Temporary threshold shift in bottlenose dolphins exposed to steady-state, 1/6-octave noise centered at 0.5 to 80 kHza).

Temporary threshold shift (TTS) was measured in bottlenose dolphins after 1-h exposures to 1/6-octave noise centered at 0.5, 2, 8, 20, 40, and 80 kHz. Tests were conducted in netted ocean enclosures, with the dolphins free-swimming during noise exposures. Exposure levels were estimated using a combination of video-based measurement of dolphin position, calibrated exposure sound fields, and animal-borne archival recording tags. Hearing thresholds were measured before and after exposures using behavioral methods (0.5, 2, 8 kHz) or behavioral and electrophysiological [auditory brainstem response (ABR)] methods (20, 40, 80 kHz). No substantial effects of the noise were seen at 40 and 80 kHz at the highest exposure levels. At 2, 8, and 20 kHz, exposure levels required for 6 dB of TTS (onset TTS exposures) were similar to previous studies; however, at 0.5 kHz, onset TTS was much lower than predicted values. No clear relationships could be identified between ABR- and behaviorally measured TTS. The results raise questions about the validity of current noise exposure guidelines for dolphins at frequencies below ∼1 kHz and how to accurately estimate received noise levels from free-swimming animals.

Bottlenose dolphin temporary threshold shift following exposure to 10-ms impulses centered at 8 kHza).

Studies of marine mammal temporary threshold shift (TTS) from impulsive sources have typically produced small TTS magnitudes, likely due to much of the energy in tested sources lying below the subjects' range of best hearing. In this study of dolphin TTS, 10-ms impulses centered at 8 kHz were used with the goal of inducing larger magnitudes of TTS and assessing the time course of hearing recovery. Most impulses had sound pressure levels of 175-180 dB re 1 µPa, while inter-pulse interval (IPI) and total number of impulses were varied. Dolphin TTS increased with increasing cumulative sound exposure level (SEL) and there was no apparent effect of IPI for exposures with equal SEL. The lowest TTS onset was 184 dB re 1 µPa2s, although early exposures with 20-s IPI and cumulative SEL of 182-183 dB re 1 µPa2s produced respective TTS of 35 and 16 dB in two dolphins. Continued testing with higher SELs up to 191 dB re 1 µPa2s in one of those dolphins, however, failed to result in TTS greater than 14 dB. Recovery rates were similar to those from other studies with non-impulsive sources and depended on the magnitude of the initial TTS.

Dolphins reduce hearing sensitivity in anticipation of repetitive impulsive noise exposures.

The auditory steady-state response (ASSR) was continuously measured in two bottlenose dolphins during impulse noise exposures to determine whether observed head movements coincided with actual changes to auditory system sensitivity. Impulses were generated by a seismic air gun at a fixed inter-pulse interval of 10 s. ASSR amplitudes were extracted from the instantaneous electroencephalogram using coherent averaging within a sliding analysis window. A decline in ASSR amplitude was seen during the time interval between air gun impulses, followed by an elevation in ASSR amplitude immediately after each impulse. Similar patterns were not observed during control trials where air gun impulses were not generated. The results suggest that the dolphins learned the timing of the impulse noise sequences and lowered their hearing sensitivity before each impulse, presumably to lessen the auditory effects of the noise. The specific mechanisms responsible for the observed effects are at present unknown.

Directional hearing sensitivity for 2-30 kHz sounds in the bottlenose dolphin (Tursiops truncatus).

Bottlenose dolphins (Tursiops truncatus) depend on sounds at frequencies lower than 30 kHz for social communication, but little information on the directional dependence of hearing thresholds for these frequencies exists. This study measured underwater behavioral hearing thresholds for 2, 10, 20, and 30 kHz sounds projected from eight different positions around dolphins in both the horizontal and vertical planes. The results showed that the sound source direction relative to the dolphin affected hearing threshold, and that directional characteristics of the receiving beam pattern were frequency dependent. Hearing thresholds obtained from two adult dolphins demonstrated a positive relationship between directivity of hearing and stimulus frequency, with asymmetric receiving beam patterns in both the horizontal and vertical planes. Projecting sound from directly behind the dolphin resulted in frequency-dependent increases in hearing threshold up to 18.5 dB compared to when sound was projected in front. When the projector was situated above the dolphin thresholds were approximately 8 dB higher as compared to below. This study demonstrates that directional hearing exists for lower frequencies than previously expected.

