Auditory masking of tonal and conspecific signals by continuous active sonar, amplitude modulated noise, and Gaussian noise in killer whales (Orcinus orca).

Continuous active sonar is thought to mitigate severe acoustic impacts due to its lower sound pressure level compared to pulsed active sonar typically used by world navies. However, due to its almost continuous duty cycle, continuous active sonar could have a higher potential for auditory masking. Here, we evaluate the auditory masking potential of several noise types including a recording of continuous active sonar, amplitude modulated noise, and Gaussian noise, on signal detection in two killer whales. Signals were either a 1.5 kHz pure tone or a recording of a broadband burst-pulse killer whale call. For the 1.5 kHz tone, all noise types resulted in statistically significant masking, however, there was a release from masking of approximately 13 dB for the amplitude-modulated noise. When the killer whale call was the signal, the whales employed an off-frequency listening strategy where the whales were able to detect frequency components of the signal that did not directly overlap with the noise. However, this strategy was less useful for the continuous active sonar noise due to its broadband harmonic structure. Continuous active sonar has spectral features that considerably overlap with those of killer whale calls, making this type of noise an effective auditory masker.

Temporal integration of tone signals by a killer whale (Orcinus orca).

A psychophysical procedure was used to measure pure-tone detection thresholds for a killer whale (Orcinus orca) as a function of both signal frequency and signal duration. Frequencies ranged between 1 and 100 kHz and signal durations ranged from 50 µs to 2 s, depending on the frequency. Detection thresholds decreased with an increase in signal duration up to a critical duration, which represents the auditory integration time. Integration times ranged from 4 ms at 100 kHz and increased up to 241 ms at 1 kHz. The killer whale data are similar to other odontocete species that have participated in similar experiments. The results have implications for noise impact predictions for signals with durations less than the auditory integration time.

Mechanisms of auditory masking in marine mammals.

Anthropogenic noise is an increasing threat to marine mammals that rely on sound for communication, navigation, detecting prey and predators, and finding mates. Auditory masking is one consequence of anthropogenic noise, the study of which is approached from multiple disciplines including field investigations of animal behavior, noise characterization from in-situ recordings, computational modeling of communication space, and hearing experiments conducted in the laboratory. This paper focuses on laboratory hearing experiments applying psychophysical methods, with an emphasis on the mechanisms that govern auditory masking. Topics include tone detection in simple, complex, and natural noise; mechanisms for comodulation masking release and other forms of release from masking; the role of temporal resolution in auditory masking; and energetic vs informational masking.

Spatial acuity of the bottlenose dolphin (Tursiops truncatus) biosonar system with a bat and human comparison.

Horizontal angular resolution was measured in two bottlenose dolphins using a two-alternative forced-choice, biosonar target discrimination paradigm. The task required a stationary dolphin positioned in a hoop to discriminate two physical targets at a range of 4 m. The angle separating the targets was manipulated to estimate an angular discrimination threshold of 1.5°. In a second experiment, a similar two-target biosonar discrimination task was conducted with one free-swimming dolphin, to test whether its emission beam was a critical factor in discriminating the targets. The spatial separation between two targets was manipulated to measure a discrimination threshold of 6.7 cm. There was a relationship between differences in acoustic signals received at each target and the dolphin's performance. The results of the angular resolution experiment were in good agreement with measures of the minimum audible angle of both dolphins and humans and remarkably similar to measures of angular difference discrimination in echolocating dolphins, bats, and humans. The results suggest that horizontal auditory spatial acuity may be a common feature of the mammalian auditory system rather than a specialized feature exclusive to echolocating auditory predators.

Auditory masking in killer whales (Orcinus orca): Critical ratios for tonal signals in Gaussian noise.

Masked detection thresholds were measured for two killer whales (Orcinus orca) using a psychoacoustic, adaptive-staircase procedure. Noise bands were 1-octave wide continuous Gaussian noise. Tonal signals extended between 500 Hz and 80 kHz. Resulting critical ratios increased with the signal frequency from 15 dB at 500 Hz up to 32 dB at 80 kHz. Critical ratios for killer whales were similar to those of other odontocetes despite considerable differences in size, hearing morphology, and hearing sensitivity between species.

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.

Dolphin echo-delay resolution measured with a jittered-echo paradigm.

Biosonar echo delay resolution was investigated in four bottlenose dolphins (Tursiops truncatus) using a "jittered" echo paradigm, where dolphins discriminated between electronic echoes with fixed delay and those whose delay alternated (jittered) on successive presentations. The dolphins performed an echo-change detection task and produced a conditioned acoustic response when detecting a change from non-jittering echoes to jittering echoes. Jitter delay values ranged from 0 to 20 µs. A passive listening task was also conducted, where dolphins listened to simulated echoes and produced a conditioned acoustic response when signals changed from non-jittering to jittering. Results of the biosonar task showed a mean jitter delay threshold of 1.3 µs and secondary peaks in error functions suggestive of the click autocorrelation function. When echoes were jittered in polarity and delay, error functions shifted by approximately 5 µs and all dolphins discriminated echoes that jittered only in polarity. Results were qualitatively similar to those from big brown bats (Eptesicus fuscus) and indicate that the dolphin biosonar range estimator is sensitive to echo phase information. Results of the passive listening task suggested that the dolphins could not passively detect changes in timing and polarity of simulated echoes.

