Variation in blubber cortisol levels in a recovering humpback whale population inhabiting a rapidly changing environment.

Glucocorticoids are regularly used as biomarkers of relative health for individuals and populations. Around the Western Antarctic Peninsula (WAP), baleen whales have and continue to experience threats, including commercial harvest, prey limitations and habitat change driven by rapid warming, and increased human presence via ecotourism. Here, we measured demographic variation and differences across the foraging season in blubber cortisol levels of humpback whales (Megaptera novaeangliae) over two years around the WAP. Cortisol concentrations were determined from 305 biopsy samples of unique individuals. We found no significant difference in the cortisol concentration between male and female whales. However, we observed significant differences across demographic groups of females and a significant decrease in the population across the feeding season. We also assessed whether COVID-19-related reductions in tourism in 2021 along the WAP correlated with lower cortisol levels across the population. The decline in vessel presence in 2021 was associated with a significant decrease in humpback whale blubber cortisol concentrations at the population level. Our findings provide critical contextual data on how these hormones vary naturally in a population over time, show direct associations between cortisol levels and human presence, and will enable comparisons among species experiencing different levels of human disturbance.

Field measurements reveal exposure risk to microplastic ingestion by filter-feeding megafauna.

Microparticles, such as microplastics and microfibers, are ubiquitous in marine food webs. Filter-feeding megafauna may be at extreme risk of exposure to microplastics, but neither the amount nor pathway of microplastic ingestion are well understood. Here, we combine depth-integrated microplastic data from the California Current Ecosystem with high-resolution foraging measurements from 191 tag deployments on blue, fin, and humpback whales to quantify plastic ingestion rates and routes of exposure. We find that baleen whales predominantly feed at depths of 50-250 m, coinciding with the highest measured microplastic concentrations in the pelagic ecosystem. Nearly all (99%) microplastic ingestion is predicted to occur via trophic transfer. We predict that fish-feeding whales are less exposed to microplastic ingestion than krill-feeding whales. Per day, a krill-obligate blue whale may ingest 10 million pieces of microplastic, while a fish-feeding humpback whale likely ingests 200,000 pieces of microplastic. For species struggling to recover from historical whaling alongside other anthropogenic pressures, our findings suggest that the cumulative impacts of multiple stressors require further attention.

Acoustic signalling and behaviour of Antarctic minke whales (Balaenoptera bonaerensis).

Acoustic signalling is the predominant form of communication among cetaceans. Understanding the behavioural state of calling individuals can provide insights into the specific function of sound production; in turn, this information can aid the evaluation of passive monitoring datasets to estimate species presence, density, and behaviour. Antarctic minke whales are the most numerous baleen whale species in the Southern Ocean. However, our knowledge of their vocal behaviour is limited. Using, to our knowledge, the first animal-borne audio-video documentation of underwater behaviour in this species, we characterize Antarctic minke whale sound production and evaluate the association between acoustic behaviour, foraging behaviour, diel patterns and the presence of close conspecifics. In addition to the previously described downsweep call, we find evidence of three novel calls not previously described in their vocal repertoire. Overall, these signals displayed peak frequencies between 90 and 175 Hz and ranged from 0.2 to 0.8 s on average (90% duration). Additionally, each of the four call types was associated with measured behavioural and environmental parameters. Our results represent a significant advancement in understanding of the life history of this species and improve our capacity to acoustically monitor minke whales in a rapidly changing Antarctic region.

Integrating remote sensing methods during controlled exposure experiments to quantify group responses of dolphins to navy sonar.

