A statistical acoustics approach for estimating population-scale bowhead whale migration speed and direction.

Bowhead whales vocalize during their annual fall migration from the Beaufort Sea to the Bering Sea, but the calling rates of individual animals are so low that tracking an individual trajectory is impractical using passive acoustic methods. However, the travel speed and direction of the migrating population can be inferred on a statistical basis by cross-correlating time sequences of call density measured at two locations spaced several kilometers apart. By using the triangulation abilities of a set of vector sensors deployed offshore the Alaskan North Slope between 2008 and 2014, call density time sequences were generated from 1-km wide and 40-km tall rectangular "zones" that were separated by distances ranging from 3.5 to 15 km. The cross-covariances between the two sequences generate a peak corresponding to the average time it takes for whales to travel between the zones. Consistent westward travel speeds of ∼5 km/h were obtained from four different locations on 6 of the 7 years of the study, independent of whether the zones were separated by 3.5, 7, or 15 km. Some sites, however, also revealed a less prominent eastern movement of whales, and shifts in migration speed were occasionally detectable over week-long time scales.

Narwhal (Monodon monoceros) echolocation click rates to support cue counting passive acoustic density estimation.

Estimating animal abundance is fundamental for effective management and conservation. It is increasingly done by combining passive acoustics with knowledge about rates at which animals produce cues (cue rates). Narwhals (Monodon monoceros) are elusive marine mammals for which passive acoustic density estimation might be plausible, but for which cue rates are lacking. Clicking rates in narwhals were investigated using a dataset from sound and movement tag records collected in August 2013-2016 and 2019 in East Greenland. Clicking rates were quantified for ∼1200 one-second-long systematic random samples from 8 different whales. Generalized additive models were used to model (1) the probability of being in a clicking state versus depth and (2) the clicking rate while in a clicking state, versus time and depth. The probability of being in a clicking state increased with depth, reaching ∼1.0 at ∼500 m, while the number of clicks per second (while in a clicking state) increased with depth. The mean cue production rate, weighted by tag duration, was 1.28 clicks per second (se = 0.13, CV = 0.10). This first cue rate for narwhals may be used for cue counting density estimation, but care should be taken if applying it to other geographical areas or seasons, given sample size, geographical, and temporal limitations.

Stuck in a corner: Anthropogenic noise threatens narwhals in their once pristine Arctic habitat.

Niche-conservative species are especially susceptible to changes in their environment, and detecting the negative effects of new stressors in their habitats is vital for safeguarding of these species. In the Arctic, human disturbance including marine traffic and exploration of resources is increasing rapidly due to climate change-induced reduction of sea ice. Here, we show that the narwhal, Monodon monoceros, is extremely sensitive to human-made noise. Narwhals avoided deep diving (> 350 m) with simultaneous reduction of foraging and increased shallow diving activity as a response to either ship sound alone or ship sound with concurrent seismic airgun pulses. Normal behavior decreased by 50 to 75% at distances where received sound levels were below background noise. Narwhals were equally responsive to both disturbance types, hence demonstrating their acute sensitivity to ship sound. This sensitivity coupled with their special behavioral-ecological strategy including a narrow ecological niche and high site fidelity makes them thus especially vulnerable to human impacts in the Arctic.

Using quantile regression and relative entropy to assess the period of anomalous behavior of marine mammals following tagging.

