Click Emission Research Articles

Acoustic behaviour in bottlenose dolphins during two different target discrimination tasks

Echolocation is an active sensory system that gives an acoustic representation of the surroundings by the animal emitting clicks, detecting and analysing echoes. However, little is known about dolphin biosonar in moving animals, as well as of the process of controlling click emissions, and the cues used by the animal to discriminate between different targets. We studied how bottlenose dolphins may use their dynamic sound production and hearing abilities, along with head and body movements, to detect and classify objects through echolocation. We designed two different experiments with blindfolded bottlenose dolphins (Tursiups truncatus) swimming freely along the pool and actively discriminating between two targets of three different materials, and a second one to determine the capability to discriminate wall thickness differences in cylindrical targets of the same material. By means of synchronized cameras and hydrophones, we observed clear differences between individuals of the same species in terms of ability to discriminate, but similar performance with the harbor porpoises in relation to the materials chosen with the difficulty of the task. Studying how the dolphins solved a simplified echolocation task, allow a better understanding of the processes behind target detection and discrimination capabilities during natural biosonar circumstances .

Latencies of click-evoked auditory responses in a harbor porpoise exceed the time interval between subsequent echolocation clicks.

Most auditory evoked potential (AEP) studies in echolocating toothed whales measure neural responses to outgoing clicks and returning echoes using short-latency auditory brainstem responses (ABRs) arising a few ms after acoustic stimuli. However, little is known about longer-latency cortical AEPs despite their relevance for understanding echo processing and auditory stream segregation. Here, we used a non-invasive AEP setup with low click repetition rates on a trained harbor porpoise to test the long-standing hypothesis that echo information from distant targets is completely processed before the next click is emitted. We reject this hypothesis by finding reliable click-related AEP peaks with latencies of 90 and 160 ms, which are longer than 99% of click intervals used by echolocating porpoises, demonstrating that some higher-order echo processing continues well after the next click emission even during slow clicking. We propose that some of the echo information, such as range to evasive prey, is used to guide vocal-motor responses within 50-100 ms, but that information used for discrimination and auditory scene analysis is processed more slowly, integrating information over many click-echo pairs. We conclude by showing theoretically that the identified long-latency AEPs may enable hearing sensitivity measurements at frequencies ten times lower than current ABR methods.

The loud crowd: Interactions between stocking density and acoustic feeding activity of different size classes of Litopenaeus vannamei

Passive acoustic monitoring (PAM) has been used to evaluate Litopenaeus vannamei feeding activity, as shrimp mandibles emit click sounds during food ingestion. PAM has also been used as a tool to estimate the population density of several aquatic species. Although stocking density is an important factor in shrimp farming, there is no information about its effect on shrimp acoustics during feeding activity. The present study aimed to explore the interactions between stocking density and acoustic activity of L. vannamei of different size classes under laboratory conditions. The trials were conducted in three circular fiberglass tanks using three shrimp stocking densities (50, 100 and 150 shrimp m−2) and four size classes (1, 3, 9 and 12 g). Recordings of feeding activity were carried out using omnidirectional hydrophones (sampling rate: 96 kHz; 16 bits) installed in each trial tank and lasted 30 min. Shrimp were fed with commercial pelleted diet and the uneaten food was collected to calculate the food consumption at the end of each recording. The clicks emitted by shrimp during acoustic recordings were automatically detect using Raven® acoustic software. The shrimp acoustic activity started immediately upon feed was offered, reaching the maximum click emission rate during the first minute and lasting up to about 10 min. The clicking emission rate shown a significant progressive increase from the lowest to the highest shrimp size class and stocking density, suggesting that a calibration approach can be applied to predict the population density when feeding sound signals are detectable. Significantly linear relationships between food consumption and number of clicks emitted by all size classes and stocking densities confirms that PAM is a feasible tool to estimate shrimp feed intake. Taken together, the present findings provide novel information about interactions between stocking density and acoustic activity that can contribute to research and development of feeding management in shrimp aquaculture.

Echolocation variability of franciscana dolphins (Pontoporia blainvillei) between estuarine and open-sea habitats, with insights into foraging patterns.

