Jason Mulsow

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.

Psychophysical and electrophysiological aerial audiograms of a Steller sea lion (Eumetopias jubatus) a)

A within-subject comparison of auditory steady-state response (ASSR) and psychophysical measurements of aerial hearing sensitivity was conducted with an individual of the largest otariid species, the Steller sea lion. Psychophysical methods were used to obtain an unmasked aerial audiogram at 13 frequencies, spanning a range of 0.125-34 kHz. The subject had a hearing range (frequencies audible at 60 dB(rms) re 20 microPa) of about 0.250-30 kHz, and a region of best hearing sensitivity from 5-14.1 kHz. The psychophysical aerial audiogram of this Steller sea lion was remarkably similar to aerial audiograms previously obtained for California sea lions and northern fur seals, suggesting that the otariid pinnipeds form a functional hearing group. ASSR thresholds, measured at frequencies of 1, 2, 5, 10, 20, and 32 kHz, were elevated relative to corresponding psychophysical thresholds, ranging from +1 dB at 20 kHz, to +31 dB at 1 kHz. The ASSR audiogram accurately predicted the subjects high-frequency cutoff, and provided a reasonable estimate of hearing sensitivity at frequencies above 2 kHz. In testing situations where psychophysical methods are not possible, ASSR methods may provide an objective and efficient estimate of behavioral hearing sensitivity in otariid pinnipeds.

Onset, growth, and recovery of in-air temporary threshold shift in a California sea lion (Zalophus californianus)

A California sea lion (Zalophus californianus) was tested in a behavioral procedure to assess noise-induced temporary threshold shift (TTS) in air. Octave band fatiguing noise was varied in both duration (1.5-50 min) and level (94-133 dB re 20 muPa) to generate a variety of equal sound exposure level conditions. Hearing thresholds were measured at the center frequency of the noise (2500 Hz) before, immediately after, and 24 h following exposure. Threshold shifts generated from 192 exposures ranged up to 30 dB. Estimates of TTS onset [159 dB re (20 muPa)(2) s] and growth (2.5 dB of TTS per dB of noise increase) were determined using an exponential function. Recovery for threshold shifts greater than 20 dB followed an 8.8 dB per log(min) linear function. Repeated testing indicated possible permanent threshold shift at the test frequency, but a later audiogram revealed no shift at this frequency or higher. Sea lions appear to be equally susceptible to noise in air and in water, provided that the noise exposure levels are referenced to absolute sound detection thresholds in both media. These data provide a framework within which to consider effects arising from more intense and/or sustained exposures.

High-resolution measurement of a bottlenose dolphin's (Tursiops truncatus) biosonar transmission beam pattern in the horizontal plane

Previous measurements of toothed whale echolocation transmission beam patterns have utilized few hydrophones and have therefore been limited to fine angular resolution only near the principal axis or poor resolution over larger azimuthal ranges. In this study, a circular, horizontal planar array of 35 hydrophones was used to measure a dolphins transmission beam pattern with 5° to 10° resolution at azimuths from -150° to +150°. Beam patterns and directivity indices were calculated from both the peak-peak sound pressure and the energy flux density. The emitted pulse became smaller in amplitude and progressively distorted as it was recorded farther off the principal axis. Beyond ±30° to 40°, the off-axis signal consisted of two distinct pulses whose difference in time of arrival increased with the absolute value of the azimuthal angle. A simple model suggests that the second pulse is best explained as a reflection from internal structures in the dolphins head, and does not implicate the use of a second sound source. Click energy was also more directional at the higher source levels utilized at longer ranges, where the center frequency was elevated compared to that of the lower amplitude clicks used at shorter range.

California sea lion (Zalophus californianus) aerial hearing sensitivity measured using auditory steady-state response and psychophysical methods.

Although electrophysiological methods of measuring the hearing sensitivity of pinnipeds are not yet as refined as those for dolphins and porpoises, they appear to be a promising supplement to traditional psychophysical procedures. In order to further standardize electrophysiological methods with pinnipeds, a within-subject comparison of psychophysical and auditory steady-state response (ASSR) measures of aerial hearing sensitivity was conducted with a 1.5-yr-old California sea lion. The psychophysical audiogram was similar to those previously reported for otariids, with a U-shape, and thresholds near 10 dB re 20 μPa at 8 and 16 kHz. ASSR thresholds measured using both single and multiple simultaneous amplitude-modulated tones closely reproduced the psychophysical audiogram, although the mean ASSR thresholds were elevated relative to psychophysical thresholds. Differences between psychophysical and ASSR thresholds were greatest at the low- and high-frequency ends of the audiogram. Thresholds measured using the multiple ASSR method were not different from those measured using the single ASSR method. The multiple ASSR method was more rapid than the single ASSR method, and allowed for threshold measurements at seven frequencies in less than 20 min. The multiple ASSR method may be especially advantageous for hearing sensitivity measurements with otariid subjects that are untrained for psychophysical procedures.

Auditory Evoked Potentials in Northern Elephant Seals ( Mirounga angustirostris )

Auditory evoked potentials (AEPs) were investigated in northern elephant seals (Mirounga angustirostris) to characterize the responses elicited by different acoustic stimulus types, examine temporal resolving capabilities, and evaluate the potential for using evoked responses to estimate hearing sensitivity. Clicks and tone pips were presented to individual seals to characterize evoked responses to broadand narrowband stimuli. Tone pip trains and sinusoidally amplitude-modulated (SAM) tones were used to determine modulation rate transfer functions (MRTF) of the auditory system and to determine if the magnitude of the envelope-following response (EFR) relative to the stimulus level can be used to estimate hearing thresholds. Click evoked responses were characterized by three early positive peaks (~2.6, 4.4, and 6.1 ms) and a dominant negative peak at 7.2 ms and had average amplitudes of 264 nV (peak-to-peak [pk-pk]) for a corresponding stimulus level of 126 dB re 20 μPa (pk-pk). The use of dissociative drugs for the immobilization of the seals showed no demonstrable effect on the latencies or amplitudes of the click evoked response. Both the rate following response (RFR) and EFR amplitudes were maximal when the stimulus repetition rate or the amplitude modulation rate, respectively, were < 100 Hz. EFR amplitudes at the rate of amplitude modulation tracked near linearly with stimulus level. Thresholds for a 4-kHz SAM tone were estimated to be 45 dB re 20 μPa. Thus, the recording of AEPs is a viable means of studying auditory processes in the northern elephant seal.

