Underwater Hearing Thresholds Research Articles

Aerial hearing thresholds and ecoacoustics of a threatened pursuit-diving seabird, the marbled murrelet Brachyramphus marmoratus

As humans increasingly utilize sensitive coastal areas, diving seabirds like the marbled murrelet Brachyramphus marmoratus face a unique combination of exposure to pervasive anthropogenic sound and acoustically mediated disturbances in terrestrial and marine environments. Despite its threatened status, the sound sensitivities and sensory ecology of this species are unknown, limiting any predictions of the frequencies or sound levels that may induce acoustic impacts. In this study, we measured electrophysiological aerial hearing thresholds for 10 wild individuals captured, sedated, examined inside a field-deployed anechoic chamber and subsequently released. Auditory responses were detected across a 0.5 to 6 kHz frequency range. The median auditory threshold was lowest at 2 kHz (33 dB), while hearing was generally sensitive between 0.75 and 3.8 kHz. B. marmoratus thresholds were elevated compared to other studied alcid species. In-air sensitivities were used to provide an initial prediction of underwater hearing thresholds. To further explore the auditory sensory ecology of this solitary-nesting species, hearing data were also compared to short-term recordings (5 d) of the aerial soundscape of a marbled murrelet nesting habitat. The soundscape contained both abiotic and biotic sounds that contributed to broadband sound levels of 46-55 dB re: 20 µPa rms (0.2-10 kHz). This comparatively quiet habitat enabled relatively frequent detection of anthropogenic sounds within the soundscape. Energy from this acoustic pollution consistently overlapped marbled murrelet sound sensitivities, indicating that the species is susceptible to disturbance from a range of noise types.

Is human underwater hearing mediated by bone conduction?

In-air and underwater audiograms and directional hearing abilities were measured in humans. The lowest underwater thresholds were 2.8 µW/m2 or 3.6 mPa at a frequency of 500 Hz. The underwater hearing thresholds were 4–26 dB and 40–62 dB higher than in-air hearing thresholds when measured in intensity and pressure units, respectively. This difference is considerably smaller than what has been reported earlier. At frequencies below 1 kHz, when measured in units of particle velocity, the underwater threshold was much lower than published bone conduction thresholds, suggesting that underwater hearing is not always mediated by bone conduction pathways to the inner ear, as previously thought. We suggest it is the resonance of air in the air-filled middle ear that produces the low underwater thresholds, at least at frequencies below 1 kHz. The ability to determine the direction of a 700 Hz underwater sound source while being blindfolded was extremely poor, with submerged test subjects showing only coarse directional hearing abilities at azimuths of less than 50˚. The physical cues to sound direction are different in air and water, and the poor directional hearing abilities indicate that, in spite of low hearing thresholds, humans have no special adaptations to process directional acoustic cues under water.

Effects of dolphin hearing bandwidth on biosonar click emissions.

Differences in odontocete biosonar emissions have been reported for animals with hearing loss compared to those with normal hearing. For example, some animals with high-frequency hearing loss have been observed to lower the dominant frequencies of biosonar signals to better match a reduced audible frequency range. However, these observations have been limited to only a few individuals and there has been no systematic effort to examine how animals with varying degrees of hearing loss might alter biosonar click properties. In the present study, relationships between age, biosonar click emissions, auditory evoked potentials (AEPs), and hearing bandwidth were studied in 16 bottlenose dolphins (Tursiops truncatus) of various ages and hearing capabilities. Underwater hearing thresholds were estimated by measuring steady-state AEPs to sinusoidal amplitude modulated tones at frequencies from 23 to 152 kHz. Input-output functions were generated at each tested frequency and used to calculate frequency-specific thresholds and the upper-frequency limit of hearing for each subject. Click emissions were measured during a biosonar aspect change detection task using a physical target. Relationships between hearing capabilities and the acoustic parameters of biosonar signals are described here and compared to previous experiments with fewer subjects.

Relationship between biosonar click emissions, age, and hearing bandwidth in bottlenose dolphins, Tursiops truncatus

Previous studies have reported changes in biosonar emissions in a few odontocete subjects as audible frequency range is reduced with increasing age (i.e., presbycusis). For example, some animals have been observed to lower the dominant frequencies of their biosonar clicks to better match their reduced audible frequency range. In the present study, relationships between age, biosonar click emissions, auditory evoked potentials, and hearing bandwidth were studied in 10 bottlenose dolphins (Tursiops truncatus) of various ages and hearing capabilities. Underwater hearing thresholds were estimated by measuring steady-state auditory evoked potentials to sinusoidal amplitude modulated tones at frequencies from 20 to 160 kHz. Input-output functions were generated at each tested frequency and used to calculate frequency-specific thresholds and the upper cut-off frequency of hearing for each subject. Click emissions were measured during a physical target aspect change detection task at a fixed range of 10 m. Relationships between hearing thresholds and the acoustic parameters of biosonar signals will be presented and compared to previous experiments with fewer subjects. [Work supported by the Office of Naval Research.]

