Similar susceptibility to temporary hearing threshold shifts despite different audiograms in harbor porpoises and harbor seals.

When they are exposed to loud fatiguing sounds in the oceans, marine mammals are susceptible to hearing damage in the form of temporary hearing threshold shifts (TTSs) or permanent hearing threshold shifts. We compared the level-dependent and frequency-dependent susceptibility to TTSs in harbor seals and harbor porpoises, species with different hearing sensitivities in the low- and high-frequency regions. Both species were exposed to 100% duty cycle one-sixth-octave noise bands at frequencies that covered their entire hearing range. In the case of the 6.5 kHz exposure for the harbor seals, a pure tone (continuous wave) was used. TTS was quantified as a function of sound pressure level (SPL) half an octave above the center frequency of the fatiguing sound. The species have different audiograms, but their frequency-specific susceptibility to TTS was more similar. The hearing frequency range in which both species were most susceptible to TTS was 22.5-50 kHz. Furthermore, the frequency ranges were characterized by having similar critical levels (defined as the SPL of the fatiguing sound above which the magnitude of TTS induced as a function of SPL increases more strongly). This standardized between-species comparison indicates that the audiogram is not a good predictor of frequency-dependent susceptibility to TTS.

Masking release at 4 and 32 kHz in harbor seals associated with sinusoidal amplitude-modulated masking noise.

Masking can reduce the efficiency of communication and prey and predator detection. Most underwater sounds fluctuate in amplitude, which may influence the amount of masking experienced by marine mammals. The hearing thresholds of two harbor seals for tonal sweeps (centered at 4 and 32 kHz) masked by sinusoidal amplitude modulated (SAM) Gaussian one-third octave noise bands centered around the narrow-band test sweep frequencies, were studied with a psychoacoustic technique. Masking was assessed in relation to signal duration, (500, 1000, and 2000 ms) and masker level, at eight amplitude modulation rates (1-90 Hz). Masking release (MR) due to SAM compared thresholds in modulated and unmodulated maskers. Unmodulated maskers resulted in critical ratios of 21 dB at 4 kHz and 31 dB at 32 kHz. Masked thresholds were similarly affected by SAM rate with the lowest thresholds and the largest MR being observed for SAM rates of 1 and 2 Hz at higher masker levels. MR was higher for 32-kHz maskers than for 4-kHz maskers. Increasing signal duration from 500 ms to 2000 ms had minimal effect on MR. The results are discussed with respect to MR resulting from envelope variation and the impact of noise in the environment on target signal detection.

Masking release at 4 kHz in harbor porpoises (Phocoena phocoena) associated with sinusoidal amplitude-modulated masking noise.

Acoustic masking reduces the efficiency of communication, prey detection, and predator avoidance in marine mammals. Most underwater sounds fluctuate in amplitude. The ability of harbor porpoises (Phocoena phocoena) to detect sounds in amplitude-varying masking noise was examined. A psychophysical technique evaluated hearing thresholds of three harbor porpoises for 500-2000 ms tonal sweeps (3.9-4.1 kHz), presented concurrently with sinusoidal amplitude-modulated (SAM) or unmodulated Gaussian noise bands centered at 4 kHz. Masking was assessed in relation to signal duration and masker level, amplitude modulation rate (1, 2, 5, 10, 20, 40, 80, and 90 Hz), modulation depth (50%, 75%, and 100%) and bandwidth (1/3 or 1 octave). Masking release (MR) due to SAM was assessed by comparing thresholds in modulated and unmodulated maskers. Masked thresholds were affected by SAM rate with the lowest thresholds (i.e., largest MR was 14.5 dB) being observed for SAM rates between 1 and 5 Hz at higher masker levels. Increasing the signal duration from 500-2000 ms increased MR by 3.3 dB. Masker bandwidth and depth of modulation had no substantial effect on MR. The results are discussed with respect to MR resulting from envelope variation and the impact of noise in the environment.

Temporary hearing threshold shift in harbor seals (Phoca vitulina) due to one-sixth-octave noise bands centered at 0.5, 1, and 2 kHz.