Environmental and ecological factors can trigger changes in the acoustic repertoire of cetaceans. This study documents the first use of a well-established passive acoustic monitoring device (C-POD) to analyze echolocation sounds and behavior of franciscana dolphins in different habitats: estuary [Babitonga Bay (BB)] and open sea [Itapirubá Beach (IB)]. A total of 10 924 click trains were recorded in BB and 6 093 in IB. An inter-click interval < 10 ms (so called "feeding buzzes") was used as a proxy for foraging activity. The main difference in the acoustic parameters between the two habitats was related to the frequency spectrum, with higher maximum and lower modal and minimum click frequencies in BB, and a train frequency range of 17 kHz, against 10 kHz in IB. Also, the click emission rate (clicks/s) was almost 20% higher in BB. Both studied habitats showed a high proportion of feeding buzzes (BB = 68%; IB = 58%), but with a higher probability of occurrence in BB (p < 0.001) and at night (p < 0.001) in both habitats. The C-PODs showed great potential to monitor occurrence, bioacoustics parameters, and echolocation behavior of franciscana dolphins. Longer-term temporal and spatial monitoring are necessary for elucidating several issues raised in this study.

Increased emission intensity can compensate for the presence of noise in human click-based echolocation

Echolocating bats adapt their emissions to succeed in noisy environments. In the present study we investigated if echolocating humans can detect a sound-reflecting surface in the presence of noise and if intensity of echolocation emissions (i.e. clicks) changes in a systematic pattern. We tested people who were blind and had experience in echolocation, as well as blind and sighted people who had no experience in echolocation prior to the study. We used an echo-detection paradigm where participants listened to binaural recordings of echolocation sounds (i.e. they did not make their own click emissions), and where intensity of emissions and echoes changed adaptively based on participant performance (intensity of echoes was yoked to intensity of emissions). We found that emission intensity had to systematically increase to compensate for weaker echoes relative to background noise. In fact, emission intensity increased so that spectral power of echoes exceeded spectral power of noise by 12 dB in 4-kHz and 5-kHz frequency bands. The effects were the same across all participant groups, suggesting that this effect occurs independently of long-time experience with echolocation. Our findings demonstrate for the first time that people can echolocate in the presence of noise and suggest that one potential strategy to deal with noise is to increase emission intensity to maintain signal-to-noise ratio of certain spectral components of the echoes.

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.]

A biosonar model of finless porpoise (Neophocaena phocaenoides) for material composition discrimination of cylinders.

Research into the physical mechanism of odontocetes biosonar has made great progress in the past several decades, especially on wave propagation and biosonar beam formation in the foreheads of odontocetes. Although a number of experimental studies have been performed, the physical mechanism of odontocetes underwater target discrimination has not yet been fully understood. Previous research has experimentally studied the finless porpoise's target discrimination using cylinders different in material [Nakahara, Takemura, Koido, and Hiruda (1997). Mar. Mamm. Sci. 13(4), 639-649]. The authors proposed a computed tomography based finite element biosonar model to simulate the detailed process of a finless porpoise click emission and target detection in order to gain a further understanding of the underlying physical mechanism. The numerical solutions of resonance features of both steel and acrylic cylinders in this study are very consistent with the analytic solutions. Furthermore, the simulated outgoing clicks and echoes match the experiment results measured by Nakahara et al. The beam patterns of the scattered field were extracted and the resonance features of cylinders in different materials were analyzed. This method in this study could be used to study some other odontocetes that are inaccessible for experimental work and could also provide physical information for intelligent biomimetic underwater signal processors design.

Jittered echo-delay resolution in bottlenose dolphins (Tursiops truncatus)

Psychophysical methods similar to those employed with bats were used to examine jittered echo-delay resolution in bottlenose dolphins (Tursiops truncatus). Two dolphins were trained to produce echolocation clicks and report a change from electronic echoes with a fixed delay of ~ 12.6 ms (~ 9.4 m simulated range) to echoes with delays that alternated (jittered) between successive emitted signals. Jitter delays varied from 0 to 50 µs. Jittered echo-delay thresholds were between 1 and 2 µs—the lowest achievable (non-zero) values with the hardware configuration. Error functions matched the click autocorrelation function near zero jitter delay, and were well within the envelope of the autocorrelation function; however, measured jitter delay thresholds were larger than predictions for a coherent or semicoherent receiver at comparable signal-to-noise ratios. When one of the two alternating jittered echoes was inverted in polarity, both dolphins reliably discriminated echoes at all jittered echo delays, including 0 µs (i.e., only jittering in polarity, not delay). Finally, both dolphins used unusual patterns of click emissions, where groups of echolocation clicks were interspersed with silent gaps. Further tests with sub-microsecond jitter values and various echo signal-to-noise ratios would be necessary for proper direct comparison with jitter detection values obtained for bats.

