Anthropogenic and Climatic Drivers of Long-Term Changes of Mercury and Feeding Ecology in Arctic Beluga (Delphinapterus leucas) Populations.

We assessed long-term changes in the feeding ecology and mercury (Hg) accumulation in Eastern High Arctic-Baffin Bay beluga (Delphinapterus leucas) using total Hg and stable isotope (δ13C, δ15N) assays in teeth samples from historical (1854-1905) and modern (1985-2000) populations. Mean δ13C values in teeth declined significantly over time, from -13.01 ± 0.55‰ historically to -14.41 ± 0.28‰ in 2000, while no consistent pattern was evident for δ15N due to high individual variability within each period. The temporal shift in isotopic niche is consistent with beluga feeding ecology changing in recent decades to a more pelagic and less isotopically diverse diet or an ecosystem wide change in isotope profiles. Mercury concentrations in modern beluga teeth were 3-5 times higher on average than those in historical beluga. These results are similar to the long-term trends of Hg and feeding ecology reported in other beluga populations and in other Arctic marine predators. Similar feeding ecology shifts across regions and species indicate a consistent increased pelagic diet response to climate change as the Arctic Ocean progressively warmed and lost sea ice. Previously, significant temporal Hg increase in beluga and other Arctic animals was attributed solely to direct inputs of anthropogenic Hg from long-range sources. Recent advances in understanding the Arctic marine Hg cycle suggest an additional, complementary possibility─increased inputs of terrestrial Hg of mixed anthropogenic-natural origin, mobilized from permafrost and other Arctic soils by climate warming. At present, it is not possible to assign relative importance to the two processes in explaining the rise of Hg concentrations in modern Arctic marine predators.

Adaptation in the auditory system of a beluga whale: effect of adapting sound parameters.

The effects of adapting sounds (pip trains or pure tones) on auditory evoked potentials (the rate following response, RFR) were investigated in a beluga whale. During RFR acquisition, adapting signals lasting 128 ms each were alternated with test signals lasting 16 ms each; the test signal levels varied randomly. Adapting signals were trains of cosine-enveloped tone pips or pure tones. Pip rate varied with the envelope cosine cycle maintained at 0.125 of pip intervals and the cosine rise-fall time maintained at 0.0625 of pip intervals. Adapting signals shifted the amplitude-level function upward compared to the baseline (no adapting signal) function. The higher the adapting signal level was, the bigger the shift in the amplitude-level function was. The slower the pips were in the adapting signal, the smaller the adaptation effect was. A train of pips with a 0.0625-ms rise-fall time and 125 dB SPL shifted the function by 35-40 dB, whereas a train of pips with a 1-ms rise-fall time or a pure tone with the same SPL shifted the function by approximately 15 dB. The difference between the "fast" and "slow" adapting signals is supposed to be associated with their abilities to stimulate the auditory system in odontocetes.

Body condition impacts blood and muscle oxygen storage capacity of free-living beluga whales (Delphinapterus leucas).

Arctic marine ecosystems are currently undergoing rapid environmental changes. Over the past 20 years, individual growth rates of beluga whales (Delphinapterus leucas) have declined, which may be a response to climate change; however, the scarcity of physiological data makes it difficult to gauge the adaptive capacity and resilience of the species. We explored relationships between body condition and physiological parameters pertaining to oxygen (O2) storage capacity in 77 beluga whales in the eastern Beaufort Sea. Muscle myoglobin concentrations averaged 77.9 mg g-1, one of the highest values reported among mammals. Importantly, blood haematocrit, haemoglobin and muscle myoglobin concentrations correlated positively to indices of body condition, including maximum half-girth to length ratios. Thus, a whale with the lowest body condition index would have ∼27% lower blood (26.0 versus 35.7 ml kg-1) and 12% lower muscle (15.6 versus 17.7 ml kg-1) O2 stores than a whale of equivalent mass with the highest body condition index; with the conservative assumption that underwater O2 consumption rates are unaffected by body condition, this equates to a >3 min difference in maximal aerobic dive time between the two extremes (14.3 versus 17.4 min). Consequently, environmental changes that negatively impact body condition may hinder the ability of whales to reach preferred prey sources, evade predators and escape ice entrapments. The relationship between body condition and O2 storage capacity may represent a vicious cycle, in which environmental changes resulting in decreased body condition impair foraging, leading to further reductions in condition through diminished prey acquisition and/or increased foraging efforts.

