Superfast Lombard response in free-flying, echolocating bats.

Acoustic cues are crucial to communication, navigation, and foraging in many animals, which hence face the problem of detecting and discriminating these cues in fluctuating noise levels from natural or anthropogenic sources. Such auditory dynamics are perhaps most extreme for echolocating bats that navigate and hunt prey on the wing in darkness by listening for weak echo returns from their powerful calls in complex, self-generated umwelts.1,2 Due to high absorption of ultrasound in air and fast flight speeds, bats operate with short prey detection ranges and dynamic sensory volumes,3 leading us to hypothesize that bats employ superfast vocal-motor adjustments to rapidly changing sensory scenes. To test this hypothesis, we investigated the onset and offset times and magnitude of the Lombard response in free-flying echolocating greater mouse-eared bats exposed to onsets of intense constant or duty-cycled masking noise during a landing task. We found that the bats invoked a bandwidth-dependent Lombard response of 0.1-0.2 dB per dB increase in noise, with very short delay and relapse times of 20 ms in response to onsets and termination of duty-cycled noise. In concert with the absence call time-locking to noise-free periods, these results show that free-flying bats exhibit a superfast, but hard-wired, vocal-motor response to increased noise levels. We posit that this reflex is mediated by simple closed-loop audio-motor feedback circuits that operate independently of wingbeat and respiration cycles to allow for rapid adjustments to the highly dynamic auditory scenes encountered by these small predators.

Daubenton's bats maintain stereotypical echolocation behaviour and a lombard response during target interception in light.

Most bats hunt insects on the wing at night using echolocation as their primary sensory modality, but nevertheless maintain complex eye anatomy and functional vision. This raises the question of how and when insectivorous bats use vision during their largely nocturnal lifestyle. Here, we test the hypothesis that the small insectivorous bat, Myotis daubentonii, relies less on echolocation, or dispenses with it entirely, as visual cues become available during challenging acoustic noise conditions. We trained five wild-caught bats to land on a spherical target in both silence and when exposed to broad-band noise to decrease echo detectability, while light conditions were manipulated in both spectrum and intensity. We show that during noise exposure, the bats were almost three times more likely to use multiple attempts to solve the task compared to in silent controls. Furthermore, the bats exhibited a Lombard response of 0.18 dB/dBnoise and decreased call intervals earlier in their flight during masking noise exposures compared to in silent controls. Importantly, however, these adjustments in movement and echolocation behaviour did not differ between light and dark control treatments showing that small insectivorous bats maintain the same echolocation behaviour when provided with visual cues under challenging conditions for echolocation. We therefore conclude that bat echolocation is a hard-wired sensory system with stereotyped compensation strategies to both target range and masking noise (i.e. Lombard response) irrespective of light conditions. In contrast, the adjustments of call intervals and movement strategies during noise exposure varied substantially between individuals indicating a degree of flexibility that likely requires higher order processing and perhaps vocal learning.

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.

Wild harbour porpoises startle and flee at low received levels from acoustic harassment device.

Acoustic Harassment Devices (AHD) are widely used to deter marine mammals from aquaculture depredation, and from pile driving operations that may otherwise cause hearing damage. However, little is known about the behavioural and physiological effects of these devices. Here, we investigate the physiological and behavioural responses of harbour porpoises (Phocoena phocoena) to a commercial AHD in Danish waters. Six porpoises were tagged with suction-cup-attached DTAGs recording sound, 3D-movement, and GPS (n = 3) or electrocardiogram (n = 2). They were then exposed to AHDs for 15 min, with initial received levels (RL) ranging from 98 to 132 dB re 1 µPa (rms-fast, 125 ms) and initial exposure ranges of 0.9-7 km. All animals reacted by displaying a mixture of acoustic startle responses, fleeing, altered echolocation behaviour, and by demonstrating unusual tachycardia while diving. Moreover, during the 15-min exposures, half of the animals received cumulative sound doses close to published thresholds for temporary auditory threshold shifts. We conclude that AHD exposure at many km can evoke both startle, flight and cardiac responses which may impact blood-gas management, breath-hold capability, energy balance, stress level and risk of by-catch. We posit that current AHDs are too powerful for mitigation use to prevent hearing damage of porpoises from offshore construction.