Tagging of animals induces a variable stress response which following release will obscure natural behavior. It is of scientific relevance to establish methods that assess recovery from such behavioral perturbation and generalize well to a broad range of animals, while maintaining model transparency. We propose two methods that allow for subdivision of animals based on covariates, and illustrate their use on N = 20 narwhals (Monodon monoceros) and N = 4 bowhead whales (Balaena mysticetus), captured and instrumented with Acousonde™ behavioral tags, but with a framework that easily generalizes to other marine animals and sampling units. The narwhals were divided into two groups based on handling time, short ( t < 58 min) and long ( t ≥ 58 min), to measure the effect on recovery. Proxies for energy expenditure (VeDBA) and rapid movement (jerk) were derived from accelerometer data. Diving profiles were characterized using two metrics (target depth and dive duration) derived from depth data. For accelerometer data, recovery was estimated using quantile regression (QR) on the log-transformed response, whereas depth data were addressed using relative entropy (RE) between hourly distributions of dive duration (partitioned into three target depth ranges) and the long-term average distribution. Quantile regression was used to address location-based behavior to accommodate distributional shifts anticipated in aquatic locomotion. For all narwhals, we found fast recovery in the tail of the distribution (<3 h) compared with a variable recovery at the median (∼1-10 h) and with a significant difference between groups separated by handling time. Estimates of bowhead whale recovery times showed fast median recovery (<3 h) and slow recovery at the tail (>6 h), but were affected by substantial uncertainty. For the diving profiles, as characterized by the component pair (target depth, dive duration), the recovery was slower (narwhals-long: t < 16 h; narwhals-short: t < 10 h; bowhead whales: <9 h) and with a difference between narwhals with short vs long handling times. Using simple statistical concepts, we have presented two transparent and general methods for analyzing high-resolution time series data from marine animals, addressing energy expenditure, activity, and diving behavior, and which allows for comparison between groups of animals based on well-defined covariates.

Extremely low seasonal prey capture efficiency in a deep-diving whale, the narwhal.

Successful foraging is essential for individuals to maintain the positive energy balance required for survival and reproduction. Yet, prey capture efficiency is poorly documented in marine apex predators, especially deep-diving mammals. We deployed acoustic tags and stomach temperature pills in summer to collect concurrent information on presumed foraging activity (through buzz detection) and successful prey captures (through drops in stomach temperature), providing estimates of feeding efficiency in narwhals. Compared to the daily number of buzzes (707 ± 368), the daily rate of feeding events was particularly low in summer (19.8 ± 8.9) and only 8-14% of the foraging dives were successful (i.e. with a detectable prey capture). This extremely low success rate resulted in a very low daily food consumption rate (less than 0.5% of body mass), suggesting that narwhals rely on body reserves accumulated in winter to sustain year-round activities. The expected changes or disappearance of their wintering habitats in response to climate change may therefore have severe fitness consequences for narwhal populations.

Narwhals react to ship noise and airgun pulses embedded in background noise.

Anthropogenic activities are increasing in the Arctic, posing a threat to niche-conservative species with high seasonal site fidelity, such as the narwhal Monodon monoceros. In this controlled sound exposure study, six narwhals were live-captured and instrumented with animal-borne tags providing movement and behavioural data, and exposed to concurrent ship noise and airgun pulses. All narwhals reacted to sound exposure with reduced buzzing rates, where the response was dependent on the magnitude of exposure defined as 1/distance to ship. Buzzing rate was halved at 12 km from the ship, and whales ceased foraging at 7-8 km. Effects of exposure could be detected at distances > 40 km from the ship.At only a few kilometres from the ship, the received high-frequency cetacean weighted sound exposure levels were below background noise indicating extreme sensitivity of narwhals towards sound disturbance and demonstrating their ability to detect signals embedded in background noise. The narwhal's reactions to sustained disturbance may have a plethora of consequences both at individual and population levels. The observed reactions of the whales demonstrate their auditory sensitivity but also emphasize, that anthropogenic activities in pristine narwhal habitats needs to be managed carefully if healthy narwhal populations are to be maintained.

Measurements of open-water arctic ocean noise directionality and transport velocity.

Measurements from bottom-mounted acoustic vector sensors, deployed seasonally between 2008 and 2014 on the shallow Beaufort Sea shelf along the Alaskan North Slope, are used to estimate the ambient sound pressure power spectral density, acoustic transport velocity of energy, and dominant azimuth between 25 and 450 Hz. Even during ice-free conditions, this region has unusual acoustic features when compared against other U.S. coastal regions. Two distinct regimes exist in the diffuse ambient noise environment: one with high pressure spectral density levels but low directionality, and another with lower spectral density levels but high directionality. The transition between the two states, which is invisible in traditional spectrograms, occurs between 73 and 79 dB re 1 µPa2/Hz at 100 Hz, with the transition region occurring at lower spectral levels at higher frequencies. Across a wide bandwidth, the high-directionality ambient noise consistently arrives from geographical azimuths between 0° and 30° from true north over multiple years and locations, with a seasonal interquartile range of 40° at low frequencies and high transport velocities. The long-term stability of this directional regime, which is believed to arise from the dominance of wind-driven sources along an east-west coastline, makes it an important feature of arctic ambient sound.