Click emission in Dall's porpoise Phocoenoides dalli, focusing on physical properties of tissues.

Dall’s porpoise (Phocoenoides dalli) is one of most common North Pacific porpoise species, for which information on sound-emitting processes is limited. To evaluate the mechanism of click emission in the head of this porpoise, the distribution of acoustic impedance in head tissues was calculated using density and Young’s modulus‘which is a measure of linear resistance to linear compression. Two Dall’s porpoise heads were examined: one for macroscopic dissection, and one for investigating the distribution of acoustic impedance calculated from CT-measured density, and Young’s modulus measured by creep meter. Acoustic impedance increased from the dorsal bursae to the melon’s emitting surface, with impedance matching observed at the boundary between the emitting surface and seawater, and was more similar in distribution to Young’s modulus than it was to density. The distribution of acoustic impedance differed from that of harbor porpoise (Phocoena phocoena), despite similarities in the sound-producing organs in the heads of Dall’s and harbor porpoises. A comparison of the physical properties of Dall’s and harbor porpoise head tissues suggests that hypertrophic vestibular sacs and an oval emitting surface are common characteristics in Phocoenidae.

Bottlenose dolphin (Tursiops truncatus) sonar slacks off before touching a non-alimentary target

Odontocetes modulate the rhythm of their echolocation clicks to draw information about their environment. When they approach preys to capture, they speed up their emissions to increase the sampling rate of “distant touch” and improve information update. This global acceleration turns into a “terminal buzz” also described in bats, which is a click train with drastic increase in rate, just as reaching the prey. This study documents and analyses under human care bottlenose dolphins’ echolocation activity, when approaching non-alimentary targets. Four dolphins’ locomotor and clicking behaviours were recorded during training sessions, when sent to immersed objects pointed by their trainers. Results illustrate that these dolphins profusely use echolocation towards immersed non-alimentary objects. They accelerate click emission when approaching the target, thus displaying a classical terminal buzz. However, their terminal buzz slackens off within a quarter of second before the end of click train. Typically, they decelerate to stop clicking just before they touch the object using their rostrum lower tip. They do not emit clicks as the contact lasts. In conclusion, when exploring inert objects, bottlenose dolphins under human accelerate clicking like other odontocetes or bats approaching preys. Bottlenose dolphins’ particular slackening-off profile at the end of the buzz shows that they anticipate the moment of direct contact, and they stop just as real touch relays distant touch of the object.

Non-auditory, electrophysiological potentials preceding dolphin biosonar click production

The auditory brainstem response to a dolphin’s own emitted biosonar click can be measured by averaging epochs of the instantaneous electroencephalogram (EEG) that are time-locked to the emitted click. In this study, averaged EEGs were measured using surface electrodes placed on the head in six different configurations while dolphins performed an echolocation task. Simultaneously, biosonar click emissions were measured using contact hydrophones on the melon and a hydrophone in the farfield. The averaged EEGs revealed an electrophysiological potential (the pre-auditory wave, PAW) that preceded the production of each biosonar click. The largest PAW amplitudes occurred with the non-inverting electrode just right of the midline—the apparent side of biosonar click generation—and posterior of the blowhole. Although the source of the PAW is unknown, the temporal and spatial properties rule out an auditory source. The PAW may be a neural or myogenic potential associated with click production; however, it is not known if muscles within the dolphin nasal system can be actuated at the high rates reported for dolphin click production, or if sufficiently coordinated and fast motor endplates of nasal muscles exist to produce a PAW detectable with surface electrodes.

