Accurate species classification of Arctic toothed whale echolocation clicks using one-third octave ratios.

Passive acoustic monitoring has been an effective tool to study cetaceans in remote regions of the Arctic. Here, we advance methods to acoustically identify the only two Arctic toothed whales, the beluga (Delphinapterus leucas) and narwhal (Monodon monoceros), using echolocation clicks. Long-term acoustic recordings collected from moorings in Northwest Greenland were analyzed. Beluga and narwhal echolocation signals were distinguishable using spectrograms where beluga clicks had most energy >30 kHz and narwhal clicks had a sharp lower frequency limit near 20 kHz. Changes in one-third octave levels (TOL) between two pairs of one-third octave bands were compared from over one million click spectra. Narwhal clicks had a steep increase between the 16 and 25 kHz TOL bands that was absent in beluga click spectra. Conversely, beluga clicks had a steep increase between the 25 and 40 kHz TOL bands that was absent in narwhal click spectra. Random Forest classification models built using the 16 to 25 kHz and 25 to 40 kHz TOL ratios accurately predicted the species identity of 100% of acoustic events. Our findings support the use of echolocation TOL ratios in future automated click classifiers for acoustic monitoring of Arctic toothed whales and potentially for other odontocete species.

Implications of porpoise echolocation and dive behaviour on passive acoustic monitoring.

Harbour porpoises are visually inconspicuous but highly soniferous echolocating marine predators that are regularly studied using passive acoustic monitoring (PAM). PAM can provide quality data on animal abundance, human impact, habitat use, and behaviour. The probability of detecting porpoise clicks within a given area (P̂) is a key metric when interpreting PAM data. Estimates of P̂ can be used to determine the number of clicks per porpoise encounter that may have been missed on a PAM device, which, in turn, allows for the calculation of abundance and ideally non-biased comparison of acoustic data between habitats and time periods. However, P̂ is influenced by several factors, including the behaviour of the vocalising animal. Here, the common implicit assumption that changes in animal behaviour have a negligible effect on P̂ between different monitoring stations or across time is tested. Using a simulation-based approach informed by acoustic biologging data from 22 tagged harbour porpoises, it is demonstrated that porpoise behavioural states can have significant (up to 3× difference) effects on P̂. Consequently, the behavioural state of the animals must be considered in analysis of animal abundance to avoid substantial over- or underestimation of the true abundance, habitat use, or effects of human disturbance.

Visual deprivation induces a stronger dive response in a harbor porpoise.

The dive response allows marine mammals to perform prolonged breath-hold dives to access rich marine prey resources. Via dynamic adjustments of peripheral vasoconstriction and bradycardia, oxygen consumption can be tailored to breath-hold duration, depth, exercise, and even expectations during dives. By investigating the heart rate of a trained harbor porpoise during a two-alternative forced choice task, where the animal is either acoustically masked or blindfolded, we test the hypothesis that sensory deprivation will lead to a stronger dive response to conserve oxygen when facing a more uncertain and smaller sensory umwelt. We show that the porpoise halves its diving heart rate (from 55 to 25 bpm) when blindfolded but presents no change in heart rate during masking of its echolocation. Therefore, visual stimuli may matter more to echolocating toothed whales than previously assumed, and sensory deprivation can be a major driver of the dive response, possibly as an anti-predator measure.

Soundscape and ambient noise levels of the Arctic waters around Greenland.