Evidence of stereotyped contact call use in narwhal (Monodon monoceros) mother-calf communication.

Narwhals (Monodon monoceros) are gregarious toothed whales that strictly reside in the high Arctic. They produce a broad range of signal types; however, studies of narwhal vocalizations have been mostly descriptive of the sounds available in the species' overall repertoire. Little is known regarding the functions of highly stereotyped mixed calls (i.e., biphonations with both sound elements produced simultaneously), although preliminary evidence has suggested that such vocalizations are individually distinctive and function as contact calls. Here we provide evidence that supports this notion in narwhal mother-calf communication. A female narwhal was tagged as part of larger studies on the life history and acoustic behavior of narwhals. At the time of tagging, it became apparent that the female had a calf, which remained close by during the tagging event. We found that the narwhal mother produced a distinct, highly stereotyped mixed call when separated from her calf and immediately after release from capture, which we interpret as preliminary evidence for contact call use between the mother and her calf. The mother's mixed call production occurred continually over the 4.2 day recording period in addition to a second prominent but different stereotyped mixed call which we believe belonged to the narwhal calf. Thus, narwhal mothers produce highly stereotyped contact calls when separated from their calves, and it appears that narwhal calves similarly produce distinct, stereotyped mixed calls which we hypothesize also contribute to maintaining mother-calf contact. We compared this behavior to the acoustic behavior of two other adult females without calves, but also each with a unique, stereotyped call type. While we provide additional support for individual distinctiveness across narwhal contact calls, more research is necessary to determine whether these calls are vocal signatures which broadcast identity.

Estimating acoustic cue rates in bowhead whales, Balaena mysticetus, during their fall migration through the Alaskan Beaufort Sea.

Eight years of passive acoustic data (2007-2014) from the Beaufort Sea were used to estimate the mean cue rate (calling rate) of individual bowhead whales (Balaena mysticetus) during their fall migration along the North Slope of Alaska. Calls detected on directional acoustic recorders (DASARs) were triangulated to provide estimates of locations at times of call production, which were then translated into call densities (calls/h/km2). Various assumptions were used to convert call density into animal cue rates, including the time for whales to cross the arrays of acoustic recorders, the population size, the fraction of the migration corridor missed by the localizing array system, and the fraction of the seasonal migration missed because recorders were retrieved before the end of the migration. Taking these uncertainties into account in various combinations yielded up to 351 cue rate estimates, which summarize to a median of 1.3 calls/whale/h and an interquartile range of 0.5-5.4 calls/whale/h.

Some like it cold: Temperature-dependent habitat selection by narwhals.

The narwhal (Monodon monoceros) is a high-Arctic species inhabiting areas that are experiencing increases in sea temperatures, which together with reduction in sea ice are expected to modify the niches of several Arctic marine apex predators. The Scoresby Sound fjord complex in East Greenland is the summer residence for an isolated population of narwhals. The movements of 12 whales instrumented with Fastloc-GPS transmitters were studied during summer in Scoresby Sound and at their offshore winter ground in 2017-2019. An additional four narwhals provided detailed hydrographic profiles on both summer and winter grounds. Data on diving of the whales were obtained from 20 satellite-linked time-depth recorders and 16 Acousonde™ recorders that also provided information on the temperature and depth of buzzes. In summer, the foraging whales targeted depths between 300 and 850 m where the preferred areas visited by the whales had temperatures ranging between 0.6 and 1.5°C (mean = 1.1°C, SD = 0.22). The highest probability of buzzing activity during summer was at a temperature of 0.7°C and at depths > 300 m. The whales targeted similar depths at their offshore winter ground where the temperature was slightly higher (range: 0.7-1.7°C, mean = 1.3°C, SD = 0.29). Both the probability of buzzing events and the spatial distribution of the whales in both seasons demonstrated a preferential selection of cold water. This was particularly pronounced in winter where cold coastal water was selected and warm Atlantic water farther offshore was avoided. It is unknown if the small temperature niche of whales while feeding is because prey is concentrated at these temperature gradients and is easier to capture at low temperatures, or because there are limitations in the thermoregulation of the whales. In any case, the small niche requirements together with their strong site fidelity emphasize the sensitivity of narwhals to changes in the thermal characteristics of their habitats.

