Killer whale presence drives bowhead whale selection for sea ice in Arctic seascapes of fear.

The effects of predator intimidation on habitat use and behavior of prey species are rarely quantified for large marine vertebrates over ecologically relevant scales. Using state space movement models followed by a series of step selection functions, we analyzed movement data of concurrently tracked prey, bowhead whales (Balaena mysticetus; n = 7), and predator, killer whales (Orcinus orca; n = 3), in a large (63,000 km2), partially ice-covered gulf in the Canadian Arctic. Our analysis revealed pronounced predator-mediated shifts in prey habitat use and behavior over much larger spatiotemporal scales than previously documented in any marine or terrestrial ecosystem. The striking shift from use of open water (predator-free) to dense sea ice and shorelines (predators present) was exhibited gulf-wide by all tracked bowheads during the entire 3-wk period killer whales were present, constituting a nonconsumptive effect (NCE) with unknown energetic or fitness costs. Sea ice is considered quintessential habitat for bowhead whales, and ice-covered areas have frequently been interpreted as preferred bowhead foraging habitat in analyses that have not assessed predator effects. Given the NCEs of apex predators demonstrated here, however, unbiased assessment of habitat use and distribution of bowhead whales and many marine species may not be possible without explicitly incorporating spatiotemporal distribution of predation risk. The apparent use of sea ice as a predator refuge also has implications for how bowhead whales, and likely other ice-associated Arctic marine mammals, will cope with changes in Arctic sea ice dynamics as historically ice-covered areas become increasingly ice-free during summer.

Range-dependent impacts of ocean acoustic propagation on automated classification of transmitted bowhead and humpback whale vocalizations.

Significant effort has been made over the last few decades to develop automated passive acoustic monitoring (PAM) systems capable of classifying cetaceans at the species level. The utility of such systems depends on the systems' ability to operate across a wide range of ocean acoustic environments; however, anecdotal evidence suggests that site-specific propagation characteristics impact the performance of PAM systems. Variability in propagation characteristics leads to differences in how each cetacean vocalization is altered as it propagates along the source-receiver path. A propagation experiment was conducted in the Gulf of Mexico to investigate the range-dependent impacts of acoustic propagation on the performance of an automated classifier. Modified bowhead and humpback vocalizations were transmitted over ranges from 1 to 10 km. When the classifier was trained with signals collected near the sound source, it was found that the performance decreased with increasing transmission range-this appeared to be largely explained by decreasing signal-to-noise ratio (SNR). Generation of performance matrices showed that one method to develop a classifier that maintains high performance across many ranges is to include a varied assortment of ranges in the training data; however, if the training set is limited, it is best to train on relatively low SNR vocalizations.

Extreme diversity in the songs of Spitsbergen's bowhead whales.

Almost all mammals communicate using sound, but few species produce complex songs. Two baleen whales sing complex songs that change annually, though only the humpback whale (Megaptera novaeangliae) has received much research attention. This study focuses on the other baleen whale singer, the bowhead whale (Balaena mysticetus). Members of the Spitsbergen bowhead whale population produced 184 different song types over a 3-year period, based on duty-cycled recordings from a site in Fram Strait in the northeast Atlantic. Distinct song types were recorded over short periods, lasting at most some months. This song diversity could be the result of population expansion, or immigration of animals from other populations that are no longer isolated from each other by heavy sea ice. However, this explanation does not account for the within season and annual shifting of song types. Other possible explanations for the extraordinary diversity in songs could be that it results either from weak selection pressure for interspecific identification or for maintenance of song characteristics or, alternatively, from strong pressure for novelty in a small population.

Abundance estimate of the Okhotsk Sea population of the bowhead whale (Balaena mysticetus Linnaeus, 1758).

Abundance of 388 ± 108 whales for the Okhotsk Sea bowhead whale population based on individual genotyping was estimated using the capture-recapture method for the open population model. The data demonstrate that this endangered population shows no signs of recovery.

Current Status of Development of Methods to Assess Effects of Cumulative or Aggregated Underwater Sounds on Marine Mammals.

There are no standards for assessment of the cumulative effects of underwater sound. Quantitative assessments typically consider a single source, whereas qualitative assessments may include multiple sources but rarely identify response variables. As a step toward understanding the cumulative effects of underwater sound, we assessed the aggregated sounds of multiple sources received by migrating bowhead whales (Balaena mysticetus). The quantitative method models the sound field from multiple sources and simulates movement of a population through it. The qualitative method uses experts to assess the responses of individuals and populations to sound sources and identify the potential mechanisms. These methods increase the transparency of assessments.

A Summary Comparison of Active Acoustic Detections and Visual Observations of Marine Mammals in the Canadian Beaufort Sea.