This study concludes a larger project on the frequency-dependent susceptibility to noise-induced temporary hearing threshold shift (TTS) in harbor seals (Phoca vitulina). Here, two seals were exposed to one-sixth-octave noise bands (NBs) centered at 0.5, 1, and 2 kHz at several sound exposure levels (SELs, in dB re 1 µPa2s). TTSs were quantified at the center frequency of each NB, half an octave above, and one octave above, at the earliest within 1-4 min after exposure. Generally, elicited TTSs were low, and the highest TTS1-4 occurred at half an octave above the center frequency of the fatiguing sound: after exposure to the 0.5-kHz NB at 210 dB SEL, the TTS1-4 at 0.71 kHz was 2.3 dB; after exposure to the 1-kHz NB at 207 dB SEL, the TTS1-4 at 1.4 kHz was 6.1 dB; and after exposure to the 2-kHz NB at 215 dB SEL, TTS1-4 at 2.8 kHz was 7.9 dB. Hearing always recovered within 60 min, and susceptibility to TTS was similar in both seals. The results show that, for the studied frequency range, the lower the center frequency of the fatiguing sound, the higher the SEL required to cause the same TTS.

Lack of reproducibility of temporary hearing threshold shifts in a harbor porpoise after exposure to repeated airgun sounds.

Noise-induced temporary hearing threshold shift (TTS) was studied in a harbor porpoise exposed to impulsive sounds of scaled-down airguns while both stationary and free-swimming for up to 90 min. In a previous study, ∼4 dB TTS was elicited in this porpoise, but despite 8 dB higher single-shot and cumulative exposure levels (up to 199 dB re 1 µPa2s) in the present study, the porpoise showed no significant TTS at hearing frequencies 2, 4, or 8 kHz. There were no changes in the study animal's audiogram between the studies or significant differences in the fatiguing sound that could explain the difference, but audible and visual cues in the present study may have allowed the porpoise to predict when the fatiguing sounds would be produced. The discrepancy between the studies may have resulted from self-mitigation by the porpoise. Self-mitigation, resulting in reduced hearing sensitivity, can be achieved via changes in the orientation of the head, or via alteration of the hearing threshold by processes in the ear or central nervous system.

Temporary hearing threshold shift in harbor seals (Phoca vitulina) due to a one-sixth-octave noise band centered at 40 kHz.

As part of a series of studies to determine frequency-dependent susceptibility to temporary hearing threshold shifts (TTS), two female harbor seals (F01 and F02) were exposed for 60 min to a one-sixth-octave noise band centered at 40 kHz at mean sound pressure levels ranging from 126 to 153 dB re 1 µPa [mean received sound exposure level (SEL) range: 162-189 dB re 1 µPa2s]. TTSs were quantified at 40, 50, and 63 kHz within 1-4 min of the exposure for F02 and within 12-16 min of the exposure for F01. In F02, significant TTS1-4 (1-4 min post exposure) occurred at 40 kHz with SELs of ≥183 dB re 1 µPa2s and at 50 kHz with SELs of ≥174 dB re 1 µPa2s. At 63 kHz, TTS1-4 occurred with SELs ≥186 dB re 1 µPa2s. In F01, significant TTS12-16 (12-16 min post exposure) occurred only at 50 kHz with SELs of ≥177 dB re 1 µPa2s. The highest TTSs (27.5 dB in F02, 29.8 dB in F01) occurred at 50 kHz, one-third of an octave above the fatiguing sound's center frequency (SEL = 189 dB re 1 µPa2s); recovery took 2 days in F02 and 4 days in F01. In most other cases, recovery was within 1 h. The seals have a similar susceptibility to TTS from 4 to 40 kHz.

Temporary hearing threshold shift in harbor seals (Phoca vitulina) due to a one-sixth-octave noise band centered at 32 kHz.