Small reductions in cargo vessel speed substantially reduce noise impacts to marine mammals.

Global reductions in the underwater radiated noise levels from cargo vessels are needed to reduce increasing cumulative impacts to marine wildlife. We use a vessel exposure simulation model to examine how reducing vessel source levels through slowdowns and technological modifications can lessen impacts on marine mammals. We show that the area exposed to ship noise reduces markedly with moderate source-level reductions that can be readily achieved with small reductions in speed. Moreover, slowdowns reduce all impacts to marine mammals despite the longer time that a slower vessel takes to pass an animal. We conclude that cumulative noise impacts from the global fleet can be reduced immediately by slowdowns. This solution requires no modification to ships and is scalable from local speed reductions in sensitive areas to ocean basins. Speed reductions can be supplemented by routing vessels away from critical habitats and by technological modifications to reduce vessel noise.

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.

Echolocating Daubenton's bats call louder, but show no spectral jamming avoidance in response to bands of masking noise during a landing task.

Echolocating bats listen for weak echoes to navigate and hunt, which makes them prone to masking from background noise and jamming from other bats and prey. As for electrical fish that display clear spectral jamming avoidance responses (JAR), bats have been reported to mitigate the effects of jamming by shifting the spectral contents of their calls, thereby reducing acoustic interference to improve echo-to-noise ratio (ENR). Here, we tested the hypothesis that frequency-modulating bats (FM bats) employ a spectral JAR in response to six masking noise bands ranging from 15 to 90 kHz, by measuring the -3 dB endpoints and peak frequency of echolocation calls from five male Daubenton's bats (Myotis daubentonii) during a landing task. The bats were trained to land on a noise-generating spherical transducer surrounded by a star-shaped microphone array, allowing for acoustic localization and source parameter quantification of on-axis calls. We show that the bats did not employ spectral JAR as the peak frequency during jamming remained unaltered compared with that of silent controls (all P>0.05, 60.73±0.96 kHz, mean±s.e.m.), and -3 dB endpoints decreased in noise irrespective of treatment type. Instead, Daubenton's bats responded to acoustic jamming by increasing call amplitude via a Lombard response that was bandwidth dependent, ranging from a mean of 0.05 dB/dB (95% confidence interval 0.04-0.06 dB/dB) noise for the most narrowband noise (15-30 kHz) to 0.17 dB/dB (0.16-0.18 dB/dB) noise for the most broadband noise (30-90 kHz). We conclude that Daubenton's bats, despite having the vocal flexibility to do so, do not employ a spectral JAR, but defend ENRs via a bandwidth-dependent Lombard response.

Echolocating Daubenton's bats are resilient to broadband, ultrasonic masking noise during active target approaches.

Echolocating bats hunt prey on the wing under conditions of poor lighting by emission of loud calls and subsequent auditory processing of weak returning echoes. To do so, they need adequate echo-to-noise ratios (ENRs) to detect and distinguish target echoes from masking noise. Early obstacle avoidance experiments report high resilience to masking in free-flying bats, but whether this is due to spectral or spatiotemporal release from masking, advanced auditory signal detection or an increase in call amplitude (Lombard effect) remains unresolved. We hypothesized that bats with no spectral, spatial or temporal release from masking noise defend a certain ENR via a Lombard effect. We trained four bats (Myotis daubentonii) to approach and land on a target that broadcasted broadband noise at four different levels. An array of seven microphones enabled acoustic localization of the bats and source level estimation of their approach calls. Call duration and peak frequency did not change, but average call source levels (SLRMS, at 0.1 m as dB re. 20 µPa) increased, from 112 dB in the no-noise treatment, to 118 dB (maximum 129 dB) at the maximum noise level of 94 dB re. 20 µPa root mean square. The magnitude of the Lombard effect was small (0.13 dB SLRMS dB-1 of noise), resulting in mean broadband and narrowband ENRs of -11 and 8 dB, respectively, at the highest noise level. Despite these poor ENRs, the bats still performed echo-guided landings, making us conclude that they are very resilient to masking even when they cannot avoid it spectrally, spatially or temporally.