Roaring and repetition: How bowhead whales adjust their call density and source level (Lombard effect) in the presence of natural and seismic airgun survey noise.

Over 500 000 automated and manual acoustic localizations, measured over seven years between 2008 and 2014, were used to examine how natural wind-driven noise and anthropogenic seismic airgun survey noise influence bowhead whale call densities (calls/km2/min) and source levels during their fall migration in the Alaskan Beaufort Sea. Noise masking effects, which confound measurements of behavioral changes, were removed using a modified point transect theory. The authors found that mean call densities generally rose with increasing continuous wind-driven noise levels. The occurrence of weak airgun pulse sounds also prompted an increase in call density equivalent to a 10-15 dB change in natural noise level, but call density then dropped substantially with increasing cumulative sound exposure level (cSEL) from received airgun pulses. At low in-band noise levels the mean source level of the acoustically-active population changed to nearly perfectly compensate for noise increases, but as noise levels increased further the mean source level failed to keep pace, reducing the population's communication space. An increase of >40 dB cSEL from seismic airgun activity led to an increase in source levels of just a few decibels. These results have implications for bowhead acoustic density estimation, and evaluations of the masking impacts of anthropogenic noise.

Spatial and temporal patterns of sound production in East Greenland narwhals.

Changes in climate are rapidly modifying the Arctic environment. As a result, human activities-and the sounds they produce-are predicted to increase in remote areas of Greenland, such as those inhabited by the narwhals (Monodon monoceros) of East Greenland. Meanwhile, nothing is known about these whales' acoustic behavior or their reactions to anthropogenic sounds. This lack of knowledge was addressed by instrumenting six narwhals in Scoresby Sound (Aug 2013-2016) with Acousonde™ acoustic tags and satellite tags. Continuous recordings over up to seven days were used to describe the acoustic behavior of the whales, in particular their use of three types of sounds serving two different purposes: echolocation clicks and buzzes, which serve feeding, and calls, presumably used for social communication. Logistic regression models were used to assess the effects of location in time and space on buzzing and calling rates. Buzzes were mostly produced at depths of 350-650 m and buzzing rates were higher in one particular fjord, likely a preferred feeding area. Calls generally occurred at shallower depths (<100 m), with more than half of these calls occurring near the surface (<7 m), where the whales also spent more than half of their time. A period of silence following release, present in all subjects, was attributed to the capture and tagging operations, emphasizing the importance of longer (multi-day) records. This study provides basic life-history information on a poorly known species-and therefore control data in ongoing or future sound-effect studies.

Paradoxical escape responses by narwhals (Monodon monoceros).

Until recent declines in Arctic sea ice levels, narwhals (Monodon monoceros) have lived in relative isolation from human perturbation and sustained predation pressures. The resulting naïvety has made this cryptic, deep-diving cetacean highly susceptible to disturbance, although quantifiable effects have been lacking. We deployed a submersible, animal-borne electrocardiograph-accelerometer-depth recorder to monitor physiological and behavioral responses of East Greenland narwhals after release from net entanglement and stranding. Escaping narwhals displayed a paradoxical cardiovascular down-regulation (extreme bradycardia with heart rate ≤4 beats per minute) superimposed on exercise up-regulation (stroke frequency >25 strokes per minute and energetic costs three to six times the resting rate of energy expenditure) that rapidly depleted onboard oxygen stores. We attribute this unusual reaction to opposing cardiovascular signals-from diving, exercise, and neurocognitive fear responses-that challenge physiological homeostasis.