Bottlenose dolphin (Tursiops truncatus) discrimination of harmonic stimuli with range-dependent signal degradation.

The importance of perceived sound source distance has been noted in controlled exposure studies with free-ranging marine mammals. Different behavioral reactions have been observed for sonar exposures with a similar received level but differing source distances. This psychophysical study examined bottlenose dolphins' use of range-dependent acoustic features in classifying frequency-modulated tonal stimuli (∼10-kHz fundamental). Repetitive tones with simulated range-dependent high-frequency attenuation (HFA) and reverberation (REV) were presented with roving levels (levels varied ±10 dB). The dolphins were trained to produce a phonic response upon hearing tones simulating relatively distant 30-km sources and to withhold response for closer-range tones. Once this behavior was reliably performed, probe trials with intermediate ranges were used to examine stimulus classification based on HFA and REV. Dolphins responded to nearly all probe trials with ranges of 10 and 20 km, while responses were less frequent at 1 and 2 km. Probes with HFA and REV decoupled from simulated source distance indicated that the dolphins used HFA to a greater degree than REV in response decisions. These results suggest that dolphins can classify harmonic signals based on range-dependent HFA and REV independent of received level, making these cues potentially useful in deciding behavioral reactions to acoustic sources.

Neural representation of the self-heard biosonar click in bottlenose dolphins (Tursiops truncatus).

The neural representation of the dolphin broadband biosonar click was investigated by measuring auditory brainstem responses (ABRs) to "self-heard" clicks masked with noise bursts having various high-pass cutoff frequencies. Narrowband ABRs were obtained by sequentially subtracting responses obtained with noise having lower high-pass cutoff frequencies from those obtained with noise having higher cutoff frequencies. For comparison to the biosonar data, ABRs were also measured in a passive listening experiment, where external clicks and masking noise were presented to the dolphins and narrowband ABRs were again derived using the subtractive high-pass noise technique. The results showed little change in the peak latencies of the ABR to the self-heard click from 28 to 113 kHz; i.e., the high-frequency neural responses to the self-heard click were delayed relative to those of an external, spectrally "pink" click. The neural representation of the self-heard click is thus highly synchronous across the echolocation frequencies and does not strongly resemble that of a frequency modulated downsweep (i.e., decreasing-frequency chirp). Longer ABR latencies at higher frequencies are hypothesized to arise from spectral differences between self-heard clicks and external clicks, forward masking from previously emitted biosonar clicks, or neural inhibition accompanying the emission of clicks.

Using Reaction Time and Equal Latency Contours to Derive Auditory Weighting Functions in Sea Lions and Dolphins.

Subjective loudness measurements are used to create equal-loudness contours and auditory weighting functions for human noise-mitigation criteria; however, comparable direct measurements of subjective loudness with animal subjects are difficult to conduct. In this study, simple reaction time to pure tones was measured as a proxy for subjective loudness in a Tursiops truncatus and Zalophus californianus. Contours fit to equal reaction-time curves were then used to estimate the shapes of auditory weighting functions.

Auditory Effects of Multiple Impulses from a Seismic Air Gun on Bottlenose Dolphins (Tursiops truncatus).

Auditory thresholds were measured in three bottlenose dolphins before and after exposure to ten impulses from a seismic air gun. Thresholds were measured using behavioral and electrophysiological methods to determine the amount of temporary threshold shift induced. The results suggest that the potential for seismic surveys using air guns to cause auditory effects on dolphins may be lower than previously predicted; however, two of the three dolphins exhibited "anticipatory" behavioral changes at the highest exposure condition that suggested they were attempting to mitigate the effects of the exposures.

Equal latency contours for bottlenose dolphins (Tursiops truncatus) and California sea lions (Zalophus californianus).

Loudness perception by non-human animals is difficult to study directly. Previous research efforts have instead focused on estimating loudness perception using simple reaction time (RT) data. These data are used to generate equal latency contours that serve as a proxy for equal loudness contours. To aid the design of auditory weighting functions for marine mammals, equal latency contours were generated using RT data for two marine mammal species that are representative of broader functional hearing groups: the bottlenose dolphin (under water) and California sea lion (in air). In all cases, median RT decreased with increasing tone sound pressure level (SPL). The equal latency contours corresponding to near-threshold SPLs were similar to audiograms for both species. The sea lion contours showed some compression at frequencies below 1 kHz; however, a similar pattern was not apparent in the more variable data for dolphins. Equal latency contours for SPLs greater than approximately 40 dB above threshold diverged from predicted equal loudness contours, likely due to the asymptotic nature of RT at the highest tested SPLs. The results suggest that auditory threshold data, potentially augmented with compression at low frequencies, may provide a useful way forward when designing auditory weighting functions for marine mammals.