Two female harbor seals were exposed for 60 min to a continuous one-sixth-octave noise band centered at 32 kHz at sound pressure levels of 92 to 152 dB re 1 µPa, resulting in sound exposure levels (SELs) of 128 to 188 dB re 1 µPa2s. This was part of a larger project determining frequency-dependent susceptibility to temporary threshold shift (TTS) in harbor seals over their entire hearing range. After exposure, TTSs were quantified at 32, 45, and 63 kHz with a psychoacoustic technique. At 32 kHz, only small TTSs (up to 5.9 dB) were measured 1-4 min (TTS1-4) after exposure, and recovery was within 1 h. The higher the SEL, the higher the TTS induced at 45 kHz. Below ∼176 dB re 1 µPa2s, the maximum TTS1-4 was at 32 kHz; above ∼176 dB re 1 µPa2s, the maximum TTS1-4 (up to 33.8 dB) was at 45 kHz. During one particular session, a seal was inadvertently exposed to an SEL of ∼191 dB re 1 µPa2s and at 45 kHz, her TTS1-4 was >45 dB; her hearing recovered over 4 days. Harbor seals appear to be equally susceptible to TTS caused by sounds in the 2.5-32 kHz range.

Temporary hearing threshold shift in harbor seals (Phoca vitulina) due to a one-sixth-octave noise band centered at 16 kHz.

Temporary hearing threshold shifts (TTSs) were investigated in two adult female harbor seals after exposure for 60 min to a continuous one-sixth-octave noise band centered at 16 kHz (the fatiguing sound) at sound pressure levels of 128-149 dB re 1 µPa, resulting in sound exposure levels (SELs) of 164-185 dB re 1 µPa2s. TTSs were quantified at the center frequency of the fatiguing sound (16 kHz) and at half an octave above that frequency (22.4 kHz) by means of a psychoacoustic hearing test method. Susceptibility to TTS was similar in both animals when measured 8-12 and 12-16 min after cessation of the fatiguing sound. TTS increased with increasing SEL at both frequencies, but above an SEL of 174 dB re 1 µPa2s, TTS was greater at 22.4 kHz than at 16 kHz for the same SELs. Recovery was rapid: the greatest TTS, measured at 22.4 kHz 1-4 min after cessation of the sound, was 17 dB, but dropped to 3 dB in 1 h, and hearing recovered fully within 2 h. The affected hearing frequency should be considered when estimating ecological impacts of anthropogenic sound on seals. Between 2.5 and 16 kHz the species appears equally susceptible to TTS.

Acoustic reflectivity of a harbor porpoise (Phocoena phocoena).

Acoustic backscatter measurements were conducted on a stationary harbor porpoise (Phocoena phocoena) under controlled conditions. The measurements were made with the porpoise in the broadside aspect using three different types of signals: (1) a 475 µs linear frequency-modulated (FM) pulse with a frequency range from 23 to 160 kHz; (2) a simulated bottlenose dolphin (Tursiops "truncates") click with a peak frequency of 120 kHz; and (3) a simulated killer whale (Orcinus orca) click with a peak frequency of 60 kHz. The measurement with the FM pulse indicated that the mean target strength at the broadside aspect decreased from -26 to -50 dB as the frequency increased from 23 to 120 kHz in a nearly linear fashion (on a logarithm plot). Target strength variation with frequency was similar to a previous backscatter measurement on a bottlenose dolphin over a comparable frequency range (23-80 kHz). The porpoise seems to be a stealth body with low backscatter properties. The target strength of the porpoise was also about 15-16 dB lower than that of the bottlenose dolphin. The difference in lung volume of the two species when expressed in dB was also approximately 15 dB.

Frequency of greatest temporary hearing threshold shift in harbor seals (Phoca vitulina) depends on fatiguing sound level.

Harbor seals may suffer hearing loss due to intense sounds. After exposure for 60 min to a continuous 6.5 kHz tone at sound pressure levels of 123-159 dB re 1 µPa, resulting in sound exposure levels (SELs) of 159-195 dB re 1 µPa2s, temporary threshold shifts (TTSs) in two harbor seals were quantified at the center frequency of the fatiguing sound (6.5 kHz) and at 0.5 and 1.0 octaves above that frequency (9.2 and 13.0 kHz) by means of a psychoacoustic technique. Taking into account the different timing of post-exposure hearing tests, susceptibility to TTS was similar in both animals. The higher the SEL, the higher the TTS induced at frequencies above the fatiguing sound's center frequency. Below ∼179 dB re 1 µPa2s, the maximum TTS was at the center frequency (6.5 kHz); above ∼179 dB re 1 µPa2s, the maximum TTS was at half an octave above the center frequency (9.2 kHz). These results should be considered when interpreting previous TTS studies, and when estimating ecological impacts of anthropogenic sound on the hearing and ecology of harbor seals. Based on the results of the present study and previous studies, harbor seal hearing, in the frequency range 2.5-6.5 kHz, appears to be approximately equally susceptible to TTS.