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.

Cryptic vocal behavior of foraging humpback whales on feeding grounds in West Greenland.

Male humpback whales (Megaptera novaeangliae) sing in mating aggregations in the form of song displays, but much less is known about how both sexes use sound on their feeding grounds. Here, we test different hypotheses about the function of vocalizations in 14 foraging humpback whales tagged with sound and movement recording Dtags in Greenland. We show that this population of foraging humpback whales have an overall low call rate of 11.9 calls h-1 (inter-quartile range = 12.1) with no support for the hypotheses that they employ sound in the localization or manipulation of prey nor in the coordination of lunge feeding. The calls had a mean received level of 135 ± 5dB re 1 µPa, which is some 30 dB lower than maximum levels of song recorded on similar deployed tags, suggesting a much smaller active space of these vocalizations. This reduced active space might, in concert with low call rates, serve to mitigate eavesdropping by predatory killer whales or conspecifics competing for the same prey resources. We conclude that feeding humpback whales in Greenland produce low level, infrequent calls suggesting that calling is not a prerequisite for successful feeding, but likely serves to mediate within group social interactions.

Hunting bats adjust their echolocation to receive weak prey echoes for clutter reduction.

How animals extract information from their surroundings to guide motor patterns is central to their survival. Here, we use echo-recording tags to show how wild hunting bats adjust their sensory strategies to their prey and natural environment. When searching, bats maximize the chances of detecting small prey by using large sensory volumes. During prey pursuit, they trade spatial for temporal information by reducing sensory volumes while increasing update rate and redundancy of their sensory scenes. These adjustments lead to very weak prey echoes that bats protect from interference by segregating prey sensory streams from the background using a combination of fast-acting sensory and motor strategies. Counterintuitively, these weak sensory scenes allow bats to be efficient hunters close to background clutter broadening the niches available to hunt for insects.

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.

The long-range echo scene of the sperm whale biosonar.

Sperm whales use their gigantic nose to produce the most powerful sounds in the animal kingdom, presumably to echolocate deep-sea prey at long ranges and possibly to debilitate prey. To test these hypotheses, we deployed sound recording tags (DTAG-4) on the tip of the nose of three sperm whales. One of these recordings yielded over 6000 echo streams from organisms detected up to 144 m ahead of the whale, supporting a long-range prey detection function of the sperm whale biosonar. The whale navigated this complex acoustic scene by maintaining a stable, long-range acoustic gaze suggesting continual resource evaluation. Less than 10% of the echoic organisms recorded by the tag were targeted for capture and only 18% of the buzzes were emitted within the 50 m depth interval of maximum organism encounter rate, demonstrating echo-guided prey selection. Buzzes were initiated more than 20 m from the prey, showing that sperm whales do not debilitate their prey with sound, but trade echo levels for reduced forward masking and rapid updates on prey location in keeping with the lower manoeuvrability of these large predators. We conclude that the powerful biosonar of sperm whales enables long-range echolocation and selection of prey, but not acoustic debilitation.

Energy compensation and received echo level dynamics in constant-frequency bats during active target approaches.