Effects of multiple impulses from a seismic air gun on bottlenose dolphin hearing and behavior.

To investigate the auditory effects of multiple underwater impulses, hearing thresholds were measured in three bottlenose dolphins before and after exposure to 10 impulses produced by a seismic air gun. Thresholds were measured at multiple frequencies using both psychophysical and electrophysiological (auditory evoked potential) methods. Exposures began at relatively low levels and gradually increased over a period of several months. The highest exposures featured peak sound pressure levels from 196 to 210 dB re 1 µPa, peak-peak sound pressure levels of 200-212 dB re 1 µPa, and cumulative (unweighted) sound exposure levels from 193 to 195 dB re 1 µPa(2)s. At the cessation of the study, no significant increases were observed in psychophysical thresholds; however, a small (9 dB) shift in mean auditory evoked potential thresholds, accompanied by a suppression of the evoked potential amplitude function, was seen in one subject at 8 kHz. At the highest exposure condition, two of the dolphins also exhibited behavioral reactions indicating that they were capable of anticipating and potentially mitigating the effects of impulsive sounds presented at fixed time intervals.

Effects of fatiguing tone frequency on temporary threshold shift in bottlenose dolphins (Tursiops truncatus).

Temporary threshold shift (TTS) was measured in two bottlenose dolphins (Tursiops truncatus) after exposure to 16-s tones between 3 and 80 kHz to examine the effects of exposure frequency on the onset, growth, and recovery of TTS. Hearing thresholds were measured approximately one-half octave above the exposure frequency using a behavioral response paradigm featuring an adaptive staircase procedure. Results show frequency-specific differences in TTS onset and growth, and suggest increased susceptibility to auditory fatigue for frequencies between approximately 10 and 30 kHz. Between 3 and 56 kHz, the relationship between exposure frequency and the exposure level required to induce 6 dB of TTS, measured 4 min post-exposure, agrees closely with an auditory weighting function for bottlenose dolphins developed from equal loudness contours [Finneran and Schlundt. (2011). J. Acoust. Soc. Am. 130, 3124-3136].

Subjective loudness level measurements and equal loudness contours in a bottlenose dolphin (Tursiops truncatus).

Loudness level measurements in human listeners are straightforward; however, it is difficult to convey the concepts of loudness matching or loudness comparison to (non-human) animals. For this reason, prior studies have relied upon objective measurements, such as response latency, to estimate equal loudness contours in animals. In this study, a bottlenose dolphin was trained to perform a loudness comparison test, where the listener indicates which of two sequential tones is louder. To enable reward of the dolphin, most trials featured tones with identical or similar frequencies, but relatively large sound pressure level differences, so that the loudness relationship was known. A relatively small percentage of trials were "probe" trials, with tone pairs whose loudness relationship was not known. Responses to the probe trials were used to construct psychometric functions describing the loudness relationship between a tone at a particular frequency and sound pressure level and that of a reference tone at 10 kHz with a sound pressure level of 90, 105, or 115 dB re 1 µPa. The loudness relationships were then used to construct equal loudness contours and auditory weighting functions that can be used to predict the frequency-dependent effects of noise on odontocetes.

Dolphin and sea lion auditory evoked potentials in response to single and multiple swept amplitude tones.

Measurement of the auditory steady-state response (ASSR) is increasingly used to assess marine mammal hearing. These tests normally entail measuring the ASSR to a sequence of sinusoidally amplitude modulated tones, so that the ASSR amplitude function can be defined and the auditory threshold estimated. In this study, an alternative method was employed, where the ASSR was elicited by an amplitude modulated stimulus whose sound pressure level was slowly varied, or "swept," over a range of levels believed to bracket the threshold. The ASSR amplitude function was obtained by analyzing the resulting grand average evoked potential using a short-time Fourier transform. The suitability of this technique for hearing assessment of bottlenose dolphins and California sea lions was evaluated by comparing ASSR amplitude functions and thresholds obtained with swept amplitude and discrete, constant amplitude stimuli. When factors such as the number of simultaneous tones, the number of averages, and the frequency analysis window length were taken into account, the performance and time required for the swept-amplitude and discrete stimulus techniques were similar. The decision to use one technique over another depends on the relative importance of obtaining suprathreshold information versus the lowest possible thresholds.