Effect of pile-driving sounds on harbor seal (Phoca vitulina) hearing.

Seals exposed to intense sounds may suffer hearing loss. After exposure to playbacks of broadband pile-driving sounds, the temporary hearing threshold shift (TTS) of two harbor seals was quantified at 4 and 8 kHz (frequencies of the highest TTS) with a psychoacoustic technique. The pile-driving sounds had: a 127 ms pulse duration, 2760 strikes per h, a 1.3 s inter-pulse interval, a ∼9.5% duty cycle, and an average received single-strike unweighted sound exposure level (SELss) of 151 dB re 1 µPa2s. Exposure durations were 180 and 360 min [cumulative sound exposure level (SELcum): 190 and 193 dB re 1 µPa2s]. Control sessions were conducted under low ambient noise. TTS only occurred after 360 min exposures (mean TTS: seal 02, 1-4 min after sound stopped: 3.9 dB at 4 kHz and 2.4 dB at 8 kHz; seal 01, 12-16 min after sound stopped: 2.8 dB at 4 kHz and 2.6 dB at 8 kHz). Hearing recovered within 60 min post-exposure. The TTSs were small, due to the small amount of sound energy to which the seals were exposed. Biological TTS onset SELcum for the pile-driving sounds used in this study is around 192 dB re 1 µPa2s (for mean received SELss of 151 dB re 1 µPa and a duty cycle of ∼9.5%).

Hearing thresholds, for underwater sounds, of harbor seals (Phoca vitulina) at the water surface.

High-amplitude impulsive sounds produced by pile driving and airguns may result in hearing damage in nearby seals. By swimming at the water surface, seals may reduce their exposure to underwater sound, as sound pressure levels (SPLs) are often lower just below the surface than deeper in the water column. Seals can make physiological adjustments such that they can switch between having maximum sensitivity for either aerial or underwater sounds. This could mean that hearing sensitivity for underwater sounds is lower when swimming at the water surface (when hearing may be focused on aerial sounds) than when swimming at depth. To investigate this possibility, hearing thresholds of two female harbor seals were quantified psychophysically, while their heads were in the position normally adopted while swimming at the surface. The seals' hearing thresholds at the water surface were similar to each other and to previous measurements made at 1 m depth. When calculating the cumulative sound exposure level for hearing damage assessment, the SPL just below the water surface needs to be measured or modeled, and the proportion of time seals normally swim at the water surface needs to be estimated, to estimate the sound energy that reaches the seals' ears.

Four odontocete species change hearing levels when warned of impending loud sound.

Hearing sensitivity change was investigated when a warning sound preceded a loud sound in the false killer whale (Pseudorca crassidens), the bottlenose dolphin (Tursiops truncatus), the beluga whale (Delphinaperus leucas) and the harbor porpoise (Phocoena phocoena). Hearing sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. When the test/warning stimuli preceded a loud sound, hearing thresholds before the loud sound increased relative to the baseline by 13 to 17 dB. Experiments with multiple frequencies of exposure and shift provided evidence of different amounts of hearing change depending on frequency, indicating that the hearing sensation level changes were not likely due to a simple stapedial reflex.

Spatial avoidance to experimental increase of intermittent and continuous sound in two captive harbour porpoises.

