High Frequency hearing in echolocating dolphins.

The Reflections series takes a look back on historical articles from The Journal of the Acoustical Society of America that have had a significant impact on the science and practice of acoustics.

The startle reflex in echolocating odontocetes: basic physiology and practical implications.

The acoustic startle reflex is an oligo-synaptic reflex arc elicited by rapid-onset sounds. Odontocetes evolved a range of specific auditory adaptations to aquatic hearing and echolocation, e.g. the ability to downregulate their auditory sensitivity when emitting clicks. However, it remains unclear whether these adaptations also led to changes of the startle reflex. We investigated reactions to startling sounds in two bottlenose dolphins (Tursiops truncatus) and one false killer whale (Pseudorca crassidens). Animals were exposed to 50 ms, 1/3 octave band noise pulses of varying levels at frequencies of 1, 10, 25 and 32 kHz while positioned in a hoop station. Startle responses were quantified by measuring rapid muscle contractions using a three-dimensional accelerometer attached to the dolphin. Startle magnitude increased exponentially with increasing received levels. Startle thresholds were frequency dependent and ranged from 131 dB at 32 kHz to 153 dB at 1 kHz (re. 1 µPa). Startle thresholds only exceeded masked auditory AEP thresholds of the animals by 47 dB but were ∼82 dB above published behavioural audiograms for these species. We also tested the effect of stimulus rise time on startle magnitude using a broadband noise pulse. Startle responses decreased with increasing rise times from 2 to 100 ms. Models suggested that rise times of 141-220 ms were necessary to completely mitigate startle responses. Our data showed that the startle reflex is conserved in odontocetes and follows similar principles as in terrestrial mammals. These principles should be considered when assessing and mitigating the effects of anthropogenic noise on marine mammals.

Transmission beam pattern and dynamics of a spinner dolphin (Stenella longirostris).

Toothed whales possess a sophisticated biosonar system by which ultrasonic clicks are projected in a highly directional transmission beam. Beam directivity is an important biosonar characteristic that reduces acoustic clutter and increases the acoustic detection range. This study measured click characteristics and the transmission beam pattern from a small odontocete, the spinner dolphin (Stenella longirostis). A formerly stranded individual was rehabilitated and trained to station underwater in front of a 16-element hydrophone array. On-axis clicks showed a mean duration of 20.1 µs, with mean peak and centroid frequencies of 58 and 64 kHz [standard deviation (s.d.) ±30 and ±12 kHz], respectively. Clicks were projected in an oval, vertically compressed beam, with mean vertical and horizontal beamwidths of 14.5° (s.d. ± 3.9) and 16.3° (s.d. ± 4.6), respectively. Directivity indices ranged from 14.9 to 27.4 dB, with a mean of 21.7 dB, although this likely represents a broader beam than what is normally produced by wild individuals. A click subset with characteristics more similar to those described for wild individuals exhibited a mean directivity index of 23.3 dB. Although one of the broadest transmission beams described for a dolphin, it is similar to other small bodied odontocetes.

Modulation rate transfer functions from four species of stranded odontocete (Stenella longirostris, Feresa attenuata, Globicephala melas, and Mesoplodon densirostris).

Odontocete marine mammals explore the environment by rapidly producing echolocation signals and receiving the corresponding echoes, which likewise return at very rapid rates. Thus, it is important that the auditory system has a high temporal resolution to effectively process and extract relevant information from click echoes. This study used auditory evoked potential methods to investigate auditory temporal resolution of individuals from four different odontocete species, including a spinner dolphin (Stenella longirostris), pygmy killer whale (Feresa attenuata), long-finned pilot whale (Globicephala melas), and Blainville's beaked whale (Mesoplodon densirostris). Each individual had previously stranded and was undergoing rehabilitation. Auditory Brainstem Responses (ABRs) were elicited via acoustic stimuli consisting of a train of broadband tone pulses presented at rates between 300 and 2000 Hz. Similar to other studied species, modulation rate transfer functions (MRTFs) of the studied individuals followed the shape of a low-pass filter, with the ability to process acoustic stimuli at presentation rates up to and exceeding 1250 Hz. Auditory integration times estimated from the bandwidths of the MRTFs ranged between 250 and 333 µs. The results support the hypothesis that high temporal resolution is conserved throughout the diverse range of odontocete species.

Off-axis targets maximize bearing Fisher Information in broadband active sonar.

Broadband active sonar systems estimate range from time delay and velocity from Doppler shift. Relatively little attention has been paid to how the received echo spectrum encodes information about the bearing of an object. This letter derives the bearing Fisher Information encoded in the frequency dependent transmitter beampattern. This leads to a counter-intuitive result: directing the sonar beam so that a target of interest is slightly off-axis maximizes the bearing information about the target. Beam aim data from a dolphin biosonar experiment agree closely with the angle predicted to maximize bearing information.

