James J. Finneran

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 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.

Temporary threshold shift in bottlenose dolphins (Tursiops truncatus) exposed to mid-frequency tones.

A behavioral response paradigm was used to measure hearing thresholds in bottlenose dolphins before and after exposure to 3 kHz tones with sound exposure levels (SELs) from 100 to 203 dB re 1 microPa2 s. Experiments were conducted in a relatively quiet pool with ambient noise levels below 55 dB re 1 microPa2/Hz at frequencies above 1 kHz. Experiments 1 and 2 featured 1-s exposures with hearing tested at 4.5 and 3 kHz, respectively. Experiment 3 featured 2-, 4-, and 8-s exposures with hearing tested at 4.5 kHz. For experiment 2, there were no significant differences between control and exposure sessions. For experiments 1 and 3, exposures with SEL=197 dB re 1 microPa2 s and SEL > or = 195 dB re 1 microPa2 s, respectively, resulted in significantly higher TTS4 than control sessions. For experiment 3 at SEL= 195 dB re 1 microPa2 s, the mean TTS4 was 2.8 dB. These data are consistent with prior studies of TTS in dolphins exposed to pure tones and octave band noise and suggest that a SEL of 195 dB re 1 microPa2 s is a reasonable threshold for the onset of TTS in dolphins and white whales exposed to midfrequency tones.

Effects of low-frequency underwater sound on hair cells of the inner ear and lateral line of the teleost fish Astronotus ocellatus.

Fish (Astronotus ocellatus, the oscar) were subject to pure tones in order to determine the effects of sound at levels typical of man-made sources on the sensory epithelia of the ear and the lateral line. Sounds varied in frequency (60 or 300 Hz), duty cycle (20% or continuous), and intensity (100, 140, or 180 dB re: 1 muPa). Fish were allowed to survive for 1 or 4 days posttreatment. Tissue was then evaluated using scanning electron microscopy to assess the presence or absence of ciliary bundles on the sensory hair cells on each of the otic endorgans and the lateral line. The only damage that was observed was in four of five fish stimulated with 300-Hz continuous tones at 180 dB re: 1 muPa and allowed to survive for 4 days. Damage was limited to small regions of the striola of the utricle and lagena. There was no damage in any other endorgan, and the size and location of the damage varied between specimens. No damage was observed in fish that had been allowed to survive for 1 day poststimulation, suggesting that damage may develop slowly after exposure.

Variation in the hearing sensitivity of a dolphin population determined through the use of evoked potential audiometry

A portable electrophysiological data collection system was used to assess hearing in a captive population of bottlenose dolphins by recording auditory evoked potentials (AEPs). The AEP system used a transducer embedded in a suction cup to deliver amplitude modulated tones to the dolphin through the lower jaw. Evoked potentials were recorded noninvasively using surface electrodes. Adaptive procedures allowed hearing thresholds to be estimated from 10 to 150 kHz in a single ear in about 45 min. Hearing thresholds were measured in 42 bottlenose dolphins (28 male, 14 female), ranging in age from 4 to 47 years. Variations in hearing sensitivity with age and sex followed patterns seen in humans and terrestrial mammals: generally, within the population there was a progressive loss of high frequency hearing with age and an earlier onset of hearing loss in males than in females. Hearing loss generally occurred between the ages of 20 and 30, and all animals over the age of 27 had some degree of hearing loss. Two dolphins with profound hearing loss were found within the population. Aberrant hearing patterns were observed in related dolphins suggesting genetic links to hearing ability may exist.

Structural and functional imaging of bottlenose dolphin (Tursiops truncatus) cranial anatomy