The continuing rise in underwater sound levels in the oceans leads to disturbance of marine life. It is thought that one of the main impacts of sound exposure is the alteration of foraging behaviour of marine species, for example by deterring animals from a prey location, or by distracting them while they are trying to catch prey. So far, only limited knowledge is available on both mechanisms in the same species. The harbour porpoise (Phocoena phocoena) is a relatively small marine mammal that could quickly suffer fitness consequences from a reduction of foraging success. To investigate effects of anthropogenic sound on their foraging efficiency, we tested whether experimentally elevated sound levels would deter two captive harbour porpoises from a noisy pool into a quiet pool (Experiment 1) and reduce their prey-search performance, measured as prey-search time in the noisy pool (Experiment 2). Furthermore, we tested the influence of the temporal structure and amplitude of the sound on the avoidance response of both animals. Both individuals avoided the pool with elevated sound levels, but they did not show a change in search time for prey when trying to find a fish hidden in one of three cages. The combination of temporal structure and SPL caused variable patterns. When the sound was intermittent, increased SPL caused increased avoidance times. When the sound was continuous, avoidance was equal for all SPLs above a threshold of 100 dB re 1 µPa. Hence, we found no evidence for an effect of sound exposure on search efficiency, but sounds of different temporal patterns did cause spatial avoidance with distinct dose-response patterns.

Effects of exposure to sonar playback sounds (3.5 - 4.1 kHz) on harbor porpoise (Phocoena phocoena) hearing.

Safety criteria for naval sonar sounds are needed to protect harbor porpoise hearing. Two porpoises were exposed to sequences of AN/SQS-53C sonar playback sounds (3.5-4.1 kHz, without significant harmonics), at a mean received sound pressure level of 142 dB re 1 µPa, with a duty cycle of 96% (almost continuous). Behavioral hearing thresholds at 4 and 5.7 kHz were determined before and after exposure to the fatiguing sound, in order to quantify temporary threshold shifts (TTSs) and hearing recovery. Control sessions were also conducted. Significant mean initial TTS1-4 of 5.2 dB at 4 kHz and 3.1 dB at 5.7 kHz occurred after 30 min exposures (mean received cumulative sound exposure level, SELcum: 175 dB re 1 µPa2s). Hearing thresholds returned to pre-exposure levels within 12 min. Significant mean initial TTS1-4 of 5.5 dB at 4 kHz occurred after 60 min exposures (SELcum: 178 dB re 1 µPa2s). Hearing recovered within 60 min. The SELcum for AN/SQS-53C sonar sounds required to induce 6 dB of TTS 4 min after exposure (the definition of TTS onset) is expected to be between 175 and 180 dB re 1 µPa2s.

Temporary hearing threshold shift in a harbor porpoise (Phocoena phocoena) after exposure to multiple airgun sounds.

In seismic surveys, reflected sounds from airguns are used under water to detect gas and oil below the sea floor. The airguns produce broadband high-amplitude impulsive sounds, which may cause temporary or permanent threshold shifts (TTS or PTS) in cetaceans. The magnitude of the threshold shifts and the hearing frequencies at which they occur depend on factors such as the received cumulative sound exposure level (SELcum), the number of exposures, and the frequency content of the sounds. To quantify TTS caused by airgun exposure and the subsequent hearing recovery, the hearing of a harbor porpoise was tested by means of a psychophysical technique. TTS was observed after exposure to 10 and 20 consecutive shots fired from two airguns simultaneously (SELcum: 188 and 191 dB re 1 µPa2s) with mean shot intervals of around 17 s. Although most of the airgun sounds' energy was below 1 kHz, statistically significant initial TTS1-4 (1-4 min after sound exposure stopped) of ∼4.4 dB occurred only at the hearing frequency 4 kHz, and not at lower hearing frequencies tested (0.5, 1, and 2 kHz). Recovery occurred within 12 min post-exposure. The study indicates that frequency-weighted SELcum is a good predictor for the low levels of TTS observed.

Acoustic dose-behavioral response relationship in sea bass (Dicentrarchus labrax) exposed to playbacks of pile driving sounds.

The foundations of offshore wind turbines are attached to the sea bed by percussion pile driving. Pile driving sounds may affect the behavior of fish. Acoustic dose-behavioral response relationships were determined for sea bass in a pool exposed for 20 min to pile driving sounds at seven mean received root-mean-square sound pressure levels [SPLrms; range: 130-166 dB re 1 µPa; single strike sound exposure level (SELss) range: 122-158; 6 dB steps]. Initial responses (sudden, short-lived changes in swimming speed and direction) and sustained responses (changes in school cohesion, swimming depth, and speed) were quantified. The 50% initial response threshold occurred at an SELss of 131 dB re 1 µPa2 s for 31 cm fish and 141 dB re 1 µPa2 s for 44 cm fish; the small fish thus reacted to lower SELss than the large fish. Analysis showed that there is no evidence, even at the highest sound level, for any consistent sustained response to sound exposure by the study animals. If wild sea bass are exposed to pile driving sounds at the levels used in the present study, there are unlikely to be any adverse effects on their ecology, because the initial responses after the onset of the piling sound observed in this study were short-lived.

