Seasonal hematology and serum chemistry of wild beluga whales (Delphinapterus leucas) in Bristol Bay, Alaska, USA

We collected blood from 18 beluga whales (Delphinapterus leucas), live-captured in Bristol Bay, Alaska, USA, in May and September 2008, to establish baseline hematologic and serum chemistry values and to determine whether there were significant differences in hematologic values by sex, season, size/age, or time during the capture period. Whole blood was collected within an average of 19 min (range=11-30 min) after the net was set for capture, and for eight animals, blood collection was repeated in a later season after between 80-100 min; all blood was processed within 12 hr. Mean hematocrit, chloride, creatinine, total protein, albumin, and alkaline phosphatase were significantly lower in May than they were in September, whereas mean corpuscular hemoglobin concentration, monocytes, phosphorous, magnesium, blood urea nitrogen, alanine aminotransferase, aspartate aminotransferase, γ-glutamyltranspeptidase, and creatinine kinase were significantly higher. Mean total protein, white blood cell count, neutrophils, and lymphocytes were significantly higher early in the capture period than they were later. No significant differences in blood analyte values were noted between males and females. Using overall body length as a proxy for age, larger (older) belugas had lower white blood cell, lymphocyte, and eosinophil counts as well as lower sodium, potassium, and calcium levels but higher creatinine levels than smaller belugas. These data provide values for hematology and serum chemistry for comparisons with other wild belugas.     

KILLER WHALE PREDATION ON BELUGAS IN COOK INLET, ALASKA: IMPLICATIONS FOR A DEPLETED POPULATION

Killer whale predation on belugas in Cook Inlet, Alaska, has become a concern since the decline of these belugas was documented during the 1990s. Accordingly, killer whale sightings were compiled from systematic surveys, observer databases, and anecdotal accounts. Killer whales have been relatively common in lower Cook Inlet (at least 100 sightings from 1975 to 2002), but in the upper Inlet, north of Kalgin Island, sightings were infrequent (18 in 27 yr), especially prior to the 1990s. Beach cast beluga carcasses with teeth marks and missing flesh also provided evidence of killer whale predation. Most observed killer whale/beluga interactions were in the upper Inlet. During 11 of 15 observed interactions, belugas were obviously injured or killed, either through direct attacks or indirectly as a result of stranding. Assuming at least one beluga mortality occurred during the other four encounters, we can account for 21 belugas killed between 1985 and 2002. This would suggest a minimum estimate of roughly 1/yr and does not include at least three instances where beluga calves accompanied an adult that was attacked.     

Genetic variation of the St. Lawrence beluga whale population assessed by DNA fingerprinting

Recent surveys suggest that the endangered St. Lawrence beluga ( Delphinapterus leucas ) population is not recovering significantly despite 20 years of protection. Dead individuals that have been autopsied show high levels of tumours and infections. This situation could be a result of pollution, loss of genetic variation, inbreeding depression or a combination of these factors. Analyses of DNA fingerprints from St. Lawrence belugas with three minisatellite probes (Jeffreys 33.6, 33.15 and M13) indicate a reduced level of genetic variation compared to Beaufort Sea animals. The average band-sharing between individuals of the St. Lawrence beluga population for the three probes (0.534, 0.573 and 0.478, respectively) was significantly higher than that of the Beaufort Sea beluga population (0.343, 0.424, 0.314, respectively). Higher levels of mean allele frequency in the St. Lawrence belugas (0.33 vs. 0.21) suggest that this population is composed of individuals which are related. Inbreeding depression could therefore be a factor in the lack of recovery of the St. Lawrence beluga population.     

Movements of beluga whales (Delphinapterus leucas) in Bristol Bay,Alaska

We describe the annual distribution of beluga whales (Delphinapterus leucas) in Bristol Bay, Alaska, using data from 31 satellite‐linked transmitters during 2002–2011. Bristol Bay has one of the largest and best studied Pacific salmon (Oncorhynchus spp.) fisheries in the world, allowing us to link the seasonal distribution of belugas to that of salmon. During salmon migrations, beluga movements were restricted to river entrances. Belugas generally did not relocate to different river entrances or change bays during peak salmon periods. However, the location of belugas was not related to the number of salmon passing counting towers, suggesting that belugas were either selecting locations that were good for catching salmon or there were simply more salmon than belugas needed to supply their nutritional needs. The distribution of belugas expanded after salmon runs ended, and was greatest in winter when belugas ranged beyond the inner bays, traveling as far west as Cape Constantine. Belugas continued to frequent the inner bays in winter whenever sea ice conditions allowed, e.g., when winds moved sea ice offshore; however, they were never located south of the southern ice edge in open water or outside of Bristol Bay.     