A longer Arctic open water season is expected to increase underwater noise levels due to anthropogenic activities such as shipping, seismic surveys, sonar, and construction. Many Arctic marine mammal species depend on sound for communication, navigation, and foraging, therefore quantifying underwater noise levels is critical for documenting change and providing input to management and legislation. Here we present long-term underwater sound recordings from 26 deployments around Greenland from 2011 to 2020. Ambient noise was analysed in third octave and decade bands and further investigated using generic detectors searching for tonal and transient sounds. Ambient noise levels partly overlap with previous Arctic observations, however we report much lower noise levels than previously documented, specifically for Melville Bay and the Greenland Sea. Consistent seasonal noise patterns occur in Melville Bay, Baffin Bay and Greenland Sea, with noise levels peaking in late summer and autumn correlating with open water periods and seismic surveys. These three regions also had similar tonal detection patterns that peaked in May/June, likely due to bearded seal vocalisations. Biological activity was more readily identified using detectors rather than band levels. We encourage additional research to quantify proportional noise contributions from geophysical, biological, and anthropogenic sources in Arctic waters.

Echolocating toothed whales use ultra-fast echo-kinetic responses to track evasive prey.

Visual predators rely on fast-acting optokinetic responses to track and capture agile prey. Most toothed whales, however, rely on echolocation for hunting and have converged on biosonar clicking rates reaching 500/s during prey pursuits. If echoes are processed on a click-by-click basis, as assumed, neural responses 100× faster than those in vision are required to keep pace with this information flow. Using high-resolution biologging of wild predator-prey interactions, we show that toothed whales adjust clicking rates to track prey movement within 50-200 ms of prey escape responses. Hypothesising that these stereotyped biosonar adjustments are elicited by sudden prey accelerations, we measured echo-kinetic responses from trained harbour porpoises to a moving target and found similar latencies. High biosonar sampling rates are, therefore, not supported by extreme speeds of neural processing and muscular responses. Instead, the neurokinetic response times in echolocation are similar to those of tracking responses in vision, suggesting a common neural underpinning.

In the animal world, split-second decisions determine whether a predator eats, or its prey survives. There is a strong evolutionary advantage to fast reacting brains and bodies. For example, the eye muscles of hunting cheetahs must lock on to a gazelle and keep track of it, no matter how quickly or unpredictably it moves. In fact, in monkeys and primates, these muscles can react to sudden movements in as little as 50 milliseconds ­ faster than the blink of an eye. But what about animals that do not rely on vision to hunt? To find food at night or in the deep ocean, whales and porpoises make short ultrasonic sounds, or 'clicks', and then listen for returning echoes. As they close in on a prey, they need to click faster to get quicker updates on its location. What is unclear is how fast they react to the echoes. Just before a kill, a harbour porpoise can click over 500 times a second: if they wait for the echo from one click before making the next one, they would need responses 100 times faster than human eyes. Exploring this topic is difficult, as it requires tracking predator and prey at the same time. Vance et al. took up the challenge by building sound and movement recorders that attach to whales with suction cups. These were used on two different hunters: deep-diving beaked whales and shallow-hunting harbour porpoises. Both species adapted their click rate depending on how far they were from their prey, but their response times were similar to visual responses in monkeys and humans. This means that whales and porpoises do not act on each echo before clicking again: instead, they respond to groups of tens of clicks at a time. This suggests that their brains may be wired in much the same way as the ones of visual animals. In the ocean, increased human activity creates a dangerous noise pollution that disrupts the delicate hunting mechanism of whales and porpoises. Better understanding how these animals find their food may therefore help conservation efforts.

Do echolocating toothed whales direct their acoustic gaze on- or off-target in a static detection task?

Echolocating mammals produce directional sound beams with high source levels to improve echo-to-noise ratios and reduce clutter. Recent studies have suggested that the differential spectral gradients of such narrow beams are exploited to facilitate target localization by pointing the beam slightly off targets to maximize the precision of angular position estimates [maximizing bearing Fisher information (FI)]. Here, we test the hypothesis that echolocating toothed whales focus their acoustic gaze askew during target detection to maximize spectral cues by investigating the acoustic gaze direction of two trained delphinids (Tursiops truncatus and Pseudorca crassidens) echolocating to detect an aluminum cylinder behind a hydrophone array in a go/no-go paradigm. The animals rarely placed their beam axis directly on the target, nor within the narrow range around the off-axis angle that maximizes FI. However, the target was, for each trial, ensonified within the swath of the half-power beam width, and hence we conclude that the animals solved the detection task using a strategy that seeks to render high echo-to-noise ratios rather than maximizing bearing FI. We posit that biosonar beam adjustment and acoustic gaze strategies are likely task-dependent and that maximizing bearing FI by pointing off-axis does not improve target detection performance.