Low-frequency temporary threshold shift not observed in spotted or ringed seals exposed to single air gun impulses.

Underwater hearing thresholds were measured at 100 Hz in trained spotted (Phoca largha) and ringed seals (Pusa hispida) before and immediately following voluntary exposure to impulsive noise from a seismic air gun. Auditory responses were determined from psychoacoustic data and behavioral responses were scored from video recordings. Four successive exposure conditions of increasing level were tested, with received unweighted sound exposure levels from 165 to 181 dB re 1 μPa2 s and peak-to-peak sound pressures from 190 to 207 dB re 1 μPa. There was no evidence that these single seismic exposures altered hearing-including in the highest exposure condition, which matched previous predictions of temporary threshold shift (TTS) onset. Following training at low exposure levels, relatively mild behavioral responses were observed for higher exposure levels. This demonstrates that individuals can learn to tolerate loud, impulsive sounds, but does not necessarily imply that similar sounds would not elicit stronger behavioral responses in wild seals. The absence of observed TTS confirms that regulatory guidelines (based on M-weighting) for single impulse noise exposures are conservative for seals. However, additional studies using multiple impulses and/or higher exposure levels are needed to quantify exposure conditions that do produce measurable changes in hearing sensitivity.

Underwater Hearing in Turtles.

The hearing of turtles is poorly understood compared with the other reptiles. Although the mechanism of transduction of sound into a neural signal via hair cells has been described in detail, the rest of the auditory system is largely a black box. What is known is that turtles have higher hearing thresholds than other reptiles, with best frequencies around 500 Hz. They also have lower underwater hearing thresholds than those in air, owing to resonance of the middle ear cavity. Further studies demonstrated that all families of turtles and tortoises share a common middle ear cavity morphology, with scaling best suited to underwater hearing. This supports an aquatic origin of the group. Because turtles hear best under water, it is important to examine their vulnerability to anthropogenic noise. However, the lack of basic data makes such experiments difficult because only a few species of turtles have published audiograms. There are also almost no behavioral data available (understandable due to training difficulties). Finally, few studies show what kinds of sounds are behaviorally relevant. One notable paper revealed that the Australian snake-necked turtle (Chelodina oblonga) has a vocal repertoire in air, at the interface, and under water. Findings like these suggest that there is more to the turtle aquatic auditory scene than previously thought.

Experimental Analysis of the Mechanism of Hearing under Water.

The mechanism of human hearing under water is debated. Some suggest it is by air conduction (AC), others by bone conduction (BC), and others by a combination of AC and BC. A clinical bone vibrator applied to soft tissue sites on the head, neck, and thorax also elicits hearing by a mechanism called soft tissue conduction (STC) or nonosseous BC. The present study was designed to test whether underwater hearing at low intensities is by AC or by osseous BC based on bone vibrations or by nonosseous BC (STC). Thresholds of normal hearing participants to bone vibrator stimulation with their forehead in air were recorded and again when forehead and bone vibrator were under water. A vibrometer detected vibrations of a dry human skull in all similar conditions (in air and under water) but not when water was the intermediary between the sound source and the skull forehead. Therefore, the intensities required to induce vibrations of the dry skull in water were significantly higher than the underwater hearing thresholds of the participants, under conditions when hearing by AC and osseous BC is not likely. The results support the hypothesis that hearing under water at low sound intensities may be attributed to nonosseous BC (STC).

Subject-based calibration of a jawphone transducer with a bottlenose dolphin (Tursiops truncatus)

Hearing studies with odontocete cetaceans often use suction-cup transducers known as``jawphones” to imitate underwater stimulus transmission. Jawphones are typically calibrated by measuring a frequency-response curve with a receiving hydrophone placed at a controlled distance in an underwater direct field. This procedure is somewhat controversial, as it may not sufficiently reproduce the odontocete sound reception pathway. This study calibrated a jawphone by comparing two behavioral audiograms for a single bottlenose dolphin. The first audiogram comprised underwater hearing thresholds (in dB re 1 μPa) measured using direct-field stimulation, the second comprised thresholds (in dBV) measured using a jawphone. All thresholds were measured using a psychophysical staircase procedure at frequencies from 14.1 to 150 kHz. The calibration curve was calculated by subtracting, at matched frequencies, jawphone thresholds from underwater direct-field thresholds. The resulting curve had the shape of a bandpass filter, with highest levels at frequencies from 56.6 to 130 kHz. This subject-based curve was similar in shape to a previously obtained direct-field calibration curve, although the subject-based values were higher above 20 kHz. These results are especially relevant to auditory evoked potential hearing studies that measure thresholds in odontocetes that are untrained for psychophysical procedures. [Work supported by ONR.]