Key Factors Determining the Distribution of Beluga Whales, <Emphasis Type="Italic">Delphinapterus leucas</Emphasis> (Pallas, 1776), in River Estuaries of Western Kamchatka

The results of observations on the distribution of beluga whales, Delphinapterus leucas (Pallas, 1776), in three large rivers of western Kamchatka in the summer and autumn seasons are discussed. In the summer, the number of beluga whales in the Khairyuzova, Belogolovaya, and Moroshechnaya rivers reaches 111–250 individuals. Most of the belugas enter the rivers during the flood tidal phase: the number of animals in the estuaries increases along with the rising water level to the maximum value at spring tide. The belugas do not move upstream out of the estuaries and tend to remain in the zone of mixing riverine and marine waters, where 20 species of fish and three species of invertebrates have been identified. At ebb tide, the belugas leave for the sea; however, during a large run of salmon some individuals remain in the estuaries and continue hunting in deep-water areas. The main issue that causes beluga whales to form summer aggregations in Kamchatkan rivers is the hunt for salmon. The distribution of beluga whales in river estuaries is defined by the dynamics and intensity of salmon spawning runs. The preference of beluga whales for these rivers can be explained by the channel type of their estuaries.     

Decadal shifts in autumn migration timing by Pacific Arctic beluga whales are related to delayed annual sea ice formation

Migrations are often influenced by seasonal environmental gradients that are increasingly being altered by climate change. The consequences of rapid changes in Arctic sea ice have the potential to affect migrations of a number of marine species whose timing is temporally matched to seasonal sea ice cover. This topic has not been investigated for Pacific Arctic beluga whales (Delphinapterus leucas) that follow matrilineally maintained autumn migrations in the waters around Alaska and Russia. For the sympatric Eastern Chukchi Sea (‘Chukchi’) and Eastern Beaufort Sea (‘Beaufort’) beluga populations, we examined changes in autumn migration timing as related to delayed regional sea ice freeze‐up since the 1990s, using two independent data sources (satellite telemetry data and passive acoustics) for both populations. We compared dates of migration between ‘early’ (1993–2002) and ‘late’ (2004–2012) tagging periods. During the late tagging period, Chukchi belugas had significantly delayed migrations (by 2 to >4 weeks, depending on location) from the Beaufort and Chukchi seas. Spatial analyses also revealed that departure from Beaufort Sea foraging regions by Chukchi whales was postponed in the late period. Chukchi beluga autumn migration timing occurred significantly later as regional sea ice freeze‐up timing became later in the Beaufort, Chukchi, and Bering seas. In contrast, Beaufort belugas did not shift migration timing between periods, nor was migration timing related to freeze‐up timing, other than for southward migration at the Bering Strait. Passive acoustic data from 2008 to 2014 provided independent and supplementary support for delayed migration from the Beaufort Sea (4 day yr^?1) by Chukchi belugas. Here, we report the first phenological study examining beluga whale migrations within the context of their rapidly transforming Pacific Arctic ecosystem, suggesting flexible responses that may enable their persistence yet also complicate predictions of how belugas may fare in the future.     