Hearing thresholds of a male and a female harbor porpoise (Phocoena phocoena).

To study intra-species variability in audiograms, the hearing sensitivity of a six-year-old female and a three-year-old male harbor porpoise was measured by using a standard psycho-acoustic technique under low ambient noise conditions. The porpoises' hearing thresholds for 13 narrow-band sweeps with center frequencies between 0.125 and 150 kHz were established. The resulting audiograms were U-shaped and similar. The main difference (25 dB) in mean thresholds between the two porpoises was at the high-frequency end of the hearing range (at 150 kHz). Maximum sensitivity (47 dB re 1 µPa for the female and 44 dB re 1 µPa for the male) occurred at 125 kHz. The range of most sensitive hearing (defined as within 10 dB of maximum sensitivity) was from 16 to ∼140 kHz. Sensitivity declined sharply above 125 kHz. All five porpoises for which a valid behavioral audiogram now exists were rehabilitated stranded animals, all were tested with similar psycho-acoustic techniques, and all had similar audiograms. The present study provides further evidence to confirm that the hearing range and sensitivity of the first three harbor porpoises, which have been used in secondary research and on which policy decisions have been based, are representative of those of young harbor porpoises in general.

Conditioned hearing sensitivity change in the harbor porpoise (Phocoena phocoena).

Hearing sensitivity, during trials in which a warning sound preceding a loud sound, was investigated in two harbor porpoises (Phocoena phocoena). Sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. When a hearing test/warning stimulus, with a frequency of either 45 or 32 kHz, preceded a loud 32 kHz tone with a sound pressure level of 152 dB re 1 µPa root mean square, lasting 2 s yielding an sound exposure level (SEL) of 155 dB re 1 µPa(2)s, pooled hearing thresholds measured just before the loud sound increased relative to baseline thresholds. During two experimental sessions the threshold increased up to 17 dB for the test frequency of 45 kHz and up to 11 dB for the test frequency of 32 kHz. An extinction test revealed very rapid threshold recovery within the first two experimental sessions. The SEL producing the hearing dampening effect was low compared to previous other odontocete hearing change efforts with each individual trial equal to 155 dB re 1 µPa(2) but the cumulative SEL for each subsession may have been as high as 168 dB re 1 µPa(2). Interpretations of conditioned hearing sensation change and possible change due to temporary threshold shifts are considered for the harbor porpoise and discussed in the light of potential mechanisms and echolocation.

Pile driving playback sounds and temporary threshold shift in harbor porpoises (Phocoena phocoena): Effect of exposure duration.

High intensity underwater sounds may cause temporary hearing threshold shifts (TTSs) in harbor porpoises, the magnitude of which may depend on the exposure duration. After exposure to playbacks of pile driving sounds, TTSs in two porpoises were quantified at 4 and 8 kHz with a psychophysical technique. At 8 kHz, the pile driving sounds caused the highest TTS. Pile driving sounds had the following: pulse duration 124 ms, rate 2760 strikes/h, inter-pulse interval 1.3 s, duty cycle ∼9.5%, average received single-strike unweighted broadband sound exposure level (SELss) 145 dB re 1 µPa(2)s, exposure duration range 15-360 min (cumulative SEL range: 173-187 dB re 1 µPa(2)s). Control sessions were also carried out. Mean TTS (1-4 min after sound exposure stopped in one porpoise, and 12-16 min in the other animal) increased from 0 dB after 15 min exposure to 5 dB after 360 min exposure. Recovery occurred within 60 min post-exposure. For the signal duration, sound pressure level (SPL), and duty cycle used, the TTS onset SELcum is estimated to be around 175 dB re 1 µPa(2)s. The small increase in TTS between 15 and 360 min exposures is due to the small amount of sound energy per unit of time to which the porpoises were exposed [average (over time) broadband SPL ∼144 dB re 1 µPa].