Context-dependent biosonar adjustments during active target approaches in echolocating harbour porpoises.

Echolocating mammals generally target individual prey items by transitioning through the biosonar phases of search (slow-rate, high-amplitude outputs), approach (gradually increasing rate and decreasing output amplitude) and buzzing (high-rate, low-amplitude outputs). The range to the main target of interest is often considered the key or sole driver of such biosonar adjustments of acoustic gaze. However, the actively generated auditory scene of an echolocator invariably comprises a large number of other reflectors and noise sources that likely also impact the biosonar strategies and source parameters implemented by an echolocating animal in time and space. In toothed whales, the importance of context on biosonar adjustments is largely unknown. To address this, we trained two harbour porpoises to actively approach the same sound recording target over the same approach distance in two highly different environments: a PVC-lined pool and a semi-natural net pen in a harbour, while blind-folded and wearing a sound recording tag (DTAG-4). We show that the approaching porpoises used considerably shorter interclick intervals (ICIs) in the pool than in the net pen, except during the buzz phase, where slightly longer ICIs were used in the pool. We further show that average click source levels were 4-7 dB higher in the net pen. Because of the very low-level in-band ambient noise in both environments, we posit that the porpoises adapted their echolocation strategy to the different reverberation levels between the two settings. We demonstrate that harbour porpoises use different echolocation strategies and biosonar parameters in two different environments for solving an otherwise identical target approach task and thus highlight that biosonar adjustments are both range and context dependent.

Dolphin echolocation behaviour during active long-range target approaches.

Echolocating toothed whales generally adjust click intensity and rate according to target range to ensure that echoes from targets of interest arrive before a subsequent click is produced, presumably facilitating range estimation from the delay between clicks and returning echoes. However, this click-echo-click paradigm for the dolphin biosonar is mostly based on experiments with stationary animals echolocating fixed targets at ranges below ∼120 m. Therefore, we trained two bottlenose dolphins instrumented with a sound recording tag to approach a target from ranges up to 400 m and either touch the target (subject TRO) or detect a target orientation change (subject SAY). We show that free-swimming dolphins dynamically increase interclick interval (ICI) out to target ranges of ∼100 m. TRO consistently kept ICIs above the two-way travel time (TWTT) for target ranges shorter than ∼100 m, whereas SAY switched between clicking at ICIs above and below the TWTT for target ranges down to ∼25 m. Source levels changed on average by 17log10(target range), but with considerable variation for individual slopes (4.1 standard deviations for by-trial random effects), demonstrating that dolphins do not adopt a fixed automatic gain control matched to target range. At target ranges exceeding ∼100 m, both dolphins frequently switched to click packet production in which interpacket intervals exceeded the TWTT, but ICIs were shorter than the TWTT. We conclude that the click-echo-click paradigm is not a fixed echolocation strategy in dolphins, and we demonstrate the first use of click packets for free-swimming dolphins when solving an echolocation task.

Narrow Acoustic Field of View Drives Frequency Scaling in Toothed Whale Biosonar.