Assessing the abundance of Bristol Bay belugas with genetic mark‐recapture methods

The Bristol Bay stock of beluga whales (Delphinapterus leucas) is genetically distinct and resides in Bristol Bay year‐round. We estimated the abundance of this population using genetic mark‐recapture, whereby genetic markers from skin biopsies, collected between 2002 and 2011, were used to identify individuals. We identified 516 individual belugas in two inner bays, 468 from Kvichak Bay and 48 from Nushagak Bay, and recaptured 75 belugas in separate years. Using a POPAN Jolly‐Seber model, abundance was estimated at 1,928 belugas (95% CI = 1,611–2,337), not including calves, which were not sampled. Most belugas were sampled in Kvichak Bay at a time when belugas are also known to occur in Nushagak Bay. The pattern of genetic recaptures and data from belugas with satellite transmitters suggested that belugas in the two bays regularly mix. Hence, the estimate of abundance likely applies to all belugas within Bristol Bay. Simulations suggested that POPAN estimates of abundance are robust to most forms of emigration, but that emigration causes negative bias in both capture and survival probabilities. Because it is likely that some belugas do not enter the sampling area during sampling, our estimate of abundance is best considered a minimum population size.     

Mating ecology of beluga (Delphinapterus leucas) and narwhal (Monodon monoceros) as estimated by reproductive tract metrics

Narwhal and beluga whales are important species to Arctic ecosystems, including subsistence hunting by Inuit, and little is understood about their mating ecology. Reproductive tract metrics vary across species in relation to mating strategy, and have been used to infer mating ecology. Reproductive tracts from beluga and narwhal were collected between 1997 and 2008 from five beluga stocks and two narwhal stocks across the Canadian Arctic. Tract length for males and females, relative testes mass for males, and tusk length for male narwhal were measured. We assessed variation relative to species, body size, stock, maturity, and season. Significant variation was found in testes mass across month and stock for beluga, and no significant difference between stock or date of harvest for narwhal. Beluga had significantly larger testes relative to body size than narwhal, suggesting they were more promiscuous than narwhal. A significant relationship was found between narwhal tusk length and testes mass, indicating the tusk may be important in female mate choice. No significant differences were found between narwhal and beluga reproductive tract length for males or females. The mating systems suggested for narwhal and belugas by our results mean the two species may respond differently to climate change.     

Bartonella henselae in captive and hunter-harvested beluga (Delphinapterus leucas)

Previously, we reported the isolation of Bartonella henselae from the blood of harbor porpoises (Phocoena phocoena) and loggerhead sea turtles (Caretta caretta) from the North Carolina coast. Hematologic, pathologic, and microbiologic findings surrounding the death of a juvenile captive beluga in Vancouver initiated an outbreak investigation designed to define the molecular prevalence of Bartonella infection in belugas. Using polymerase chain reaction analyses targeting the intergenic spacer region (ITS), two B. henselae ITS strains were identified in 78% of captive and free-ranging hunter-harvested belugas. These findings may have public health implications and may influence aquarium management procedures for captive marine mammals.     

Identification of novel Helicobacter spp. from a beluga whale

The gastric fluid and feces of three belugas from the Mystic Aquarium were assessed for the presence of Helicobacter spp. Gastric fluid and feces from the two clinically healthy belugas were negative for helicobacter, and endoscopy performed on these animals revealed no lesions. However, a helicobacter isolate and PCR product similar to helicobacter strains previously recovered from dolphins were identified, respectively, from the feces and gastric fluid of a beluga manifesting intermittent inappetence and lethargy. Esophageal and forestomach ulcers were noted on endoscopy. This is the first report of novel Helicobacter spp. being identified from whales.     

Beluga (Delphinapterus leucas) habitat selection in the eastern Beaufort Sea in spring, 1975�C1979

An understanding of the adaptability of belugas (Delphinapterus leucas) to changing ice conditions is required to interpret and predict possible changes in habitat selection in response to projected loss of sea ice throughout the circumpolar Arctic. We analyzed beluga observations made during spring aerial surveys for ringed seals conducted from 1975 to 1979 in the eastern Beaufort Sea. Despite inter-annual variability in the extent and distribution of sea ice, belugas consistently selected areas with water depths of 200–500 m and heavy ice concentrations (8/10 to 10/10) while areas of open water to light ice concentrations (0/10 to 1/10) were not selected. Belugas were also found in proximity to regions with ≥0.5 degrees seafloor slope which include the continental slope and other areas with the potential for oceanographic upwellings. In most years (4 of 5), fast-ice edges and coastal areas were not selected. In the lightest ice year analyzed, belugas showed less specificity in habitat selection as their distribution expanded and shifted shoreward to fast-ice edges. The observed distribution is discussed in terms of predator–prey relationships particularly with reference to beluga feeding on polar cod (Boreogadus saida). More research is required to examine and compare possible changes in distribution since the late 1970s and to investigate the factors driving the patterns described.     