Auditory evoked potentials in two short-finned pilot whales (Globicephala macrorhynchus).

The hearing sensitivities of two short-finned pilot whales (Globicephala macrorhynchus) were investigated by measuring auditory evoked potentials generated in response to clicks and sinusoidal amplitude modulated (SAM) tones. The first whale tested, an adult female, was a long-time resident at SeaWorld San Diego with a known health history. Click-evoked responses in this animal were similar to those measured in other echolocating odontocetes. Auditory thresholds were comparable to dolphins of similar age determined with similar evoked potential methods. The region of best sensitivity was near 40 kHz and the upper limit of functional hearing was between 80 and 100 kHz. The second whale tested, a juvenile male, was recently stranded and deemed non-releasable. Click-evoked potentials were not detected in this animal and testing with SAM tones suggested severe hearing loss above 10 kHz.

Frequency-dependent and longitudinal changes in noise-induced hearing loss in a bottlenose dolphin (Tursiops truncatus).

Temporary threshold shift (TTS) was measured in a bottlenose dolphin (Tursiops truncatus) after exposure to 16-s tones at 3 and 20 kHz to examine the effects of exposure frequency on the onset and growth of TTS. Thresholds were measured approximately one-half octave above the exposure frequency using a behavioral response paradigm featuring an adaptive staircase procedure. Preliminary data provide evidence of frequency-specific differences in TTS onset and growth, and increased susceptibility to auditory fatigue after exposure to 3-kHz tones compared to data obtained two years earlier.

Growth and recovery of temporary threshold shift at 3 kHz in bottlenose dolphins: experimental data and mathematical models.

Measurements of temporary threshold shift (TTS) in marine mammals have become important components in developing safe exposure guidelines for animals exposed to intense human-generated underwater noise; however, existing marine mammal TTS data are somewhat limited in that they have typically induced small amounts of TTS. This paper presents experimental data for the growth and recovery of larger amounts of TTS (up to 23 dB) in two bottlenose dolphins (Tursiops truncatus). Exposures consisted of 3-kHz tones with durations from 4 to 128 s and sound pressure levels from 100 to 200 dB re 1 µPa. The resulting TTS data were combined with existing data from two additional dolphins to develop mathematical models for the growth and recovery of TTS. TTS growth was modeled as the product of functions of exposure duration and sound pressure level. TTS recovery was modeled using a double exponential function of the TTS at 4-min post-exposure and the recovery time.

Temporary threshold shift in a bottlenose dolphin (Tursiops truncatus) exposed to intermittent tones.

Temporary threshold shift (TTS) was measured in a bottlenose dolphin exposed to a sequence of four 3-kHz tones with durations of 16 s and sound pressure levels (SPLs) of 192 dB re 1 µPa. The tones were separated by 224 s of silence, resulting in duty cycle of approximately 7%. The resulting growth and recovery of TTS were compared to experimentally measured TTS in the same subject exposed to single, continuous tones with similar SPLs. The data confirm the potential for accumulation of TTS across multiple exposures and for recovery of hearing during the quiet intervals between exposures. The degree to which various models could predict the growth of TTS across multiple exposures was also examined.

Underwater sound pressure variation and bottlenose dolphin (Tursiops truncatus) hearing thresholds in a small pool.

Studies of underwater hearing are often hampered by the behavior of sound waves in small experimental tanks. At lower frequencies, tank dimensions are often not sufficient for free field conditions, resulting in large spatial variations of sound pressure. These effects may be mitigated somewhat by increasing the frequency bandwidth of the sound stimulus, so effects of multipath interference average out over many frequencies. In this study, acoustic fields and bottlenose dolphin (Tursiops truncatus) hearing thresholds were compared for pure tone and frequency modulated signals. Experiments were conducted in a vinyl-walled, seawater-filled pool approximately 3.7 x 6 x 1.5 m. Acoustic signals were pure tone and linear and sinusoidal frequency modulated tones with bandwidths/modulation depths of 1%, 2%, 5%, 10%, and 20%. Thirteen center frequencies were tested between 1 and 100 kHz. Acoustic fields were measured (without the dolphin present) at three water depths over a 60 x 65 cm grid with a 5-cm spacing. Hearing thresholds were measured using a behavioral response paradigm and up/down staircase technique. The use of FM signals significantly improved the sound field without substantially affecting the measured hearing thresholds.