Spectral cues and temporal integration during cylinder echo discrimination by bottlenose dolphins (Tursiops truncatus).

Three bottlenose dolphins (Tursiops truncatus) participated in simulated cylinder wall thickness discrimination tasks utilizing electronic "phantom" echoes. The first experiment resulted in psychometric functions (percent correct vs wall thickness difference) similar to those produced by a dolphin performing the task with physical cylinders. In the second experiment, a wide range of cylinder echoes was simulated, with the time separation between echo highlights covering a range from <30 to >300 µs. Dolphin performance and a model of the dolphin auditory periphery suggest that the dolphins used high-frequency, spectral-profiles of the echoes for discrimination and that the utility of spectral cues degraded when the time separation between echo highlights approached and exceeded the dolphin's temporal integration time of ∼264 µs.

The effect of jamming stimuli on the echolocation behavior of the bottlenose dolphin, Tursiops truncatus.

Echolocating bats and odontocetes face the potential challenge of acoustic interference from neighbors, or sonar jamming. To counter this, many bat species have adapted jamming avoidance strategies to improve signal detection, but any such avoidance strategies in dolphins is unknown. This study provides an investigation into whether dolphins modify echolocation behavior during jamming scenarios. Recorded echolocation clicks were projected at different click repetition rates and at different aspect angles relative to two dolphins' heads while each dolphin was performing a target detection task. Changes in the timing, amplitude, and frequency of structure of the dolphin's emitted signals were compared to determine if and how dolphins modify echolocation when faced with potentially interfering conspecific echolocation signals. The results indicate that both dolphins demonstrated different responses when faced with jamming scenarios, which may reflect optimal strategies according to individual auditory perception abilities.

Effects of vibratory pile driver noise on echolocation and vigilance in bottlenose dolphins (Tursiops truncatus).

Vibratory pile drivers, used for marine construction, can produce sustained, high sound pressure levels (SPLs) in areas that overlap with dolphin habitats. Dolphins rely on echolocation for navigation, detecting predators and prey, and to coordinate group behavior. This study examined the effects of vibratory pile driver noise on dolphin sustained target detection capabilities through echolocation. Five dolphins were required to scan their enclosure and indicate the occurrences of phantom echoes during five different source levels of vibratory pile driver playback sound (no-playback control, 110, 120, 130, and 140 dB re 1 µPa). Three of the dolphins demonstrated a significant decrease in target detection performance at 140 dB playback level that was associated with an almost complete secession of echolocation activity. The performance of two dolphins was not affected. All dolphins rapidly returned to baseline levels of target detection performance by their second replication. However, an increased number of clicks was produced at the highest playback SPL. The data suggest that the decrease in vigilant behavior was due to the vibratory pile driver noise distracting the dolphins and decreasing their motivation to perform the task.

Killer whale (Orcinus orca) behavioral audiograms.

Killer whales (Orcinus orca) are one of the most cosmopolitan marine mammal species with potential widespread exposure to anthropogenic noise impacts. Previous audiometric data on this species were from two adult females [Szymanski, Bain, Kiehl, Pennington, Wong, and Henry (1999). J. Acoust. Soc. Am. 108, 1322-1326] and one sub-adult male [Hall and Johnson (1972). J. Acoust. Soc. Am. 51, 515-517] with apparent high-frequency hearing loss. All three killer whales had best sensitivity between 15 and 20 kHz, with thresholds lower than any odontocete tested to date, suggesting this species might be particularly sensitive to acoustic disturbance. The current study reports the behavioral audiograms of eight killer whales at two different facilities. Hearing sensitivity was measured from 100 Hz to 160 kHz in killer whales ranging in age from 12 to 52 year. Previously measured low thresholds at 20 kHz were not replicated in any individual. Hearing in the killer whales was generally similar to other delphinids, with lowest threshold (49 dB re 1 µPa) at approximately 34 kHz, good hearing (i.e., within 20 dB of best sensitivity) from 5 to 81 kHz, and low- and high-frequency hearing cutoffs (>100 dB re µPa) of 600 Hz and 114 kHz, respectively.

Composite critical ratio functions for odontocete cetaceans.

Critical ratios (CRs) are useful for estimating detection thresholds of tonal signals when the spectral density of noise is known. In cetaceans, CRs have only been measured for a few animals representing four odontocete species. These data are sparse, particularly for lower frequencies where anthropogenic noise is concentrated. There is currently no systematic method for implementing CR predictions (e.g., a composite frequency-dependent CR function). The current study measures CRs for two bottlenose dolphins (Tursiops truncatus) and estimates composite CR functions. The composite models can aid in predicting and extrapolating auditory masking for a broad range of frequencies.