Echo jitter delay discrimination in bottlenose dolphins (Tursiops truncatus)

Experiments with bats show echo delay discrimination capabilities on sub-microsecond scales, which is an acuity that is much higher than that predicted by the auditory nervous system’s ability to directly encode high-frequency phase information (i.e., through neural phase locking). To provide a cross-species comparison, echoic discrimination experiments were conducted with two bottlenose dolphins. Dolphins were trained to echolocate a “phantom” target and report a change from a target with a static delay of ~12 ms to one with alternating delay, or “jitter,” imposed on the static delay. Performance was measured as a function of jitter delay. Both dolphins were able to reliably detect jitter down to ±1 μs, although lower amounts of jitter were not detected. When the jittered echo was phase shifted by 180° relative to the static echo, performance was near 100% at all jitter delays, including ±0 μs. Both dolphins utilized intermittent patterns of click emissions, which were unusual for the relatively short ranges employed. Bottlenose dolphins do not appear to possess the sub-microsecond delay acuity capabilities observed in some bats. However, the current results suggest that dolphins can encode information resembling echo phase information in determining target range. [Funding from ONR.]

Mouth-clicks used by blind expert human echolocators - signal description and model based signal synthesis.

Echolocation is the ability to use sound-echoes to infer spatial information about the environment. Some blind people have developed extraordinary proficiency in echolocation using mouth-clicks. The first step of human biosonar is the transmission (mouth click) and subsequent reception of the resultant sound through the ear. Existing head-related transfer function (HRTF) data bases provide descriptions of reception of the resultant sound. For the current report, we collected a large database of click emissions with three blind people expertly trained in echolocation, which allowed us to perform unprecedented analyses. Specifically, the current report provides the first ever description of the spatial distribution (i.e. beam pattern) of human expert echolocation transmissions, as well as spectro-temporal descriptions at a level of detail not available before. Our data show that transmission levels are fairly constant within a 60° cone emanating from the mouth, but levels drop gradually at further angles, more than for speech. In terms of spectro-temporal features, our data show that emissions are consistently very brief (~3ms duration) with peak frequencies 2-4kHz, but with energy also at 10kHz. This differs from previous reports of durations 3-15ms and peak frequencies 2-8kHz, which were based on less detailed measurements. Based on our measurements we propose to model transmissions as sum of monotones modulated by a decaying exponential, with angular attenuation by a modified cardioid. We provide model parameters for each echolocator. These results are a step towards developing computational models of human biosonar. For example, in bats, spatial and spectro-temporal features of emissions have been used to derive and test model based hypotheses about behaviour. The data we present here suggest similar research opportunities within the context of human echolocation. Relatedly, the data are a basis to develop synthetic models of human echolocation that could be virtual (i.e. simulated) or real (i.e. loudspeaker, microphones), and which will help understanding the link between physical principles and human behaviour.

Audible sonar images generated with proprioception for target analysis

Some blind humans have demonstrated the ability to detect and classify objects with echolocation using palatal clicks. An audible-sonar robot mimics human click emissions, binaural hearing, and head movements to extract interaural time and level differences from target echoes. Targets of various complexity are examined by transverse displacements of the sonar and by target pose rotations that model movements performed by the blind. Controlled sonar movements executed by the robot provide data that model proprioception information available to blind humans for examining targets from various aspects. The audible sonar uses this sonar location and orientation information to form two-dimensional target images that are similar to medical diagnostic ultrasound tomograms. Simple targets, such as single round and square posts, produce distinguishable and recognizable images. More complex targets configured with several simple objects generate diffraction effects and multiple reflections that produce image artifacts. The presentation illustrates the capabilities and limitations of target classification from audible sonar images.

Using “phantom” echoes to study dolphin biosonar

Biosonar studies have greatly benefited from the use of electronic, or “phantom,” echoes. In this paradigm, amplitude and timing information are extracted from an emitted biosonar pulse, then a delayed signal is broadcast to the animal to appear as an echo from a more distant target. Phantom echoes provide unique capabilities for studying biosonar, since they allow echo features such as amplitude and delay to be independently manipulated. In 1987, Whit Au and colleagues described a phantom echo system for use with marine mammals [Au et al. (1987). “Phantom electronic target for dolphin sonar research,” J. Acoust. Soc. Am. 82, 711-713]. In this system, delayed broadcasts of one or more replicas of the dolphin click were triggered by dolphin click emissions. A major improvement in phantom echo systems was later described by Aubauer and Au (1998) [“Phantom echo generation: A new technique for investigating dolphin echolocation,” J. Acoust. Soc. Am. 104, 1165-1170], who simulated the impulse response of a physical target, rather than broadcasting a stereotyped waveform. In this talk, phantom echo system concepts are briefly presented and several recent applications of phantom echo systems—inspired by the work of Aubauer and Au—are discussed. [Work supported by ONR.]