Effects of tones associated with drilling activities on bowhead whale calling rates.

During summer 2012 Shell performed exploratory drilling at Sivulliq, a lease holding located in the autumn migration corridor of bowhead whales (Balaena mysticetus), northwest of Camden Bay in the Beaufort Sea. The drilling operation involved a number of vessels performing various activities, such as towing the drill rig, anchor handling, and drilling. Acoustic data were collected with six arrays of directional recorders (DASARs) deployed on the seafloor over ~7 weeks in Aug-Oct. Whale calls produced within 2 km of each DASAR were identified and localized using triangulation. A "tone index" was defined to quantify the presence and amplitude of tonal sounds from industrial machinery. The presence of airgun pulses originating from distant seismic operations was also quantified. For each 10-min period at each of the 40 recorders, the number of whale calls localized was matched with the "dose" of industrial sound received, and the relationship between calling rates and industrial sound was modeled using negative binomial regression. The analysis showed that with increasing tone levels, bowhead whale calling rates initially increased, peaked, and then decreased. This dual behavioral response is similar to that described for bowhead whales and airgun pulses in earlier work. Increasing call repetition rates can be a viable strategy for combating decreased detectability of signals arising from moderate increases in background noise. Meanwhile, as noise increases, the benefits of calling may decrease because information transfer becomes increasingly error-prone, and at some point calling may no longer be worth the effort.

Decadal-scale frequency shift of migrating bowhead whale calls in the shallow Beaufort Sea.

Automated and manual acoustic localizations of bowhead whale calls in the Beaufort Sea were used to estimate the minimum frequency attained by their highly variable FM-modulated call repertoire during seven westerly fall migrations. Analyses of 13 355 manual and 100 009 automated call localizations found that between 2008 and 2014 the proportion of calls that dipped below 75 Hz increased from 27% to 41%, shifting the mean value of the minimum frequency distribution from 94 to 84 Hz. Multivariate regression analyses using both generalized linear models and generalized estimating equations found that this frequency shift persisted even when accounting for ten other factors, including calling depth, call range, call type, noise level, signal-to-noise ratio, local water depth (site), airgun activity, and call spatial density. No single call type was responsible for the observed shift, but so-called "complex" calls experienced larger percentage downward shifts. By contrast, the call source level distribution remained stable over the same period. The observed frequency shift also could not be explained by migration corridor shifts, relative changes in call detectability between different frequency bands, long-term degradation in the automated airgun detector, physiological growth in the population, or behavioral responses to increasing population density (estimated via call density).

Acoustic vector sensor beamforming reduces masking from underwater industrial noise during passive monitoring.

Masking from industrial noise can hamper the ability to detect marine mammal sounds near industrial operations, whenever conventional (pressure sensor) hydrophones are used for passive acoustic monitoring. Using data collected from an autonomous recorder with directional capabilities (Directional Autonomous Seafloor Acoustic Recorder), deployed 4.1 km from an arctic drilling site in 2012, the authors demonstrate how conventional beamforming on an acoustic vector sensor can be used to suppress noise arriving from a narrow sector of geographic azimuths. Improvements in signal-to-noise ratio of up to 15 dB are demonstrated on bowhead whale calls, which were otherwise undetectable using conventional hydrophones.

Source level and calling depth distributions of migrating bowhead whale calls in the shallow Beaufort Sea.

Automated and manual acoustic localizations of migrating bowhead whales were used to estimate source level and calling depth distributions of their frequency-modulated-modulated calls over seven years between 2008 and 2014. Whale positions were initially triangulated using directional autonomous seafloor acoustic recorders, deployed between 25 and 55 m water depth near Kaktovik, Alaska, during the fall westward migration. Calling depths were estimated by minimizing the "discrepancy" between source level estimates from at least three recorders detecting the same call. Applying a detailed waveguide propagation model to the data yielded broadband source levels of 161 ± 9 dB re 1 µPa2 s at 1 m (SEL) for calls received between 20 and 170 Hz. Applying a simpler 15 log10(R) power-law propagation model yielded SEL source levels of 158 ± 10 dB. The most probable calling depths lay between 22 and 30 m: optimal depths for long-range acoustic signal transmission in this particular environment.