The effect of signal duration on the underwater hearing thresholds of two harbor seals (Phoca vitulina) for single tonal signals between 0.2 and 40 kHz

The underwater hearing sensitivities of two 2-year-old female harbor seals were quantified in a pool built for acoustic research by using a behavioral psycho-acoustic technique. The animals were trained only to respond when they detected an acoustic signal ("go/no-go" response). Detection thresholds were obtained for pure tone signals (frequencies: 0.2-40 kHz; durations: 0.5-5000 ms, depending on the frequency; 59 frequency-duration combinations). Detection thresholds were quantified by varying the signal amplitude by the 1-up, 1-down staircase method, and were defined as the stimulus levels, resulting in a 50% detection rate. The hearing thresholds of the two seals were similar for all frequencies except for 40 kHz, for which the thresholds differed by, on average, 3.7 dB. There was an inverse relationship between the time constant (tau), derived from an exponential model of temporal integration, and the frequency [log(tau)=2.86-0.94 log(f);tau in ms and f in kHz]. Similarly, the thresholds increased when the pulse was shorter than approximately 780 cycles (independent of the frequency). For pulses shorter than the integration time, the thresholds increased by 9-16 dB per decade reduction in the duration or number of cycles in the pulse. The results of this study suggest that most published hearing thresholds <or=1 kHz for harbor seals are probably not absolute, as they were derived from signals with durations shorter than the time constants for those frequencies.

Evolution of navy diver exposure standards for deterministic underwater sound in the 100–500 Hz band.

The US Navy developed low‐frequency active (LFA) sonar that had the potential for adverse exposure of divers to high levels of LFA sound. A number of studies into the effects on divers of deterministic waveforms in the frequency band 100–500 Hz were conducted. Animal, human diver, and modeling underwater sound exposure studies were completed across a broad array of organ systems. Human diver studies have investigated underwater hearing thresholds, aversion, wet suit attenuation, and psychophysical response. Tests have included both laboratory and field studies at sound pressure levels up to 160 dB re 1 μPa. Ultimately, over 500 exposures using over 100 different test subjects were conducted. These tests yielded a baseline set of guidelines for the exposure of Navy and recreational divers to deterministic sonar transmissions in the subject test band. A summary of the initial and subsequent testing and a tracing of the evolution of the current guidelines will be presented.

A comparison of underwater hearing sensitivity in bottlenose dolphins (Tursiops truncatus) determined by electrophysiological and behavioral methods

Variable stimulus presentation methods are used in auditory evoked potential (AEP) estimates of cetacean hearing sensitivity, each of which might affect stimulus reception and hearing threshold estimates. This study quantifies differences in underwater hearing thresholds obtained by AEP and behavioral means. For AEP estimates, a transducer embedded in a suction cup (jawphone) was coupled to the dolphin's lower jaw for stimulus presentation. Underwater AEP thresholds were obtained for three dolphins in San Diego Bay and for one dolphin in a quiet pool. Thresholds were estimated from the envelope following response at carrier frequencies ranging from 10 to 150 kHz. One animal, with an atypical audiogram, demonstrated significantly greater hearing loss in the right ear than in the left. Across test conditions, the range and average difference between AEP and behavioral threshold estimates were consistent with published comparisons between underwater behavioral and in-air AEP thresholds. AEP thresholds for one animal obtained in-air and in a quiet pool demonstrated a range of differences of -10 to 9 dB (mean = 3 dB). Results suggest that for the frequencies tested, the presentation of sound stimuli through a jawphone, underwater and in-air, results in acceptable differences to AEP threshold estimates.

Reliability of underwater hearing thresholds in pinnipeds

Repeated measures of low-frequency underwater hearing sensi- tivity in individuals of three pinniped species tested over 4-7 years are pre- sented. Despite changes in the experience of the subjects and certain testing parameters (e.g., equipment and research personnel), measured underwater hearing thresholds within subjects over relatively long periods of time were quite similar at the frequencies tested (0.2-6.4 kHz). These data address the reliability of acoustic signal detection measurements over time in pinnipeds using psychophysical techniques. They are also relevant in considering the cumulative effects of aging, experience, and noise exposure on pinniped hear- ing in certain frequency bands.