Nearfield and farfield measurements of dolphin echolocation beam patterns: No evidence of focusing.

The potential for bottlenose dolphins to actively focus their biosonar transmissions was examined by measuring emitted clicks in four dolphins using horizontal, planar hydrophone arrays. Two hydrophone configurations were used: a rectangular array with hydrophones 0.2 to 2 m from the dolphins and a polar array with hydrophones 0.5 to 5 m from the dolphins. The biosonar task was a target change detection utilizing physical targets at ranges from 1.3 to 6.3 m with all subjects and "phantom" targets at simulated ranges from 2.5 to 20 m with two subjects. To provide a basis for evaluating the experimental data, sound fields radiated from flat and focused circular pistons were mathematically simulated using transient excitation functions similar to dolphin clicks. The array measurements showed no evidence that the dolphins adaptively focused their click emissions; axial amplitudes and iso-amplitude contours matched the pattern of the simulation results for flat transducers and showed a single region of maximum amplitude, beyond which spherical spreading loss was approximated.

Short-term enhancement and suppression of dolphin auditory evoked responses following echolocation click emission.

Biosonar gain control mechanisms in a bottlenose dolphin were investigated by measuring the auditory steady-state response (ASSR) to an external tone while the animal echolocated. The dolphin performed an echo change-detection task that utilized electronically synthesized echoes with echo delays corresponding to 25- and 50-m target range. During the task, amplitude modulated tones with carrier frequencies from 25 to 125 kHz were continuously presented and the instantaneous electroencephalogram stored for later analysis. ASSRs were extracted from the electroencephalogram by synchronously averaging time epochs temporally aligned with the onset of the external tone modulation cycle nearest to each of the dolphin's echolocation clicks. Results showed an overall suppression of the ASSR amplitude for tones with frequencies near the click center frequencies. A larger, temporary suppression of the ASSR amplitude was also measured at frequencies above 40-50 kHz, while a temporary enhancement was observed at lower frequencies. Temporal patterns for ASSR enhancement or suppression were frequency-, level-, and range-dependent, with recovery to pre-click values occurring within the two-way travel time. Suppressive effects fit the patterns expected from forward masking by the emitted biosonar pulse, while the specific mechanisms responsible for the frequency-dependent enhancement are unknown.

Auditory steady-state response measurement of the temporal dynamics of hearing sensitivity in an echolocating bottlenose dolphin (Tursiops truncatus)

Studies with some echolocating odontocetes demonstrate that receiver-based automatic gain control (AGC) compensates for reductions in echo strength resulting from acoustic spreading loss. This study examined AGC in an echolocating bottlenose dolphin by measuring changes in hearing sensitivity over time courses corresponding to single click-echo pairs. The electrophysiological auditory steady-state response (ASSR) elicited by a 113-kHz sinusoidally amplitude-modulated tone was recorded while the dolphin performed a target discrimination task. Auditory electrophysiological responses were extracted from the instantaneous electroencephalogram and coherently averaged using the modulation rate of the 113-kHz tone as a reference. A Fourier transform was then performed with a 10-ms sliding window to obtain the ASSR amplitude as a function of time relative to the dolphin’s outgoing click and received echo. The ASSR amplitude initially decreased at the time of click emission and then recovered over a course of 25 to 70 ms, depending on target range. This relatively long time course of recovery appears to be consistent with forward-masking, as opposed to an AGC mechanism based on the contraction and gradual release of middle ear muscles coincident with click emission. [Work funded by SSC Pacific Naval Innovative Science and Engineering (NISE) program.]

Using the auditory steady-state response to assess temporal dynamics of hearing sensitivity during bottlenose dolphin echolocation

The auditory steady-state response (ASSR) to an external tone was measured in an echolocating dolphin to determine if hearing sensitivity changes could be tracked over time scales corresponding to single click-echo pairs. Individual epochs containing click-echo pairs were first extracted from the instantaneous electroencephalogram. Epochs were coherently averaged using the external tone modulation rate as a timing reference, then Fourier transformed using a sliding, 10-ms temporal window to obtain the ASSR amplitude as a function of time. The results revealed a decrease in the ASSR amplitude at the time of click emission, followed by a 25-70 ms recovery.