Learning and extinction of conditioned hearing sensation change in the beluga whale (Delphinapterus leucas).

Ice-dwelling beluga whales are increasingly being exposed to anthropogenic loud sounds. Beluga's hearing sensitivity measured during a warning sound just preceding a loud sound was tested using pip-train stimuli and auditory evoked potential recording. When the test/warning stimulus with a frequency of 32 or 45 kHz preceded the loud sound with a frequency of 32 kHz and a sound pressure level of 153 dB re 1 µPa, 2 s, hearing thresholds before the loud sound increased relative to the baseline. The threshold increased up to 15 dB for the test frequency of 45 kHz and up to 13 dB for the test frequency of 32 kHz. These threshold increases were observed during two sessions of 36 trials each. Extinction tests revealed no change during three experimental sessions followed by a jump-like return to baseline thresholds. The low exposure level producing the hearing-dampening effect (156 dB re 1 µPa(2)s in each trial), and the manner of extinction, may be considered as evidence that the observed hearing threshold increases were a demonstration of conditioned dampening of hearing when the whale anticipated the quick appearance of a loud sound in the same way demonstrated in the false killer whale and bottlenose dolphin.

Expectancy and conditioned hearing levels in the bottlenose dolphin (Tursiops truncatus).

The hearing sensitivity of a bottlenose dolphin for a warning sound, when the exact time of the arrival of a loud sound could or could not be predicted, was measured. Sensitivity was measured when the time of onset of the loud sound was randomly varied (random-variation sessions) and when the time of onset of the loud sound and the pattern of stimulus levels was constant (fixed-stimulus sessions). The loud sound was kept the same in both of the series. The mean duration and mean range of the levels of the test/warning signal were also kept equal across experimental sessions. Hearing sensitivity was measured using the auditory evoked potential method with rhythmic trains of short pips as test stimuli. With randomly varied warning sounds, thresholds before the loud sound were on average 10.6 dB higher than the baseline thresholds. With fixed warning signals, thresholds were on average 4.4 dB higher than the baseline thresholds. Considering that the loud sounds were identical, the difference between the random-variation and the fixed-stimulus sessions cannot be explained by a direct (unconditioned) influence of sound exposure. Therefore, the data provide reliable evidence for the conditioning nature of the hearing-dampening effect and also demonstrate that hearing sensitivity change also depends on when the animal can expect the loud sound to occur.

Hearing Sensation Changes When a Warning Predicts a Loud Sound in the False Killer Whale (Pseudorca crassidens).

Stranded whales and dolphins have sometimes been associated with loud anthropogenic sounds. Echolocating whales produce very loud sounds themselves and have developed the ability to protect their hearing from their own signals. A false killer whale's hearing sensitivity was measured when a faint warning sound was given just before the presentation of an increase in intensity to 170 dB. If the warning occurred within 1-9 s, as opposed to 20-40 s, the whale showed a 13-dB reduction in hearing sensitivity. Warning sounds before loud pulses may help mitigate the effects of loud anthropogenic sounds on wild animals.

Hearing in Whales and Dolphins: Relevance and Limitations.

Understanding the hearing of marine mammals has been a priority to quantify and mitigate the impact of anthropogenic sound on these apex predators. Yet our knowledge of cetacean hearing is still limited to a few dozen species, therefore compromising any attempt to design adaptive management strategies. The use of auditory evoked potentials allows scientists to rapidly and noninvasively obtain the hearing data of species rarely available in captivity. Unfortunately, many practical and ethical reasons still limit the availability of large whales, thus restricting the possibility to effectively ensure that anthropogenic sounds have minimum effects on these species. The example of a recent Blainville's beaked whale (Mesoplodon densirostris) audiogram collected after a stranding indicated, for instance, very specialized hearing between 40 and 50 kHz, which corresponded to the frequency-modulated upsweep signals used by this species during echolocation. The methods used during a stranding event are presented along with the major difficulties that have slowed down the scientific community in measuring the audition of large whales and the potential value in obtaining such results when successful.

Conditioned hearing sensitivity change in the harbor porpoise (Phocoena phocoena).