Fisheries sonar was used to determine the applicability of active acoustic monitoring (AAM) for marine mammal detection in the Canadian Beaufort Sea. During 170 h of simultaneous observation by marine mammal observers and active acoustic observation, 119 Balaena mysticetus (bowheads) and 4 Delphinapterus leucas (belugas) were visually sighted, while 59 acoustic signals of bowheads were detected by AAM operators. Observations and detection of seals were also recorded. Comparative results indicate that commercially available active acoustic systems can detect seals at distances up to 500 m and large baleen whales at distances up to 2 km.

Summer molting of bowhead whales Balaena mysticetus Linnaeus, 1758, of the Okhotsk Sea population.

In bowhead whales summering in Ulbanskiy Bay of the Okhotsk Sea, molting of epidermis has been found and histologically confirmed. The outer layer of the molting whale epidermis is longitudinally stratified and rejected in the form of relatively large plates up to several millimeters thick, each representing a lamellar formation consisting of longitudinal rows of parakeratocytes with degenerated nuclei, numerous pigment granules, and lipid inclusions. Molting intensity is correlated with the level of proliferation and regeneration of all epidermal layers, which helps to maintain the optimal skin thickness.

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.

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.

Automated aural classification used for inter-species discrimination of cetaceans.

Passive acoustic methods are in widespread use to detect and classify cetacean species; however, passive acoustic systems often suffer from large false detection rates resulting from numerous transient sources. To reduce the acoustic analyst workload, automatic recognition methods may be implemented in a two-stage process. First, a general automatic detector is implemented that produces many detections to ensure cetacean presence is noted. Then an automatic classifier is used to significantly reduce the number of false detections and classify the cetacean species. This process requires development of a robust classifier capable of performing inter-species classification. Because human analysts can aurally discriminate species, an automated aural classifier that uses perceptual signal features was tested on a cetacean data set. The classifier successfully discriminated between four species of cetaceans-bowhead, humpback, North Atlantic right, and sperm whales-with 85% accuracy. It also performed well (100% accuracy) for discriminating sperm whale clicks from right whale gunshots. An accuracy of 92% and area under the receiver operating characteristic curve of 0.97 were obtained for the relatively challenging bowhead and humpback recognition case. These results demonstrated that the perceptual features employed by the aural classifier provided powerful discrimination cues for inter-species classification of cetaceans.

Flow-dependent porosity and other biomechanical properties of mysticete baleen.

Despite its vital function in a highly dynamic environment, baleen is typically assumed to be a static material. Its biomechanical and material properties have not previously been explored. Thus I tested sections of baleen from bowhead whales, Balaena mysticetus, and humpback whales, Megaptera novaeangliae, alone or in groups representing miniature 'racks', in a flow tank through which water and buoyant particles circulated with variable flow velocity. Kinematic sequences were recorded through an endoscopic camera or viewing window. One set of experiments investigated particle capture; another series analyzed biomechanical behavior, including fringe spacing, movement and interaction. Baleen fringe porosity directly correlates, in a mostly linear fashion, with velocity of incident water flow. However, undulation and interaction of fringes (especially of bowheads) at higher flow velocities can decrease porosity. Fringe porosity depends on distance from the baleen plate. Porosity also varies, with fringe length, by position along the length of an individual plate. Plate orientation, which varied from 0 to 90 deg relative to water flow, is crucial in fringe spacing and particle capture. At all flow velocities, porosity is lowest with plates aligned parallel to water flow. Turbulence introduced when plates rotate perpendicular to flow (as in cross-flow filtration) increases fringe interaction, so that particles more easily strike fringes yet more readily dislodge. Baleen of bowhead whales, which feed by continuous ram filtration, differs biomechanically from that of humpbacks, which use intermittent lunge filtration. The longer, finer fringes of bowhead baleen readily form a mesh-like mat, especially at higher flow velocities, to trap tiny particles.

Bowhead whale acoustic activity in the southeast Beaufort Sea during late 2008-2010.

Autonomous passive acoustic recorders were deployed to record sounds of bowhead whales (Balaena mysticetus) in the southeast Beaufort Sea for periods of 30-55 days during the late summer, open-water seasons of 2008-2010. Recordings were made in three areas licensed for hydrocarbon exploration, spanning the continental slope and adjacent outer shelf, and in a shallow inner-shelf area where bowheads have been observed congregating to feed in recent decades. Bowhead sounds were counted in samples comprising 10% of each recorded hour. In mid-August and September in all 3 years, the rate of bowhead calling at outer shelf sites exceeded that at adjacent continental slope sites by one to two orders of magnitude. Higher rates of calling occurred on the slope in late July and early August than at later dates. Calling rates varied by an order of magnitude between years in the one area that was monitored in different years. The highest rates of calling occurred on the inner shelf, offshore of the northern Tuktoyaktuk Peninsula. These trends are consistent with patterns of habitat use previously reported from aerial surveys in this and nearby areas of the Beaufort Sea and with the results of satellite tagging studies.