Position of an acoustic window in a beluga whale: Computation based on auditory evoked potential latencies.

In a beluga whale, the positions of sound receiving areas on the head surface were determined by comparing the acoustic delays from different sound source positions. For this investigation, auditory evoked potentials (AEPs) in response to short tone pips were recorded. Latencies of the first AEP wave that presumably reflected the activity of the auditory nerve were measured at different sound source azimuths. For AEPs of equal amplitudes, the difference in AEP latencies was attributed to the difference in the acoustic delays. These delay differences were used to compute the azimuths of sound receiving points. Measurements were conducted at frequencies from 22.5 to 90 kHz in half-octave steps. At all stimulus frequencies, the receiving points were located 24-38 cm caudal of the melon tip, which is near a proximal part of the lower jaw. Thus, the results indicated the latero-mandibular acoustic window. Possible causes for not finding a lateral or ventro-mandibular window are discussed.

Preliminary observations of an unusual mouth interaction between beluga calves (Delphinapterus leucas).

Although many animals, including odontocetes, exhibit interactions involving mouths (e.g., mouthing, nuzzling, biting), a limited number of animals display mouth-to-mouth social interactions that involve mutual coordination and collaboration. The purpose of this paper is to describe briefly a spontaneous and unexpected mouth-to-mouth social interaction between beluga calves in human care during their first year of life. Forty-seven independent events were identified after event sampling from more than 345 hr of observations of four mother-calf pairs and their companions. Unique aspects of this behavior included early emergence presumably without the benefit of a model and a preference for similar aged partners. Adult belugas did not display this social interaction. Based on its early emergence, the presence of similar-aged partner preferences, and affiliative cooperative contexts, this unusual mouth-to-mouth social interaction may play a significant role in beluga social and physical development. To evaluate this possibility, additional research is needed in which the complete topography, possible functions, and potential outcomes associated with this rare but conspicuous behavior exhibited by beluga calves are assessed.

Variation in hearing within a wild population of beluga whales (Delphinapterus leucas).

Documenting hearing abilities is vital to understanding a species' acoustic ecology and for predicting the impacts of increasing anthropogenic noise. Cetaceans use sound for essential biological functions such as foraging, navigation and communication; hearing is considered to be their primary sensory modality. Yet, we know little regarding the hearing of most, if not all, cetacean populations, which limits our understanding of their sensory ecology, population level variability and the potential impacts of increasing anthropogenic noise. We obtained audiograms (5.6-150 kHz) of 26 wild beluga whales to measure hearing thresholds during capture-release events in Bristol Bay, AK, USA, using auditory evoked potential methods. The goal was to establish the baseline population audiogram, incidences of hearing loss and general variability in wild beluga whales. In general, belugas showed sensitive hearing with low thresholds (<80 dB) from 16 to 100 kHz, and most individuals (76%) responded to at least 120 kHz. Despite belugas often showing sensitive hearing, thresholds were usually above or approached the low ambient noise levels measured in the area, suggesting that a quiet environment may be associated with hearing sensitivity and that hearing thresholds in the most sensitive animals may have been masked. Although this is just one wild population, the success of the method suggests that it should be applied to other populations and species to better assess potential differences. Bristol Bay beluga audiograms showed substantial (30-70 dB) variation among individuals; this variation increased at higher frequencies. Differences among individual belugas reflect that testing multiple individuals of a population is necessary to best describe maximum sensitivity and population variance. The results of this study quadruple the number of individual beluga whales for which audiograms have been conducted and provide the first auditory data for a population of healthy wild odontocetes.

Influence of background noise on auditory evoked responses to rippled-spectrum signals.