Hearing sensitivity, during trials in which a warning sound preceding a loud sound, was investigated in two harbor porpoises (Phocoena phocoena). Sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. When a hearing test/warning stimulus, with a frequency of either 45 or 32 kHz, preceded a loud 32 kHz tone with a sound pressure level of 152 dB re 1 µPa root mean square, lasting 2 s yielding an sound exposure level (SEL) of 155 dB re 1 µPa(2)s, pooled hearing thresholds measured just before the loud sound increased relative to baseline thresholds. During two experimental sessions the threshold increased up to 17 dB for the test frequency of 45 kHz and up to 11 dB for the test frequency of 32 kHz. An extinction test revealed very rapid threshold recovery within the first two experimental sessions. The SEL producing the hearing dampening effect was low compared to previous other odontocete hearing change efforts with each individual trial equal to 155 dB re 1 µPa(2) but the cumulative SEL for each subsession may have been as high as 168 dB re 1 µPa(2). Interpretations of conditioned hearing sensation change and possible change due to temporary threshold shifts are considered for the harbor porpoise and discussed in the light of potential mechanisms and echolocation.

Transmission beam characteristics of a Risso's dolphin (Grampus griseus).

The echolocation system of the Risso's dolphin (Grampus griseus) remains poorly studied compared to other odontocete species. In this study, echolocation signals were recorded from a stationary Risso's dolphin with an array of 16 hydrophones and the two-dimensional beam shape was explored using frequency-dependent amplitude plots. Click source parameters were similar to those already described for this species. Centroid frequency of click signals increased with increasing sound pressure level, while the beamwidth decreased with increasing center frequency. Analysis revealed primarily single-lobed, and occasionally vertically dual-lobed, beam shapes. Overall beam directivity was found to be greater than that of the harbor porpoise, bottlenose dolphin, and a false killer whale. The relationship between frequency content, beam directivity, and head size for this Risso's dolphin deviated from the trend described for other species. These are the first reported measurements of echolocation beam shape and directivity in G. griseus.

Conditioned frequency-dependent hearing sensitivity reduction in the bottlenose dolphin (Tursiops truncatus).

The frequency specificity of conditioned dampening of hearing, when a loud sound is preceded by a warning sound, was investigated in a bottlenose dolphin. The loud sounds were 5 s tones of 16, 22.5 or 32 kHz, sound pressure level of 165 dB root mean square (RMS) re. 1 µPa. Hearing sensitivity was tested at the same three frequencies. Hearing sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. The test sound stimuli served also as warning sounds. The durations of the warning sounds were varied randomly to avoid locking a conditioning effect to the timing immediately before the loud sound. Hearing thresholds before the loud sound increased, relative to the baseline, at test frequencies equal to or higher than the loud sound frequency. The highest threshold increase appeared at test frequencies of 0.5 octaves above the loud sound frequencies.

Support for the beam focusing hypothesis in the false killer whale.

The odontocete sound production system is complex and composed of tissues, air sacs and a fatty melon. Previous studies suggested that the emitted sonar beam might be actively focused, narrowing depending on target distance. In this study, we further tested this beam focusing hypothesis in a false killer whale. Using three linear arrays of hydrophones, we recorded the same emitted click at 2, 4 and 7 m distance and calculated the beamwidth, intensity, center frequency and bandwidth as recorded on each array at every distance. If the whale did not focus her beam, acoustics predicts the intensity would decay with range as a function of spherical spreading and the angular beamwidth would remain constant. On the contrary, our results show that as the distance from the whale to the array increases, the beamwidth is narrower and the received click intensity is higher than that predicted by a spherical spreading function. Each of these measurements is consistent with the animal focusing her beam on a target at a given range. These results support the hypothesis that the false killer whale is 'focusing' its sonar beam, producing a narrower and more intense signal than that predicted by spherical spreading.

Conditioned hearing sensitivity reduction in a bottlenose dolphin (Tursiops truncatus).

The conditioned change in hearing sensitivity during a warning sound preceding a loud sound was investigated in the bottlenose dolphin. Hearing sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. When the test/warning stimulus with a frequency of 22.5 or 32 kHz preceded the loud sound with a frequency of 22.5 kHz and a sound pressure level of 165 dB re. 1 µPa rms, hearing thresholds before the loud sound increased relative to the baseline. The threshold increased up to 15 dB. In order to further investigate whether the observed threshold increase was due to conditioning, the dependence of the effect on warning duration and inter-trial interval was investigated. The duration of the warning substantially influenced the effect. Shorter warnings resulted in deeper suppression of responses and higher threshold increases than longer warnings. In contrast, the effect was nearly independent of the duration of the inter-trial interval, i.e. it was independent of the delay from the loud sound to the test/warning sound in the subsequent trial. These data are considered as evidence that the observed hearing threshold increases were not a result of the unconditioned effect of the loud sound and were instead a manifestation of a conditioned dampening of hearing when the bottlenose dolphin anticipated the quick appearance of a loud sound in the same way as previously demonstrated in the false killer whale.

Buzzing during biosonar-based interception of prey in the delphinids Tursiops truncatus and Pseudorca crassidens.