Underwater hearing thresholds in pinnipeds measured over a 6-year period

While absolute hearing thresholds have been obtained for some marine mammals, few published data are available on how measurements of individual auditory sensitivity may change over relatively long periods of time. Studies that have investigated temporal changes in sensitivity have typically focused on animals in which differences in hearing are anticipated (age-related hearing loss). This study investigated the replicability of underwater hearing thresholds in prime-aged individuals of three pinniped species over a 6-year period. Aside from their age and experience with behavioral signal detection tasks, test subjects were of similar physical condition throughout this experiment. They were tested in the same enclosure at similar test frequencies (0.1–6.4 kHz) using identical methodology and criteria. Underwater hearing thresholds obtained throughout this testing period were not significantly different. These data indicate that underwater hearing sensitivity may remain relatively stable over long periods in nonsenescent marine mammals, including those regularly exposed to noise. Further, our results suggest that variability in testing equipment and experimental personnel may have little impact on behavioral hearing data, as long as similar testing methodologies and subject response bias are carefully maintained.

Auditory and behavioral responses of California sea lions (Zalophus californianus) to single underwater impulses from an arc-gap transducer.

A behavioral response paradigm was used to measure underwater hearing thresholds in two California sea lions (Zalophus californianus) before and after exposure to underwater impulses from an arc-gap transducer. Preexposure and postexposure hearing thresholds were compared to determine if the subjects experienced temporary shifts in their masked hearing thresholds (MTTS). Hearing thresholds were measured at 1 and 10 kHz. Exposures consisted of single underwater impulses produced by an arc-gap transducer referred to as a "pulsed power device" (PPD). The electrical charge of the PPD was varied from 1.32 to 2.77 kJ; the distance between the subject and the PPD was varied over the range 3.4 to 25 m. No MTTS was observed in either subject at the highest received levels: peak pressures of approximately 6.8 and 14 kPa, rms pressures of approximately 178 and 183 dB re: 1 microPa, and total energy fluxes of 161 and 163 dB re: 1 microPa2s for the two subjects. Behavioral reactions to the tests were observed in both subjects. These reactions primarily consisted of temporary avoidance of the site where exposure to the PPD impulse had previously occurred.

Temporary shift in masked hearing thresholds in odontocetes after exposure to single underwater impulses from a seismic watergun.

A behavioral response paradigm was used to measure masked underwater hearing thresholds in a bottlenose dolphin (Tursiops truncatus) and a white whale (Delphinapterus leucas) before and after exposure to single underwater impulsive sounds produced from a seismic watergun. Pre- and postexposure thresholds were compared to determine if a temporary shift in masked hearing thresholds (MTTS), defined as a 6-dB or larger increase in postexposure thresholds, occurred. Hearing thresholds were measured at 0.4, 4, and 30 kHz. MTTSs of 7 and 6 dB were observed in the white whale at 0.4 and 30 kHz, respectively, approximately 2 min following exposure to single impulses with peak pressures of 160 kPa, peak-to-peak pressures of 226 dB re 1 microPa, and total energy fluxes of 186 dB re 1 microPa2 x s. Thresholds returned to within 2 dB of the preexposure value approximately 4 min after exposure. No MTTS was observed in the dolphin at the highest exposure conditions: 207 kPa peak pressure, 228 dB re 1 microPa peak-to-peak pressure, and 188 dB re 1 microPa2 x s total energy flux.

Temporary threshold shift (TTS) in bottlenose dolphins (Tursiops truncatus) exposed to tonal signals

A behavioral response paradigm was used to measure underwater hearing thresholds in two bottlenose dolphins (Tursiops truncatus) before and after exposure to intense tones. The fatiguing sounds were 3 kHz, 1 s tones. Hearing thresholds were measured at 3 and 4.5 kHz using a vocal response technique and a modified version of the Method of Free Response. Tests were conducted in a 6 m diam, 1.5 m deep vinyl-walled swimming pool. Ambient noise spectral density levels in the pool were approximately 44 dB re: 1 Pa2/Hz. Postexposure threshold measurements normally began within two minutes of exposure and continued for 1015 min following exposure. A temporary threshold shift (TTS) was defined as a 6 dB or larger increase in threshold compared to the corresponding pre-exposure level. Preliminary results indicate no TTS at 4.5 kHz for either subject at received SPLs of 200 dB re: 1 Pa. These data, as well as the test paradigm, absolute hearing thresholds, and observed behavioral reactions, will be presented and compared to existing TTS data for odontocetes.