An estimate of the fraction of belugas (<Emphasis Type="Italic">Delphinapterus leucas</Emphasis>) in the Canadian high Arctic that winter in West Greenland

Five belugas, or white whales (Delphinapterus leucas), were tracked by satellite from Creswell Bay, Somerset Island, in the Canadian high Arctic towards West Greenland in autumn 2001. After 1 October, three of the whales stayed in the North Water polynya and the other two whales moved to West Greenland. One of the whales that moved to Greenland migrated south along the west coast, following a route and timing similar to another beluga tracked in 1996. The belugas that moved towards West Greenland from Canada did so before or near 1 October. The movements of both these whales followed a similar timing and assumed migratory route of belugas hunted in autumn in West Greenland. In Greenland, the hunt begins in September, where the first whales are taken in the northernmost community of Qaanaaq. Hunting takes place farther south in Upernavik in October, and finally in November and December, belugas are taken even farther south in Uummannaq and Disko Bay. The whales that remain in the North Water after 1 October most likely do not contribute to the harvest in West Greenland. Based on the total number of belugas satellite-tracked in Canada between 1995 and 2001 with tags that lasted beyond 1 October, approximately 0.15 (95% CI 0.06-0.35; n=26) of the summering stock of belugas in the Canadian high Arctic move to West Greenland for the winter. Genetic studies have indicated that belugas moving east through Lancaster Sound are significantly differentiated from belugas taken in the autumn hunt in West Greenland. These conflicting results suggest molecular genetics cannot be solely relied on to reveal the stock identity of these belugas.     

KILLER WHALES, ORCINUS ORCA, IN THE SOUTHEASTERN BERING SEA: RECENT SIGHTINGS andPREDATION ON OTHER MARINE MAMMALS

An unusual number of killer whales appeared in inshore waters of the southeastern Bering Sea in summer 1989 and 1990. Multiple sightings occurred in Bristol and Kuskokwim bays where killer whales had been seen only rarely in previous years. Three animals became stranded on mud flats in Kuskokwim Bay but were able to free themselves on a high tide. Killer whales were observed interacting with salmon, harbor seals, Steller sea lions, walruses, and beluga whales. Detailed observations were made of killer whales attacking belugas in the Naknek River. Local conditions and behavioral adaptations may reduce the susceptibility of belugas to killer whale predation. Continued killer whale activity in this area would be unlikely to affect fish resources, but might have some influence on beluga whales.     

Exchange of “signature” calls in captive belugas (Delphinapterus leucas)

Belugas (Delphinapterus leucas) produce echolocation clicks, burst pulses, and whistles. The sounds of 3 captive belugas were recorded using 2 hydrophones at the Port of Nagoya Public Aquarium. There were stable individual differences in the pulse patterning of one type of pulsed sounds (PS1 call), suggesting that belugas use these as “signature” calls. Eighty-eight percent of PS1 calls initiated PS1 calls from other animals within 1 s. PS1 calls repeated by the same individual occurred primarily when other belugas did not respond within 1 s of the first call. Belugas delayed successive PS1 calls when other belugas responded with a PS1 call within 1 s. There was no clear temporal pattern for whistles. It appears that the time limit for responding to calls is 1 s after the initial call. If other individuals do not respond to the PS1 call of a beluga within 1 s, belugas tend to repeat the call and wait for a response. The results of this study suggest that the belugas exchange their individual signatures by using PS1 calls, in a manner similar to that of signature whistles used by bottlenose dolphins.     

Identification of Novel Helicobacter spp. from a Beluga Whale

The gastric fluid and feces of three belugas from the Mystic Aquarium were assessed for the presence of Helicobacter spp. Gastric fluid and feces from the two clinically healthy belugas were negative for helicobacter, and endoscopy performed on these animals revealed no lesions. However, a helicobacter isolate and PCR product similar to helicobacter strains previously recovered from dolphins were identified, respectively, from the feces and gastric fluid of a beluga manifesting intermittent inappetence and lethargy. Esophageal and forestomach ulcers were noted on endoscopy. This is the first report of novel Helicobacter spp. being identified from whales.     