SUMMARY Bottlenose dolphins were submitted to structural (CT) and functional (SPECT/PET) scans to investigate their in vivo anatomy and physiology with respect to structures important to hearing and echolocation. The spatial arrangement of the nasal passage and sinus air spaces to the auditory bullae and phonic lips was studied in two dolphins via CT. Air volume of the sinuses and nasal passages ranged from 267.4 to 380.9 ml. Relationships of air spaces to the auditory bullae and phonic lips support previous hypotheses that air protects the ears from echolocation clicks generated by the dolphin and contributes to dolphin hearing capabilities (e.g. minimum angular resolution, inter-aural intensity differences). Lung air may replenish reductions in sinus and nasal passage air volume via the palatopharyngeal sphincter, thus permitting the echolocation mechanism to operate at depth. To determine the relative extent of regional blood flow within the head of the dolphin, two dolphins were scanned with SPECT after an intravenous dose of 1850 MBq 99mTc-bicisate. A single dolphin received 740 MBq of 18F-2-fluoro-2-deoxyglucose (FDG) to identify the relative metabolic activity of head tissues. Substantial blood flow was noted across the dorsoanterior curvature of the melon and within the posterior region of the lower jaw fats. Metabolism of these tissues relative to others within the head was nominal. It is suggested that blood flow in these fat bodies serves to thermoregulate lipid density of the melon and jaw canal. Sound velocity is inversely related to the temperature of acoustic lipids (decreasing lipid density), and changes in lipid temperature are likely to impact the wave guide properties of the sound projection and reception pathways. Thermoregulation of lipid density may maintain sound velocity gradients of the acoustic lipid complexes, particularly in the outer shell of the melon, which otherwise might vary in response to changing environmental temperatures.

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 dolphins 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.

Assessing temporary threshold shift in a bottlenose dolphin (Tursiops truncatus) using multiple simultaneous auditory evoked potentials

Hearing sensitivity was measured in a bottlenose dolphin before and after exposure to an intense 20-kHz fatiguing tone in three different experiments. In each experiment, hearing was characterized using both the auditory steady-state response (ASSR) and behavioral methods. In experiments 1 and 2, ASSR stimuli consisted of seven frequency-modulated tones, each with a unique carrier and modulation frequency. The tones were simultaneously presented to the subject and the ASSR at each modulation rate measured to determine the effects of the sound exposure at the corresponding carrier frequency. In experiment 3 behavioral thresholds and ASSR input-output functions were measured at a single frequency before and after three exposures. Hearing loss was frequency-dependent, with the largest temporary threshold shifts occurring (in order) at 30, 40, and 20 kHz. ASSR threshold shifts reached 40-45 dB and were always larger than behavioral shifts (19-33 dB). The ASSR input-output functions were represented as the sum of two processes: a low threshold, saturating process and a higher threshold, linear process, that react and recover to fatigue at different rates. The loss of the near-threshold saturating process after exposure may explain the discrepancies between the ASSR and behavioral threshold shifts.

Comparison of in-air evoked potential and underwater behavioral hearing thresholds in four bottlenose dolphins (Tursiops truncatus)

Traditional behavioral techniques for hearing assessment in marine mammals are limited by the time and access required to train subjects. Electrophysiological methods, where passive electrodes are used to measure auditory evoked potentials (AEPs), are attractive alternatives to behavioral techniques; however, there have been few attempts to compare AEP and behavioral results for the same subject. In this study, behavioral and AEP hearing thresholds were compared in four bottlenose dolphins. AEP thresholds were measured in-air using a piezoelectric sound projector embedded in a suction cup to deliver amplitude modulated tones to the dolphin through the lower jaw. Evoked potentials were recorded noninvasively using surface electrodes. Adaptive procedures allowed AEP hearing thresholds to be estimated from 10 to 150 kHz in a single ear in about 45 min. Behavioral thresholds were measured in a quiet pool and in San Diego Bay. AEP and behavioral threshold estimates agreed closely as to the upper cutoff frequency beyond which thresholds increased sharply. AEP thresholds were strongly correlated with pool behavioral thresholds across the range of hearing; differences between AEP and pool behavioral thresholds increased with threshold magnitude and ranged from 0 to + 18 dB.

Comodulation masking release in bottlenose dolphins (Tursiops truncatus)

The acoustic environment of the bottlenose dolphin often consists of noise where energy across frequency regions is coherently modulated in time (e.g., ambient noise from snapping shrimp). However, most masking studies with dolphins have employed random Gaussian noise for estimating patterns of masked thresholds. The current study demonstrates a pattern of masking where temporally fluctuating comodulated noise produces lower masked thresholds (up to a 17 dB difference) compared to Gaussian noise of the same spectral density level. Noise possessing wide bandwidths, low temporal modulation rates, and across-frequency temporal envelope coherency resulted in lower masked thresholds, a phenomenon known as comodulation masking release. The results are consistent with a model where dolphins compare temporal envelope information across auditory filters to aid in signal detection. Furthermore, results suggest conventional models of masking derived from experiments using random Gaussian noise may not generalize well to environmental noise that dolphins actually encounter.