Echolocating bats and toothed whales probe their environment with ultrasonic sound pulses, using returning echoes to navigate and find prey in a process that appears to have resulted from a remarkable convergence of the two taxa. Here, we report the first detailed quantification of echolocation behaviour during prey capture in the most studied delphinid species, a false killer whale and a bottlenose dolphin. Using acoustic DTAGs, we demonstrate that just prior to prey interception these delphinids change their acoustic gaze dramatically by reducing inter-click intervals and output >10-fold in a high repetition rate, low output buzz. Buzz click rates of 250-500 Hz for large but agile animals suggest that sampling rates during capture are scaled with the whale's manoeuvrability. These observations support the growing notion that fast sonar sampling accompanied by a low output level is critical for high rate feedback to inform motor patterns during prey interception in all echolocating toothed whales.

Gain control in the sonar of odontocetes.

The sonar of odontocetes processes echo-signals within a wide range of echo levels. The level of echoes varies widely by tens of decibels depending on the level of the emitted sonar pulse, the target strength, the distance to the target, and the sound absorption by the water media. The auditory system of odontocetes must be capable of effective perception, analysis, and discrimination of echo-signals within all this variability. The sonar of odontocetes has several mechanisms to compensate for the echo-level variation (gain control). To date, several mechanisms of the biosonar gain control have been revealed in odontocetes: (1) adjustment of emitted sonar pulse levels (the longer the distance to the target, the higher the level of the emitted pulse), (2) short-term variation of hearing sensitivity based on forward masking of the echo by the preceding self-heard emitted pulse and subsequent release from the masking, and (3) active long-term control of hearing sensitivity. Recent investigations with the use of the auditory evoked-potential technique have demonstrated that these mechanisms effectively minimize the variation of the response to the echo when either the emitted sonar pulse level, or the target distance, or both vary within a wide range. A short review of these data is presented herein.

A false killer whale reduces its hearing sensitivity when a loud sound is preceded by a warning.

We investigated the possibility of conditioned dampening of whale hearing thresholds when a loud sound is preceded by a warning sound. The loud sound was a tone of 20 kHz, 170 dB re. 1 µPa, 5 s. Hearing sensitivity was measured using pip-train test stimuli and auditory evoked potential recording. The same test-sound stimuli served as warning sounds. The durations of the warning sounds were varied randomly to avoid locking an anticipated conditioning effect to the timing immediately before the loud sound. When the warning sound lasted from 1 to 9 s or from 5 to 35 s prior to the loud sound, hearing thresholds before the loud sound increased, relative to the baseline, by 12.7 and 7.3 dB, respectively. When the warning sound duration varied within a range of 20 to 140 s, the threshold increase was as low as 3.0 dB. The observed hearing threshold increase was not a result of the unconditioned effect of the loud sound, like a temporary threshold shift, so it was considered to be a manifestation of a conditioned dampening of hearing when the subject anticipated the quick appearance of a loud sound, most likely to protect its hearing.

Discrimination of phase altered targets by an echolocating Atlantic bottlenose dolphin.

Sensitivity of echolocating dolphins to phase changes within echoes may be a vital piece of information when constructing echolocation models. Previous experiments have yielded ambiguous results leaving it unclear what cues might have been used by passively listening dolphins to discriminate between different phase altered signals. This study used a phantom echo generator to produce computer controlled echoes. The dolphin interacted with the system in a real echolocation task to discriminate between simulated targets that were unaltered and those that had a 180° phase shift. The frequency amplitude spectral content between the two targets was the same. There were no temporal differences between the two targets. The only cue that the dolphin could use to discriminate between them was the 180° phase shift. The dolphin preformed at a success level of 40% in discriminating the two echoes. This indicates that the 180° phase shift was not perceived.

Keeping returns optimal: gain control exerted through sensitivity adjustments in the harbour porpoise auditory system.

Animals that use echolocation (biosonar) listen to acoustic signals with a large range of intensities, because echo levels vary with the fourth power of the animal's distance to the target. In man-made sonar, engineers apply automatic gain control to stabilize the echo energy levels, thereby rendering them independent of distance to the target. Both toothed whales and bats vary the level of their echolocation clicks to compensate for the distance-related energy loss. By monitoring the auditory brainstem response (ABR) during a psychophysical task, we found that a harbour porpoise (Phocoena phocoena), in addition to adjusting the sound level of the outgoing signals up to 5.4 dB, also reduces its ABR threshold by 6 dB when the target distance doubles. This self-induced threshold shift increases the dynamic range of the biosonar system and compensates for half of the variation of energy that is caused by changes in the distance to the target. In combination with an increased source level as a function of target range, this helps the porpoise to maintain a stable echo-evoked ABR amplitude irrespective of target range, and is therefore probably an important tool enabling porpoises to efficiently analyse and classify received echoes.