Measurement and Response Characteristics of Auditory Brainstem Responses in Pinnipeds

The measurement of auditory evoked potentials (AEPs) has proven to be a useful tool for examining the auditory physiology of odontocete cetaceans and there is growing interest in applying this electrophysiological approach to study the hearing of other marine mammals. The aim of the current investigation was to examine some of the basic measurement and response characteristics of the auditory brainstem response (ABR) in pinnipeds. The subjects were California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and northern elephant seals (Mirounga angustirostris) that were awake, sedated, or anesthetized during in-air testing. Auditory stimuli were broadband clicks and Hanning-gated tone bursts that were presented binaurally in a direct field. The amplitude and waveform of the ABRs were evaluated as a function of subject state, electrode type and position, analog bandpass filtering, stimulus presentation rate, and stimulus bandwidth. Results indicate that the ABRs were of highest amplitude when measured from subdermal electrodes arranged in a common reference configuration, with the cephalic electrode placed 2 to 4 cm forward of the ears on the dorsal midline of the head. The ABR waveforms were generally similar among the species tested, although the amplitude of the elephant seal ABR was much smaller than that of the other two species at similar stimulus levels. Bandpass filtering of the ABR resulted in improved signal-tonoise ratios but also caused reduction in response amplitude and distortion of the ABR waveform at high-pass settings above 65 Hz. Five-cycle tone bursts provided the best tradeoff between response amplitude and frequency specificity. The amplitude of ABRs evoked by clicks and tone bursts as a function of stimulus level was approximately linear for California sea lions and harbor seals over a range of ~25 dB. Visually estimated thresholds for California sea lions were noise limited but were sensitive enough to show hearing loss in one older subject. These findings should inform future research efforts involving electrophysiological assessment of auditory function, hearing sensitivity, and noise impacts in pinnipeds.

Underwater psychophysical audiogram of a young male California sea lion (Zalophus californianus)a)

Auditory evoked potential (AEP) data are commonly obtained in air while sea lions are under gas anesthesia; a procedure that precludes the measurement of underwater hearing sensitivity. This is a substantial limitation considering the importance of underwater hearing data in designing criteria aimed at mitigating the effects of anthropogenic noise exposure. To determine if some aspects of underwater hearing sensitivity can be predicted using rapid aerial AEP methods, this study measured underwater psychophysical thresholds for a young male California sea lion (Zalophus californianus) for which previously published aerial AEP thresholds exist. Underwater thresholds were measured in an aboveground pool at frequencies between 1 and 38 kHz. The underwater audiogram was very similar to those previously published for California sea lions, suggesting that the current and previously obtained psychophysical data are representative for this species. The psychophysical and previously measured AEP audiograms were most similar in terms of high-frequency hearing limit (HFHL), although the underwater HFHL was sharper and occurred at a higher frequency. Aerial AEP methods are useful for predicting reductions in the HFHL that are potentially independent of the testing medium, such as those due to age-related sensorineural hearing loss.

Noise‐induced permanent threshold shift in a harbor seal

Investigation of auditory temporary threshold shift (TTS) in marine mammals has provided a means of predicting the harmful effects of underwater anthropogenic noise. As complete recovery of hearing is requisite in these studies, they have been considered appropriate in light of subject availability and ethical considerations. In our psychophysical studies of TTS in pinnipeds, we have employed methods designed to safely titrate from sound levels of noise inducing no TTS to levels of significant but completely recoverable hearing loss. In the present study, these methods were used with a harbor seal (Phoca vitulina) exposed to an underwater 4.1 kHz pure tone fatiguing stimulus. Sound levels and durations were gradually increased to a maximum received sound pressure of 184 dB re 1 μPa with a duration of 60 s (SEL=202 dB re 1 μPa2s). Upon the second exposure to this fatiguing stimulus, an initial threshold shift in excess of 50 dB was estimated at a test frequency of 5.8 kHz, a half‐octave above the fatiguing...

Auditory evoked potentials in a bottlenose dolphin during moderate-range echolocation tasks

Studies with echolocating odontocetes have suggested that forms of automatic gain control mediate auditory electrophysiological responses to target-related echoes. This study used a phantom echo generator and auditory evoked potential measurements to examine automatic gain control in a bottlenose dolphin. Auditory evoked potentials to outgoing clicks and incoming echoes were recorded for simulated ranges from 2.5 to 80 m. When geometric spreading loss was simulated, echo-evoked potential amplitudes were essentially constant up to 14 m and progressively decreased with increasing range. When the echo levels were held constant relative to clicks, echo-evoked potential amplitudes increased with increasing range up to 80 m. These results suggest that automatic gain control maintains distance-independent echo-evoked potential amplitudes at close range, but does not fully compensate for attenuation due to spreading loss at longer ranges. The automatic gain control process appears to arise from an interaction of transmitter and receiver based processes, resulting in a short-range region of distance-independent echo-evoked potential amplitudes for relevant targets, and a longer-range region in which echo-evoked potential amplitudes are reduced.