The resolution of spectral patterns in adaptation background noise was investigated in a beluga whale, Delphinapterus leucas, using the evoked-potential technique. The resolution of spectral patterns was investigated using rippled-spectrum test stimuli of various levels and ripple densities and recording the rhythmic evoked responses (the rate following response, RFR) to ripple phase reversals. In baseline (no adaptation background noise) experiments, the highest RFR magnitude was observed at signal sound pressure levels (SPLs) of 100-110 dB re 1 µPa; at SPLs both below the optimum (down to 80 dB re 1 µPa) and above the optimum (up to 140 dB re 1 µPa), the RFR magnitude decreased. For high signal levels (above 110 dB re 1 µPa), low-level adaptation background noise (from -10 to -20 dB re signal level) increased RFR magnitude compared to baseline. This effect is considered to be a result of the optimization of the sensation level of the high-SPL signals due to decreasing hearing sensitivity caused by the adaptation background noise.

Influence of the Background Noise on Recognition of Signals with a Complex Spectrum Structure in the Beluga Whale (Delphinapterus leucas).

The frequency resolving power of hearing (FRP) of the beluga whale Delphinapterus leucas was studied as dependent on influence of lasting low-intensity sounds (of the ultrasonic range from -20 to +10 dB). Testing of the spectrum ripple-phase reversal was used in conjunction with a noninvasive recording of auditory evoked potentials. FRP parameters were found to depend nonmonotonically on the intensity of the background noise. The resultant adaptation effects can be explained by the fact that, in response to the high-intensity signals, the auditory system sensitivity is reduced to the level optimal for analysis of these signals.

Influence of fatiguing noise on auditory evoked responses to stimuli of various levels in a beluga whale, Delphinapterus leucas.

The negative impact of man-made noise on the hearing of odontocetes has attracted considerable recent attention. In the majority of studies, permanent or temporary reductions in sensitivity, known as permanent or temporary threshold shift (PTS or TTS, respectively), have been investigated. In the present study, the effects of a fatiguing sound on the hearing of a beluga whale, Delphinapterus leucas, within a wide range of levels of test signals was investigated. The fatiguing noise was half-octave band-limited noise centered at 32 kHz. Post-exposure effects of this noise on the evoked responses to test stimuli (rhythmic pip trains with a 45-kHz center frequency) at various levels (from threshold to 60 dB above threshold) were measured. For baseline (pre-exposure) responses, the magnitude-versus-level function featured a segment of steep magnitude dependence on level (up to 30 dB above threshold) that was followed by a plateau segment that featured little dependence on level (30 to 55 dB above threshold). Post-exposure, the function shifted upward along the level scale. The shift was 23 dB at the threshold and up to 33 dB at the supra-threshold level. Owing to the plateau in the magnitude-versus-level function, post-exposure suppression of responses depended on the stimulus level such that higher levels corresponded to less suppression. The experimental data may be modeled based on the compressive non-linearity of the cochlea. According to the model, post-exposure responses of the cochlea to high-level stimuli are minimally suppressed compared with the pre-exposure responses, despite a substantially increased threshold.

A beluga whale socialized with bottlenose dolphins imitates their whistles.

The research on imitation in the animal kingdom has more than a century-long history. A specific kind of imitation, auditory-vocal imitation, is well known in birds, especially among songbirds and parrots, but data for mammals are limited to elephants, marine mammals, and humans. Cetaceans are reported to imitate various signals, including species-specific calls, artificial sounds, and even vocalizations from other species if they share the same habitat. Here we describe the changes in the vocal repertoire of a beluga whale that was housed with a group of bottlenose dolphins. Two months after the beluga's introduction into a new facility, we found that it began to imitate whistles of the dolphins, whereas one type of its own calls seemed to disappear. The case reported here may be considered as an interesting phenomenon of vocal accommodation to new social companions and cross-species socialization in cetaceans.

Temporal shifts in intraguild predation pressure between beluga whales and Greenland halibut in a changing Arctic.