Masked temporary threshold shift (MTTS) in odontocetes after exposure to single underwater impulses from a seismic watergun

A behavioral response paradigm was used to measure masked underwater hearing thresholds in a bottlenose dolphin (Tursiops truncatus) and white whale (Delphinapterus leucas) before and after exposure to single underwater impulses produced by a seismic watergun. Hearing thresholds were measured at 0.4, 4, and 30 kHz using a vocal response technique and a modified version of the Method of Free Response. A pre-exposure threshold was generally measured 34 min before presentation of the impulse. Post-exposure threshold measurements began within 2 min of exposure to the impulse and continued for approximately 20 min following exposure, in order to track recovery. A masked temporary threshold shift (MTTS) was defined as a 6-dB or larger increase in threshold compared to the corresponding pre-exposure measurement. The MTTS test paradigm will be discussed and preliminary MTTS and behavioral response data presented and compared to existing TTS data for odontocetes. [Work supported by ONR.]

Auditory and behavioral responses of bottlenose dolphins (Tursiops truncatus) and a beluga whale (Delphinapterus leucas) to impulsive sounds resembling distant signatures of underwater explosions.

A behavioral response paradigm was used to measure masked underwater hearing thresholds in two bottlenose dolphins and one beluga whale before and after exposure to impulsive underwater sounds with waveforms resembling distant signatures of underwater explosions. An array of piezoelectric transducers was used to generate impulsive sounds with waveforms approximating those predicted from 5 or 500 kg HBX-1 charges at ranges from 1.5 to 55.6 km. At the conclusion of the study, no temporary shifts in masked-hearing thresholds (MTTSs), defined as a 6-dB or larger increase in threshold over pre-exposure levels, had been observed at the highest impulse level generated (500 kg at 1.7 km, peak pressure 70 kPa); however, disruptions of the animals' trained behaviors began to occur at exposures corresponding to 5 kg at 9.3 km and 5 kg at 1.5 km for the dolphins and 500 kg at 1.9 km for the beluga whale. These data are the first direct information regarding the effects of distant underwater explosion signatures on the hearing abilities of odontocetes.

Temporary shift in masked hearing thresholds of bottlenose dolphins, Tursiops truncatus, and white whales, Delphinapterus leucas, after exposure to intense tones.

A behavioral response paradigm was used to measure masked underwater hearing thresholds in five bottlenose dolphins and two white whales before and immediately after exposure to intense 1-s tones at 0.4, 3, 10, 20, and 75 kHz. The resulting levels of fatiguing stimuli necessary to induce 6 dB or larger masked temporary threshold shifts (MTTSs) were generally between 192 and 201 dB re: 1 microPa. The exceptions occurred at 75 kHz, where one dolphin exhibited an MTTS after exposure at 182 dB re: 1 microPa and the other dolphin did not show any shift after exposure to maximum levels of 193 dB re: 1 microPa, and at 0.4 kHz, where no subjects exhibited shifts at levels up to 193 dB re: 1 microPa. The shifts occurred most often at frequencies above the fatiguing stimulus. Dolphins began to exhibit altered behavior at levels of 178-193 dB re: 1 microPa and above; white whales displayed altered behavior at 180-196 dB re: 1 microPa and above. At the conclusion of the study all thresholds were at baseline values. These data confirm that cetaceans are susceptible to temporary threshold shifts (TTS) and that small levels of TTS may be fully recovered.

Masked hearing thresholds for a bottlenose dolphin (Tursiops truncatus) and white whale (Delphinapterus leucas) in the far field and hydrodynamic near field

A behavioral response paradigm was used to measure masked underwater hearing thresholds in a bottlenose dolphin (Tursiops truncatus) and white whale (Delphinapterus leucas) within the far field and hydrodynamic near field of an underwater sound projector. Masked hearing thresholds at 100 and 300 Hz were measured at source distances of 1, 2, and 4 m; over these distances the specific acoustic impedance ratio varied from approximately −10 to 0 dB at 100 Hz and −3 to 0 dB at 300 Hz. Individual hearing test trials consisted of a 3.5-s noise burst alone (N) or a noise burst along with a 1-s tone (S+N). Subjects were trained to produce an audible whistle in response to S+N trials and to remain silent for N trials. Thresholds were estimated using an up–down staircase procedure. Preliminary results indicate no significant differences between thresholds measured at the three different source distances for either test subject. [Work supported by ONR.]