Patterns of mortality in endangered Cook Inlet beluga whales: Insights from pairing a long-term photo-identification study with stranding records

Mortality is a demographic metric crucial for understanding the dynamics of endangered populations such as Cook Inlet beluga whales (CIBWs, Delphinapterus leucas), but patterns of mortality are currently not well understood for CIBWs, making decisions about recovery actions challenging. We combined long-term photo-ID data from approximately 420 individual belugas identified during the period 2005–2017 with stranding data from 95 dead belugas to identify patterns of mortality with respect to age, sex, geographic range, cause of death, and to estimate minimum mortality rates. Reported mortality was greatest for adults of reproductive age, followed by calves, with fewer subadults and no adults older than 49 years in the stranding data set despite lifespans of 70+ years reported in other beluga populations. Dead females and males were evenly represented. Live stranding was the predominant assigned cause of death but represented only ~33% of deaths of known cause. Causal factors for the majority of deaths and live strandings are unknown. Annual mortality estimated from reported carcasses relative to total population size averaged 2.2%. Our analysis advances our current understanding of mortality patterns in CIBWs but linking a greater proportion of carcasses to photo-ID individuals would further improve our understanding; we conclude with recommendations for achieving this.     

AIRCRAFT SOUND AND DISTURBANCE TO BOWHEAD AND BELUGA WHALES DURING SPRING MIGRATION IN THE ALASKAN BEAUFORT SEA

Short‐term behavioral responses of bowhead whales (Balaena mysticetus) and beluga whales (Delphinapterus leucas) to a Bell 212 helicopter and Twin Otter fixed‐wing aircraft were observed opportunistically during four spring seasons (1989–1991 and 1994). Behaviors classified as reactions consisted of short surfacings, immediate dives or turns, changes in behavior state, vigorous swimming, and breaching. The helicopter elicited fewer detectable responses by bowheads (14% of 63 groups) than by belugas (38% of 40). Most observed reactions by bowheads (63%) and belugas (86%) occurred when the helicopter was at altitudes ≤150 m and lateral distances ≤250 m. Belugas reacted significantly more frequently during overflights at lateral distances ≤250 m than at longer lateral distances (P= 0.004). When the helicopter was on the ice with engines running, 7 of 14 groups of belugas reacted, up to 320 m away, sometimes with small‐scale (≤100 m) diversion; only 1 of 8 groups of bowheads reacted. For the fixed‐wing aircraft, few bowheads (2.2%) or belugas (3.2%) were observed to react to overflights at altitudes 60–460 m. Most observed reactions by bowheads (73%) and belugas (70%) occurred when the fixed‐wing aircraft was at altitudes ≤182 m and lateral distances ≤250 m. However, the proportions reacting, especially to low‐altitude flights (e. g., ≤182 m), were underestimated for both species because observation opportunities were brief. Even so, reactions were more common when the aircraft was low (≤182 m): P= 0.009 for belugas, P= 0.06 for bowheads. There was little if any reaction by bowheads when the aircraft circled at altitude 460 m and radius 1 km. Aircraft sounds measured underwater at depths 3 m and 18 m showed that a Bell 212 helicopter was 7–17.5 dB noisier than a Twin Otter (10–500 Hz band). Bell 212 sound consisted mainly of main rotor tones ahead of the helicopter and tail rotor tones behind it. Twin Otter sound contained fewer prominent tones. Peak sound level as received underwater was inversely related to aircraft altitude, and received levels at 3 m depth averaged 2.5 dB higher than at 18 m depth. The dominant low‐frequency components of aircraft sound are presumed to be readily audible to bowheads. For belugas, these components may be inaudible, or at most only weakly audible. Mid‐frequency sound components, visual cues, or both, are probably important in eliciting beluga reactions to aircraft.     