Bats have been reported to adjust the energy of their outgoing vocalizations to target range (R) in a logarithmic fashion close to 20log10R which has been interpreted as providing one-way compensation for increasing echo levels during target approaches. However, it remains unknown how species using high-frequency calls, which are strongly affected by absorption, adjust their vocal outputs during approaches to point targets. We hypothesized that such species should compensate less than the 20log10R model predicts at longer distances and more at shorter distances as a consequence of the significant influence of absorption at longer ranges. Using a microphone array and an acoustic recording tag, we show that the output adjustments of two Hipposideros pratti and one Hipposiderosarmiger do not decrease logarithmically during approaches to different-sized targets. Consequently, received echo levels increase dramatically early in the approach phase with near-constant output levels, but level off late in the approach phase as a result of substantial output reductions. To improve echo-to-noise ratio, we suggest that bats using higher frequency vocalizations compensate less at longer ranges, where they are strongly affected by absorption. Close to the target, they decrease their output levels dramatically to mitigate reception of very high echo levels. This strategy maintains received echo levels between 6 and 40 dB re. 20 µPa2 s across different target sizes. The bats partially compensated for target size, but not in a one-to-one dB fashion, showing that these bats do not seek to stabilize perceived echo levels, but may instead use them to gauge target size.

Deep-diving pilot whales make cheap, but powerful, echolocation clicks with 50 µL of air.

Echolocating toothed whales produce powerful clicks pneumatically to detect prey in the deep sea where this long-range sensory channel makes them formidable top predators. However, air supplies for sound production compress with depth following Boyle's law suggesting that deep-diving whales must use very small air volumes per echolocation click to facilitate continuous sensory flow in foraging dives. Here we test this hypothesis by analysing click-induced acoustic resonances in the nasal air sacs, recorded by biologging tags. Using 27000 clicks from 102 dives of 23 tagged pilot whales (Globicephala macrorhynchus), we show that click production requires only 50 µL of air/click at 500 m depth increasing gradually to 100 µL at 1000 m. With such small air volumes, the metabolic cost of sound production is on the order of 40 J per dive which is a negligible fraction of the field metabolic rate. Nonetheless, whales must make frequent pauses in echolocation to recycle air between nasal sacs. Thus, frugal use of air and periodic recycling of very limited air volumes enable pilot whales, and likely other toothed whales, to echolocate cheaply and almost continuously throughout foraging dives, providing them with a strong sensory advantage in diverse aquatic habitats.

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.

Long-term sound and movement recording tags to study natural behavior and reaction to ship noise of seals.

The impact of anthropogenic noise on marine fauna is of increasing conservation concern with vessel noise being one of the major contributors. Animals that rely on shallow coastal habitats may be especially vulnerable to this form of pollution.Very limited information is available on how much noise from ship traffic individual animals experience, and how they may react to it due to a lack of suitable methods. To address this, we developed long-duration audio and 3D-movement tags (DTAGs) and deployed them on three harbor seals and two gray seals in the North Sea during 2015-2016.These tags recorded sound, accelerometry, magnetometry, and pressure continuously for up to 21 days. GPS positions were also sampled for one seal continuously throughout the recording period. A separate tag, combining a camera and an accelerometer logger, was deployed on two harbor seals to visualize specific behaviors that helped interpret accelerometer signals in the DTAG data.Combining data from depth, accelerometer, and audio sensors, we found that animals spent 6.6%-42.3% of the time hauled out (either on land or partly submerged), and 5.3%-12.4% of their at-sea time resting at the sea bottom, while the remaining time was used for traveling, resting at surface, and foraging. Animals were exposed to audible vessel noise 2.2%-20.5% of their time when in water, and we demonstrate that interruption of functional behaviors (e.g., resting) in some cases coincides with high-level vessel noise. Two-thirds of the ship noise events were traceable by the AIS vessel tracking system, while one-third comprised vessels without AIS.This preliminary study demonstrates how concomitant long-term continuous broadband on-animal sound and movement recordings may be an important tool in future quantification of disturbance effects of anthropogenic activities at sea and assessment of long-term population impacts on pinnipeds.

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.