The Northwest Passage opens for bowhead whales.

The loss of Arctic sea ice is predicted to open up the Northwest Passage, shortening shipping routes and facilitating the exchange of marine organisms between the Atlantic and the Pacific oceans. Here, we present the first observations of distribution overlap of bowhead whales (Balaena mysticetus) from the two oceans in the Northwest Passage, demonstrating this route is already connecting whales from two populations that have been assumed to be separated by sea ice. Previous satellite tracking has demonstrated that bowhead whales from West Greenland and Alaska enter the ice-infested channels of the Canadian High Arctic during summer. In August 2010, two bowhead whales from West Greenland and Alaska entered the Northwest Passage from opposite directions and spent approximately 10 days in the same area, documenting overlap between the two populations.

Automated detection and localization of bowhead whale sounds in the presence of seismic airgun surveys.

An automated procedure has been developed for detecting and localizing frequency-modulated bowhead whale sounds in the presence of seismic airgun surveys. The procedure was applied to four years of data, collected from over 30 directional autonomous recording packages deployed over a 280 km span of continental shelf in the Alaskan Beaufort Sea. The procedure has six sequential stages that begin by extracting 25-element feature vectors from spectrograms of potential call candidates. Two cascaded neural networks then classify some feature vectors as bowhead calls, and the procedure then matches calls between recorders to triangulate locations. To train the networks, manual analysts flagged 219 471 bowhead call examples from 2008 and 2009. Manual analyses were also used to identify 1.17 million transient signals that were not whale calls. The network output thresholds were adjusted to reject 20% of whale calls in the training data. Validation runs using 2007 and 2010 data found that the procedure missed 30%-40% of manually detected calls. Furthermore, 20%-40% of the sounds flagged as calls are not present in the manual analyses; however, these extra detections incorporate legitimate whale calls overlooked by human analysts. Both manual and automated methods produce similar spatial and temporal call distributions.

Evidence for simultaneous sound production in the bowhead whale (Balaena mysticetus).

Simultaneous production of two harmonically independent sounds, the two-voice phenomenon, is a well-known feature in bird song. Some toothed whales can click and whistle simultaneously, and a few studies have also reported simultaneous sound production by baleen whales. The mechanism for sound production in toothed whales has been largely uncovered within the last three decades, whereas mechanism for sound production in baleen whales remains poorly understood. This study provides three lines of evidence from recordings made in 2008 and 2009 in Disko Bay, Western Greenland, strongly indicating that bowhead whales are capable of simultaneous dual frequency sound production. This capability may function to enable more complex singing in an acoustically mediated reproductive advertisement display, as has been suggested for songbirds, and/or have significance in individual recognition.

Bowhead and beluga whale acoustic detections in the western Beaufort Sea 2008-2018.

The Distributed Biological Observatory (DBO) was established to detect environmental changes in the Pacific Arctic by regular monitoring of biophysical responses in each of 8 DBO regions. Here we examine the occurrence of bowhead and beluga whale vocalizations in the western Beaufort Sea acquired by acoustic instruments deployed from September 2008-July 2014 and September 2016-October 2018 to examine inter-annual variability of these Arctic endemic species in DBO Region 6. Acoustic data were collected on an oceanographic mooring deployed in the Beaufort shelfbreak jet at ~71.4°N, 152.0°W. Spectrograms of acoustic data files were visually examined for the presence or absence of known signals of bowhead and beluga whales. Weekly averages of whale occurrence were compared with outputs of zooplankton, temperature and sea ice from the BIOMAS model to determine if any of these variables influenced whale occurrence. In addition, the dates of acoustic whale passage in the spring and fall were compared to annual sea ice melt-out and freeze-up dates to examine changes in phenology. Neither bowhead nor beluga whale migration times changed significantly in spring, but bowhead whales migrated significantly later in fall from 2008-2018. There were no clear relationships between bowhead whales and the environmental variables, suggesting that the DBO 6 region is a migratory corridor, but not a feeding hotspot, for this species. Surprisingly, beluga whale acoustic presence was related to zooplankton biomass near the mooring, but this is unlikely to be a direct relationship: there are likely interactions of environmental drivers that result in higher occurrence of both modeled zooplankton and belugas in the DBO 6 region. The environmental triggers that drive the migratory phenology of the two Arctic endemic cetacean species likely extend from Bering Sea transport of heat, nutrients and plankton through the Chukchi and into the Beaufort Sea.

