned reflexes with food reinforcement. It was shown that, in the frequency range of 8-30 kHz, the absolute sensitivity of dolphin hearing in any ventral and lateral directions of the transverse plane is only by 2-8 dB worse than in the nasal direction. Moreover, it is approximately by 25-30 dB better than at frequencies of 50-100 kHz. At frequencies of 8-30 kHz, a pronounced dorsoventral asymmetry has been observed. In this frequency range, it reaches approximately 15-18 dB whereas at frequencies of 50-100 kHz, this asymmetry decreases to 2-3 dB. In the dorsal direction, the auditory sensitivity is by 18 dB worse than in the nasal one at frequencies of around 8 kHz, and the difference rises smoothly to 33 dB at frequencies of about 100 kHz. At frequencies of 50-100 kHz, the acoustical thresholds of the cross-section plane in comparison with thresholds for the with nasal direction get worse almost uniformly in all directions by 25-33 dB. As a result, in the transversal plane, the beam patterns have a nearly circular form, unlike the patterns at frequencies of 8-30 kHz. The results are discussed in terms of the model of sound perception through the left and right mental foramens. The biological expediency of the asymmetry is emphasized.     

Pacific herring hearing does not include ultrasound

Recent studies have shown that some clupeid fishes, including shad and menhaden, can detect ultrasound (sound with frequencies higher than 20 kHz) and actively avoid it. However, other clupeids, including sardines and anchovies, do not detect ultrasound. The hearing abilities of herring are of particular interest because of their commercial importance, our reliance on acoustics to monitor their populations and behavioural evidence of responses to high-frequency sound by some clupeid species. We measured the hearing sensitivity of Pacific herring (Clupea pallasii) using the auditory brainstem response and found that they were unable to detect ultrasonic signals at received levels up to 185 dB re 1 microPa. Herring had hearing thresholds at lower frequencies (100-5000 Hz) that were typical of other non-ultrasound-detecting clupeids. This lower-frequency hearing sensitivity could explain the results of several earlier studies showing responses to broadband sounds.     

长江和畅洲江段大型船舶的噪声特征及其对长江江豚的潜在影响

长江航运业的快速发展导致长江中船舶数量激增,相应的水体噪声污染可能对同水域的长江江豚（Neophocaena asiaeorientalis asiaeorientalis）产生一定的负面影响,本研究采用宽频录音设备对长江和畅洲北汊非正式通航江段的各类常见大型船舶（长>15m且宽>5m）的航行噪声进行了记录,并分析其峰值-峰值声压级强度（SPLp-p）和功率谱密度（PSD）等。结果表明,大型船舶的航行噪声能量分布频率范围较广（>100kHz）,但主要集中于中低频（<10kHz）部分,各频率（20Hz~144kHz）处的均方根声压级（SPLrms）对环境背景噪声在该频率处的噪声增量范围为3.7~66.5dB。接收到的1/3倍频程声压级（TOL）在各频率处都大于70dB,在8~140kHz频段内都高于长江江豚的听觉阈值。说明大型船舶的航行噪声可能会对长江江豚个体间的声通讯及听觉带来不利影响,如听觉掩盖。