Blow Collection as a Non-Invasive Method for Measuring Cortisol in the Beluga (Delphinapterus leucas)

Non-invasive sampling techniques are increasingly being used to monitor glucocorticoids, such as cortisol, as indicators of stressor load and fitness in zoo and wildlife conservation, research and medicine. For cetaceans, exhaled breath condensate (blow) provides a unique sampling matrix for such purposes. The purpose of this work was to develop an appropriate collection methodology and validate the use of a commercially available EIA for measuring cortisol in blow samples collected from belugas (Delphinapterus leucas). Nitex membrane stretched over a petri dish provided the optimal method for collecting blow. A commercially available cortisol EIA for measuring human cortisol (detection limit 35 pg ml⁻¹) was adapted and validated for beluga cortisol using tests of parallelism, accuracy and recovery. Blow samples were collected from aquarium belugas during monthly health checks and during out of water examination, as well as from wild belugas. Two aquarium belugas showed increased blow cortisol between baseline samples and 30 minutes out of water (Baseline, 0.21 and 0.04 µg dl⁻¹; 30 minutes, 0.95 and 0.14 µg dl⁻¹). Six wild belugas also showed increases in blow cortisol between pre and post 1.5 hour examination (Pre 0.03, 0.23, 0.13, 0.19, 0.13, 0.04 µg dl⁻¹, Post 0.60, 0.31, 0.36, 0.24, 0.14, 0.16 µg dl⁻¹). Though this methodology needs further investigation, this study suggests that blow sampling is a good candidate for non-invasive monitoring of cortisol in belugas. It can be collected from both wild and aquarium animals efficiently for the purposes of health monitoring and research, and may ultimately be useful in obtaining data on wild populations, including endangered species, which are difficult to handle directly.     

Ecosystem regime shifts have not affected growth and survivorship of eastern Beaufort Sea belugas

Large-scale ocean-atmosphere physical dynamics can have profound impacts on the structure and organization of marine ecosystems. These changes have been termed “regime shifts”, and five different episodes have been detected in the North Pacific Ocean, with concurrent changes also occurring in the Bering and Beaufort Seas. Belugas from the Eastern Beaufort Sea (EBS) use the Bering Sea during winter and the Beaufort Sea during summer, yet the potential effects of regime shifts on belugas have not been assessed. We investigated whether body size and survivorship of EBS belugas harvested in the Mackenzie River delta region between 1993 and 2003 have been affected by previous purported regime shifts in the North Pacific. Residuals from the relationship between body length and age were calculated and compared among belugas born between 1932 and 1989. Residual body size was not significantly related to birth year for any regime, nor to the age group individuals belonged to during any regime. The percentage deviation in number of belugas born in any given year that survived to be included in the hunt (survivorship) did not show any significant trend within or between regimes. Accounting for lags of 1–5 years did not reveal any evidence of delayed effects. Furthermore, neither population index was significantly related to changes in major climatic variables that precede regime shifts. Our results suggest that EBS beluga body size and survivorship have not been affected by the major regime shifts of the North Pacific and the adjacent Bering and Beaufort Seas. EBS belugas may have been able to modify their diet without compromising their growth and survivorship. Diet and reproductive analyses over large and small time scales can help understand the mechanisms enabling belugas to avoid significant growth and reproductive effects of past regime shifts. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Contact call diversity in natural beluga entrapments in an Arctic estuary: Preliminary evidence of vocal signatures in wild belugas

Broadband, pulsed contact calls have been described for captive and temporarily restrained belugas, but little information exists on their usage in the wild. We examined vocal production during 14 natural beluga entrapments in a shallow channel in Cunningham Inlet, as isolation events offer ideal contexts to study contact calls. Drone footage, overhead photos, and shore‐based photos confirmed the number of individuals and age composition in each entrapment. Contact calls comprised the majority (61%) of vocalizations produced by entrapped whales compared to the free‐ranging herd (10%). We divided contact calls into complex (80%), those with a stereotyped, spectrographically prominent component overlapping the pulse train that characterizes all beluga contact calls, and simple (20%), those with no overlapping component. For each entrapment, we generated a catalogue of complex contact call types, totaling 87 types. Our classification was corroborated both quantitatively and by 55 naïve human judges. Occasional instances of overlapping contact calls of the same type indicated dyadic production. The number of contact call types per entrapment was strongly related to (never exceeding) the number of individuals, excluding neonates. Although this suggests a system of vocal signatures in belugas, consistent with their fission‐fusion society and earlier findings, whether signature identity is encoded individually or shared with related animals remains unknown.