Lingering Chukchi Sea sea ice and Chukchi Sea mean winds influence population age structure of euphausiids (krill) found in the bowhead whale feeding hotspot near Pt. Barrow, Alaska.

Interannual variability in euphausiid (krill) abundance and population structure and associations of those measures with environmental drivers were investigated in an 11-year study conducted in late August-early September 2005-2015 in offshelf waters (bottom depth > 40 m) in Barrow Canyon and the Beaufort Sea just downstream of Distributed Biological Observatory site 5 (DBO5) near Pt. Barrow, Alaska. Statistically-significant positive correlations were observed among krill population structure (proportion of juveniles and adults), the volume of Late Season Melt Water (LMW), and late-spring Chukchi Sea sea ice extent. High proportions of juvenile and adult krill were seen in years with larger volumes of LMW and greater spring sea ice extents (2006, 2009, 2012-2014) while the converse, high proportions of furcilia, were seen in years with smaller volumes of LMW and lower spring sea ice extent (2005, 2007, 2010, 2011, 2015). These different life stage, sea ice and water mass regimes represent integrated advective responses to mean fall and/or spring Chukchi Sea winds, driven by prevailing atmospheric pressure distributions in the two sets of years. In years with high proportions of juveniles and adults, late-spring and preceding-fall winds were weak and variable while in years with high proportions of furcilia, late-spring and preceding-fall winds were strong, easterly and consistent. The interaction of krill life history with yearly differences in the northward transports of krill and water masses along with sea ice retreat determines the population structure of late-summer krill populations in the DBO5 region near Pt. Barrow. Years with higher proportions of mature krill may provide larger prey to the Pt. Barrow area bowhead whale prey hotspot. The characteristics of prey near Pt. Barrow is dependent on krill abundance and size, large-scale environmental forcing, and interannual variability in recruitment success of krill in the Bering Sea.

Bowhead whales use two foraging strategies in response to fine-scale differences in zooplankton vertical distribution.

As zooplanktivorous predators, bowhead whales (Balaena mysticetus) must routinely locate patches of prey that are energy-rich enough to meet their metabolic needs. However, little is known about how the quality and quantity of prey might influence their feeding behaviours. We addressed this question using a new approach that included: (1) multi-scale biologging and unmanned aerial system observations of bowhead whales in Cumberland Sound, Nunavut (Canada), and (2) an optical plankton counter (OPC) and net collections to identify and enumerate copepod prey species through the water column. The OPC data revealed two prey layers comprised almost exclusively of lipid-rich calanoid copepods. The deep layer contained fewer, but larger, particles (10% greater overall biomass) than the shallow prey layer. Dive data indicated that the whales conducted long deep Square-shaped dives (80% of dives; averaging depth of 260.4 m) and short shallow Square-shaped dives (16%; averaging depth of 22.5 m) to feed. The whales tended to dive proportionally more to the greater biomass of zooplankton that occurred at depth. Combining behavioural recordings with prey sampling showed a more complex feeding ecology than previously understood, and provides a means to evaluate the energetic balance of individuals under current environmental conditions.

Whale tear glands in the bowhead and the beluga whales: Source and function.

Orbital glands are found in many tetrapod vertebrates, and are usually separate structures, consisting of individual glands lying in the eyelids and both canthi of the orbit. In cetaceans, however, the orbital glandular units are less distinct and have been described by numerous authors as a single, periorbital mass. There are few histochemical and immunhistochemical studies to date of these structures. In this study, we examined the orbital glandular region of both the bowhead whale (Balaena mysticetus: Mysticeti) and the beluga whale (Delphinapterus leucas: Odontoceti) using histological, histochemical, and immunohistochemical techniques. Histologically, in the bowhead, three glandular areas were noted (circumorbital, including Harderian and lacrimal poles), palpebral (midway in the lower eyelid), and rim (near the edge of the eyelid). In the beluga, there was only a large, continuous mass within the eyelid itself. Histochemical investigation suggests neither sexual dimorphism nor age-related differences, but both whales had two cell types freely intermingling with each other in all glandular masses. Large cells (cell type 1) were distended by four histochemically distinct intracellular secretory granules. Smaller cells (cell type 2) were not distended (fewer granules) and had two to three histochemically distinct intracellular secretory granules. The beluga orbital glands had additional lipid granules in cell type 1. Counterintuitively, both lipocalin and transferrin were localized to cell type 2 only. This intermingling of cell types is unusual for vertebrates in whom individual orbital glands usually have one cell type with one to two different secretory granules present. The heterogeneity of the orbital fluid produced by cetacean orbital glands implies a complex function, or series of functions, for these orbital glands and their role in producing the tear fluid.