Asymmetrical intraguild predation (AIGP), which combines both predation and competition between predator species, is pervasive in nature with relative strengths varying by prey availability. But with species redistributions associated with climate change, the response by endemic predators within an AIGP context to changing biotic-abiotic conditions over time (i.e. seasonal and decadal) has yet to be quantified. Furthermore, little is known on AIGP dynamics in ecosystems undergoing rapid directional change such as the Arctic. Here, we investigate the flexibility of AIGP among two predators in the same trophic guild: beluga (Delphinapterus leucas) and Greenland halibut (Reinhardtius hippoglossoides), by season and over 30 years in Cumberland Sound-a system where forage fish capelin (Mallotus villosus) have recently become more available. Using stable isotopes, we illustrate different predator responses to temporal shifts in forage fish availability. On a seasonal cycle, beluga consumed less Greenland halibut and increased consumption of forage fish during summer, contrasting a constant consumption rate of forage fish by Greenland halibut year-round leading to decreased AIGP pressure between predators. Over a decadal scale (1982-2012), annual consumption of forage fish by beluga increased with a concomitant decline in the consumption of Greenland halibut, thereby indicating decreased AIGP pressure between predators in concordance with increased forage fish availability. The long-term changes of AIGP pressure between endemic predators illustrated here highlights climate-driven environmental alterations to interspecific intraguild interactions in the Arctic.

A comparison of blood nitric oxide metabolites and hemoglobin functional properties among diving mammals.

The ability of marine mammals to hunt prey at depth is known to rely on enhanced oxygen stores and on selective distribution of blood flow, but the molecular mechanisms regulating blood flow and oxygen transport remain unresolved. To investigate the molecular mechanisms that may be important in regulating blood flow, we measured concentration of nitrite and S-nitrosothiols (SNO), two metabolites of the vasodilator nitric oxide (NO), in the blood of 5 species of marine mammals differing in their dive duration: bottlenose dolphin, South American sea lion, harbor seal, walrus and beluga whale. We also examined oxygen affinity, sensitivity to 2,3-diphosphoglycerate (DPG) and nitrite reductase activity of the hemoglobin (Hb) to search for possible adaptive variations in these functional properties. We found levels of plasma and red blood cells nitrite similar to those reported for terrestrial mammals, but unusually high concentrations of red blood cell SNO in bottlenose dolphin, walrus and beluga whale, suggesting enhanced SNO-dependent signaling in these species. Purified Hbs showed similar functional properties in terms of oxygen affinity and sensitivity to DPG, indicating that reported large variations in blood oxygen affinity among diving mammals likely derive from phenotypic variations in red blood cell DPG levels. The nitrite reductase activities of the Hbs were overall slightly higher than that of human Hb, with the Hb of beluga whale, capable of longest dives, having the highest activity. Taken together, these results underscore adaptive variations in circulatory NO metabolism in diving mammals but not in the oxygenation properties of the Hb.

Learning and extinction of conditioned hearing sensation change in the beluga whale (Delphinapterus leucas).

Ice-dwelling beluga whales are increasingly being exposed to anthropogenic loud sounds. Beluga's hearing sensitivity measured during a warning sound just preceding a loud sound was tested using pip-train stimuli and auditory evoked potential recording. When the test/warning stimulus with a frequency of 32 or 45 kHz preceded the loud sound with a frequency of 32 kHz and a sound pressure level of 153 dB re 1 µPa, 2 s, hearing thresholds before the loud sound increased relative to the baseline. The threshold increased up to 15 dB for the test frequency of 45 kHz and up to 13 dB for the test frequency of 32 kHz. These threshold increases were observed during two sessions of 36 trials each. Extinction tests revealed no change during three experimental sessions followed by a jump-like return to baseline thresholds. The low exposure level producing the hearing-dampening effect (156 dB re 1 µPa(2)s in each trial), and the manner of extinction, may be considered as evidence that the observed hearing threshold increases were a demonstration of conditioned dampening of hearing when the whale anticipated the quick appearance of a loud sound in the same way demonstrated in the false killer whale and bottlenose dolphin.

Temporary Threshold Shifts in Naïve and Experienced Belugas: Can Dampening of the Effects of Fatiguing Sounds Be Learned?