Hearing Mechanisms and Noise Metrics Related to Auditory Masking in Bottlenose Dolphins (Tursiops truncatus).

Odontocete cetaceans are acoustic specialists that depend on sound to hunt, forage, navigate, detect predators, and communicate. Auditory masking from natural and anthropogenic sound sources may adversely affect these fitness-related capabilities. The ability to detect a tone in a broad range of natural, anthropogenic, and synthesized noise was tested with bottlenose dolphins using a psychophysical, band-widening procedure. Diverging masking patterns were found for noise bandwidths greater than the width of an auditory filter. Despite different noise types having equal-pressure spectral-density levels (95 dB re 1 µPa(2)/Hz), masked detection threshold differences were as large as 22 dB. Consecutive experiments indicated that noise types with increased levels of amplitude modulation resulted in comodulation masking release due to within-channel and across-channel auditory mechanisms. The degree to which noise types were comodulated (comodulation index) was assessed by calculating the magnitude-squared coherence between the temporal envelope from an auditory filter centered on the signal and temporal envelopes from flanking filters. Statistical models indicate that masked thresholds in a variety of noise types, at a variety of levels, can be explained with metrics related to the comodulation index in addition to the pressure spectral-density level of noise. This study suggests that predicting auditory masking from ocean noise sources depends on both spectral and temporal properties of the noise.

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.

Energetic and informational masking of complex sounds by a bottlenose dolphin (Tursiops truncatus).

With few exceptions, laboratory studies of auditory masking in marine mammals have been limited to examining detection thresholds for simple tonal signals embedded in broadband noise. However, detection of a sound has little adaptive advantage without the knowledge of what produced the sound (recognition) and where the sound originated (localization). In the current study, a bottlenose dolphin's masked detection thresholds (energetic masking) and masked recognition thresholds (informational masking) were estimated for a variety of complex signals including dolphin vocalizations, frequency modulated signals, and a 10 kHz pure tone. Broadband noise types included recordings of natural sounds and computer generated sounds. Detection thresholds were estimated using a standard go, no-go adaptive staircase procedure. The same dolphin learned to associate whistle-like FM sounds with specific arbitrary objects using a three alternative, matching-to-sample (MTS) procedure. The dolphin's performance in the MTS task was then tested in the presence of the same masking noise types used in the detection task. Recognition thresholds were, on average, about 4 dB higher than detection thresholds for similar signal-noise conditions. The 4 dB difference is likely due to additional cognitive demands of recognition, including attention and pattern recognition.

Auditory sensitivity in aquatic animals.

A critical concern with respect to marine animal acoustics is the issue of hearing "sensitivity," as it is widely used as a criterion for the onset of noise-induced effects. Important aspects of research on sensitivity to sound by marine animals include: uncertainties regarding how well these species detect and respond to different sounds; the masking effects of man-made sounds on the detection of biologically important sounds; the question how internal state, motivation, context, and previous experience affect their behavioral responses; and the long-term and cumulative effects of sound exposure. If we are to better understand the sensitivity of marine animals to sound we must concentrate research on these questions. In order to assess population level and ecological community impacts new approaches can possibly be adopted from other disciplines and applied to marine fauna.

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.

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 dolphin's 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 dolphin's 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.

Discrimination of mixed-directional whistles by a bottlenose dolphin (Tursiops truncatus).

Dolphins are hypothesized to deduce the swimming direction of group members by attending to the spectral pattern of whistle harmonics. This is known as the direction of movement cue hypothesis and may facilitate coordination of complex group behavior when visibility is poor. The direction of movement cue hypothesis hinges on the assumption that dolphins can discriminate between whistles with different harmonic patterns that are associated with signaler orientation. This assumption was tested with a bottlenose dolphin. Whistles were recorded from a dolphin at different azimuth positions (0° to 180° in 45° increments). Noise-free, synthetic whistles were created to mimic the direction-dependant spectral profiles of the recorded whistles. A dolphin was then tested in its ability to discriminate between the synthetic whistles using fixed level and roving level conditions. The dolphin's discrimination performance in both the fixed and roving level conditions was near 100% for whistles separated by angles greater than 45°, and near chance for 45° separations. Computer simulations of the task, along with the dolphin's performance, suggest that the dolphin's discrimination was level invariant and based on the spectral pattern of the whistles.

Time and frequency metrics related to auditory masking of a 10 kHz tone in bottlenose dolphins (Tursiops truncatus).

Metrics related to the frequency spectrum of noise (e.g., critical ratios) are often used to describe and predict auditory masking. In this study, detection thresholds for a 10 kHz tone were measured in the presence of anthropogenic, natural, and synthesized noise. Time-domain and frequency-domain metrics were calculated for the different noise types, and regression models were used to determine the relationship between noise metrics and masked tonal thresholds. Statistical models suggested that detection thresholds, masked by a variety of noise types at a variety of noise levels, can be explained with metrics related to the spectral density of noise and the degree to which amplitude modulation is correlated across frequency regions of the noise. The results demonstrate the need to include time-domain metrics when describing and predicting auditory masking.