Toothed whales are apex predators varying in size from 40-kg porpoises to 50-ton sperm whales that all forage by emitting high-amplitude ultrasonic clicks and listening for weak returning echoes [1, 2]. The sensory field of view of these echolocating animals depends on the characteristics of the biosonar signals and the morphology of the sound generator, yet it is poorly understood how these biophysical relationships have shaped the evolution of biosonar parameters as toothed whales adapted to different foraging niches. Here we test how biosonar output, frequency, and directivity vary with body size to understand the co-evolution of biosonar signals and sound-generating structures. We show that the radiated power increases twice as steeply with body mass (P ∝ M1.47 ± 0.25) than expected from typical scaling laws of call intensity [3], indicating an evolutionary hyperallometric investment into sound production structures that may be driven by a strong selective pressure for long-range biosonar. We find that biosonar frequency scales inversely with body size (F ∝ M-0.19 ± 0.03), resulting in remarkably stable biosonar beamwidth that is independent of body size. We discuss why the three main hypotheses for inverse frequency scaling in animal communication signals [3-5] do not explain frequency scaling in toothed whale biosonar. We instead propose that a narrow acoustic field of view, analogous to the fovea of many visual predators, is the primary evolutionary driver of biosonar frequency in toothed whales, serving as a spatial filter to reduce clutter levels and facilitate long-range prey detection.

Amazon river dolphins (Inia geoffrensis) modify biosonar output level and directivity during prey interception in the wild.

Toothed whales have evolved to live in extremely different habitats and yet they all rely strongly on echolocation for finding and catching prey. Such biosonar-based foraging involves distinct phases of searching for, approaching and capturing prey, where echolocating animals gradually adjust sonar output to actively shape the flow of sensory information. Measuring those outputs in absolute levels requires hydrophone arrays centred on the biosonar beam axis, but this has never been done for wild toothed whales approaching and capturing prey. Rather, field studies make the assumption that toothed whales will adjust their biosonar in the same manner to arrays as they will when approaching prey. To test this assumption, we recorded wild botos (Inia geoffrensis) as they approached and captured dead fish tethered to a hydrophone in front of a star-shaped seven-hydrophone array. We demonstrate that botos gradually decrease interclick intervals and output levels during prey approaches, using stronger adjustment magnitudes than predicted from previous boto array data. Prey interceptions are characterised by high click rates, but although botos buzz during prey capture, they do so at lower click rates than marine toothed whales, resulting in a much more gradual transition from approach phase to buzzing. We also demonstrate for the first time that wild toothed whales broaden biosonar beamwidth when closing in on prey, as is also seen in captive toothed whales and bats, thus resulting in a larger ensonified volume around the prey, probably aiding prey tracking by decreasing the risk of prey evading ensonification.

Amazon river dolphins (Inia geoffrensis) use a high-frequency short-range biosonar.

Toothed whales produce echolocation clicks with source parameters related to body size; however, it may be equally important to consider the influence of habitat, as suggested by studies on echolocating bats. A few toothed whale species have fully adapted to river systems, where sonar operation is likely to result in higher clutter and reverberation levels than those experienced by most toothed whales at sea because of the shallow water and dense vegetation. To test the hypothesis that habitat shapes the evolution of toothed whale biosonar parameters by promoting simpler auditory scenes to interpret in acoustically complex habitats, echolocation clicks of wild Amazon river dolphins were recorded using a vertical seven-hydrophone array. We identified 404 on-axis biosonar clicks having a mean SLpp of 190.3 ± 6.1 dB re. 1 µPa, mean SLEFD of 132.1 ± 6.0 dB re. 1 µPa(2)s, mean Fc of 101.2 ± 10.5 kHz, mean BWRMS of 29.3 ± 4.3 kHz and mean ICI of 35.1 ± 17.9 ms. Piston fit modelling resulted in an estimated half-power beamwidth of 10.2 deg (95% CI: 9.6-10.5 deg) and directivity index of 25.2 dB (95% CI: 24.9-25.7 dB). These results support the hypothesis that river-dwelling toothed whales operate their biosonars at lower amplitude and higher sampling rates than similar-sized marine species without sacrificing high directivity, in order to provide high update rates in acoustically complex habitats and simplify auditory scenes through reduced clutter and reverberation levels. We conclude that habitat, along with body size, is an important evolutionary driver of source parameters in toothed whale biosonars.