In belugas (Delphinapterus leucas), substantial (10-15 dB) differences in temporary threshold shifts (TTSs) were observed between the first and subsequent experimental sessions in the same subjects. In the first session (naïve subject state), the TTSs produced by exposure to fatiguing noises were larger than the TTSs produced in subsequent sessions (experienced subject state). After one to two sessions, the TTSs stabilized. The baseline hearing thresholds did not differ between the naïve and experienced states. One possible explanation for this effect is that the animals learned to dampen their hearing during exposure to fatiguing noises and thus mitigate the impact of those noises.

Is Sound Exposure Level a Convenient Metric to Characterize Fatiguing Sounds? A Study in Beluga Whales.

Both the level and duration of fatiguing sounds influence temporary threshold shifts (TTSs) in odontocetes. These two parameters were combined into a sound exposure level (SEL). In the beluga whale Delphinapterus leucas, TTSs were investigated at various sound pressure level (SPL)-to-duration ratios at a specific SEL. At low SPL-to-duration ratios, the dependence was positive: shorter high-level sounds produced greater TTSs than long low-level sounds of the same SEL. At high SPL-to-duration ratios, the dependence was negative: long low-level sounds produced greater TTSs than short high-level sounds of the same SEL. Thus, the validity of SEL as a metric for fatiguing sound efficiency is limited.

Frequency Tuning of Hearing in the Beluga Whale.

Data on frequency tuning in odontocetes are contradictory: different authors have reported filter qualities from 2 to almost 50. In this study, frequency tuning was measured in a beluga whale (Delphinapterus leucas) using a rippled-noise test stimulus in conjunction with the auditory evoked potential (AEP) technique. The response to ripple reversions was considered to indicate resolvability of the ripple pattern. The limit of ripple-pattern resolution ranged from 20 to 32 ripples per octave (rpo). A model of interaction of the ripple spectrum with frequency-tuned filters suggests that this resolution limit requires a filter quality of 29-46.

Measuring Hearing in Wild Beluga Whales.

We measured the hearing abilities of seven wild beluga whales (Delphinapterus leucas) during a collection-and-release experiment in Bristol Bay, AK. Here we summarize the methods and initial data from one animal and discuss the implications of this experiment. Audiograms were collected from 4 to 150 kHz. The animal with the lowest threshold heard best at 80 kHz and demonstrated overall good hearing from 22 to 110 kHz. The robustness of the methodology and data suggest that the auditory evoked potential audiograms can be incorporated into future collection-and-release health assessments. Such methods may provide high-quality results for multiple animals, facilitating population-level audiograms and hearing measures in new species.

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.

Cardiorespiratory Responses to Acoustic Noise in Belugas.

To date, most research on the adverse effects of anthropogenic noise on marine mammals has focused on auditory and behavioral responses. Other responses have received little attention and are often ignored. In this study, the effect of acoustic noise on heart rate was examined in captive belugas. The data suggest that (1) heart rate can be used as a measure of physiological response (including stress) to noise in belugas and other cetaceans, (2) cardiac response is influenced by parameters of noise and adaptation to repeated exposure, and (3) cetacean calves are more vulnerable to the adverse effect of noise than adults.

Auditory sensitivity to local stimulation of the head surface in a beluga whale (Delphinapterus leucas).

Using the auditory evoked response technique, sensitivity to local acoustic stimulation of the ventro-lateral head surface was investigated in a beluga whale (Delphinapterus leucas). The stimuli were tone pip trains of carrier frequencies ranging from 16 to 128 kHz with a pip rate of 1 kHz. For higher frequencies (90-128 kHz), the low-threshold point was located next to the medial side of the middle portion of the lower jaw. For middle (32-64 kHz) and lower (16-22.5 kHz) frequencies, the low-threshold point was located at the lateral side of the middle portion of the lower jaw. For lower frequencies, there was an additional low-threshold point next to the bulla-meatus complex. Based on these data, several frequency-specific paths of sound conduction to the auditory bulla are suggested: (i) through an area on the lateral surface of the lower jaw and further through the intra-jaw fat-body channel (for a wide frequency range); (ii) through an area on the ventro-lateral head surface and further through the medial opening of the lower jaw and intra-jaw fat-body channel (for a high-frequency range); and (iii) through an area on the lateral (near meatus) head surface and further through the lateral fat-body channel (for a low-frequency range).