Effects of airgun sounds on bowhead whale calling rates: evidence for two behavioral thresholds.

In proximity to seismic operations, bowhead whales (Balaena mysticetus) decrease their calling rates. Here, we investigate the transition from normal calling behavior to decreased calling and identify two threshold levels of received sound from airgun pulses at which calling behavior changes. Data were collected in August-October 2007-2010, during the westward autumn migration in the Alaskan Beaufort Sea. Up to 40 directional acoustic recorders (DASARs) were deployed at five sites offshore of the Alaskan North Slope. Using triangulation, whale calls localized within 2 km of each DASAR were identified and tallied every 10 minutes each season, so that the detected call rate could be interpreted as the actual call production rate. Moreover, airgun pulses were identified on each DASAR, analyzed, and a cumulative sound exposure level was computed for each 10-min period each season (CSEL10-min). A Poisson regression model was used to examine the relationship between the received CSEL10-min from airguns and the number of detected bowhead calls. Calling rates increased as soon as airgun pulses were detectable, compared to calling rates in the absence of airgun pulses. After the initial increase, calling rates leveled off at a received CSEL10-min of ~94 dB re 1 µPa2-s (the lower threshold). In contrast, once CSEL10-min exceeded ~127 dB re 1 µPa2-s (the upper threshold), whale calling rates began decreasing, and when CSEL10-min values were above ~160 dB re 1 µPa2-s, the whales were virtually silent.

Ranging bowhead whale calls in a shallow-water dispersive waveguide.

This paper presents the performance of three methods for estimating the range of broadband (50-500 Hz) bowhead whale calls in a nominally 55-m-deep waveguide: Conventional mode filtering (CMF), synthetic time reversal (STR), and triangulation. The first two methods use a linear vertical array to exploit dispersive propagation effects in the underwater sound channel. The triangulation technique used here, while requiring no knowledge about the propagation environment, relies on a distributed array of directional autonomous seafloor acoustics recorders (DASARs) arranged in triangular grid with 7 km spacing. This study uses simulations and acoustic data collected in 2010 from coastal waters near Kaktovik, Alaska. At that time, a 12-element vertical array, spanning the bottom 63% of the water column, was deployed alongside a distributed array of seven DASARs. The estimated call location-to-array ranges determined from CMF and STR are compared with DASAR triangulation results for 19 whale calls. The vertical-array ranging results are generally within ±10% of the DASAR results with the STR results providing slightly better agreement. The results also indicate that the vertical array can range calls over larger ranges and with greater precision than the particular distributed array discussed here, whenever the call locations are beyond the distributed array boundaries.

Range estimation of bowhead whale (Balaena mysticetus) calls in the Arctic using a single hydrophone.

Bowhead whales generate low-frequency calls in shallow-water Arctic environments, whose dispersive propagation characteristics are well modeled by normal mode theory. As each mode propagates with a different group speed, a call's range can be inferred by the relative time-frequency dispersion of the modal arrivals. Traditionally, at close ranges modal arrivals are separated using synchronized hydrophone arrays. Here a nonlinear signal processing method called "warping" is used to filter the modes on just a single hydrophone. The filtering works even at relatively short source ranges, where distinct modal arrivals are not separable in a conventional spectrogram. However, this warping technique is limited to signals with monotonically increasing or decreasing frequency modulations, a relatively common situation for bowhead calls. Once modal arrivals have been separated, the source range can be estimated using conventional modal dispersion techniques, with the original source signal structure being recovered as a by-product. Twelve bowhead whale vocalizations recorded near Kaktovik (Alaska) in 2010, with signal-to-noise ratios between 6 and 23 dB, are analyzed, and the resulting single-receiver range estimates are consistent with those obtained independently via triangulation from widely-distributed vector sensor arrays. Geoacoustic inversions for each call are necessary in order to obtain the correct ranges.