Human noise can be harmful to sound-centric marine mammals. Significant research has focused on characterizing behavioral responses of protected cetacean species to navy mid-frequency active sonar (MFAS). Controlled exposure experiments (CEE) using animal-borne tags have proved valuable, but smaller dolphins are not amenable to tagging and groups of interacting individuals are more relevant behavioral units for these social species. To fill key data gaps on group responses of social delphinids that are exposed to navy MFAS in large numbers, we describe novel approaches for the coordinated collection and integrated analysis of multiple remotely-sensed datasets during CEEs. This involves real-time coordination of a sonar source, shore-based group tracking, aerial photogrammetry to measure fine-scale movements and passive acoustics to quantify vocal activity. Using an example CEE involving long-beaked common dolphins (Delphinus delphis bairdii), we demonstrate how resultant quantitative metrics can be used to estimate behavioral changes and noise exposure-response relationships.

The Southern Ocean Exchange: porous boundaries between humpback whale breeding populations in southern polar waters.

Humpback whales (Megaptera novaeangliae) are a cosmopolitan species and perform long annual migrations between low-latitude breeding areas and high-latitude feeding areas. Their breeding populations appear to be spatially and genetically segregated due to long-term, maternally inherited fidelity to natal breeding areas. In the Southern Hemisphere, some humpback whale breeding populations mix in Southern Ocean waters in summer, but very little movement between Pacific and Atlantic waters has been identified to date, suggesting these waters constituted an oceanic boundary between genetically distinct populations. Here, we present new evidence of summer co-occurrence in the West Antarctic Peninsula feeding area of two recovering humpback whale breeding populations from the Atlantic (Brazil) and Pacific (Central and South America). As humpback whale populations recover, observations like this point to the need to revise our perceptions of boundaries between stocks, particularly on high latitude feeding grounds. We suggest that this "Southern Ocean Exchange" may become more frequent as populations recover from commercial whaling and climate change modifies environmental dynamics and humpback whale prey availability.

Lunge filter feeding biomechanics constrain rorqual foraging ecology across scale.

Fundamental scaling relationships influence the physiology of vital rates, which in turn shape the ecology and evolution of organisms. For diving mammals, benefits conferred by large body size include reduced transport costs and enhanced breath-holding capacity, thereby increasing overall foraging efficiency. Rorqual whales feed by engulfing a large mass of prey-laden water at high speed and filtering it through baleen plates. However, as engulfment capacity increases with body length (engulfment volume∝body length3.57), the surface area of the baleen filter does not increase proportionally (baleen area∝body length1.82), and thus the filtration time of larger rorquals predictably increases as the baleen surface area must filter a disproportionally large amount of water. We predicted that filtration time should scale with body length to the power of 1.75 (filter time∝body length1.75). We tested this hypothesis on four rorqual species using multi-sensor tags with corresponding unoccupied aircraft systems-based body length estimates. We found that filter time scales with body length to the power of 1.79 (95% CI: 1.61-1.97). This result highlights a scale-dependent trade-off between engulfment capacity and baleen area that creates a biomechanical constraint to foraging through increased filtration time. Consequently, larger whales must target high-density prey patches commensurate to the gulp size to meet their increased energetic demands. If these optimal patches are absent, larger rorquals may experience reduced foraging efficiency compared with smaller whales if they do not match their engulfment capacity to the size of targeted prey aggregations.

A comparison of baleen whale density estimates derived from overlapping satellite imagery and a shipborne survey.

As whales recover from commercial exploitation, they are increasing in abundance in habitats that they have been absent from for decades. However, studying the recovery and habitat use patterns of whales, particularly in remote and inaccessible regions, frequently poses logistical and economic challenges. Here we trial a new approach for measuring whale density in a remote area, using Very-High-Resolution WorldView-3 satellite imagery. This approach has capacity to provide sightings data to complement and assist traditional sightings surveys. We compare at-sea whale density estimates to estimates derived from satellite imagery collected at a similar time, and use suction-cup archival logger data to make an adjustment for surface availability. We demonstrate that satellite imagery can provide useful data on whale occurrence and density. Densities, when unadjusted for surface availability are shown to be considerably lower than those estimated by the ship survey. However, adjusted for surface availability and weather conditions (0.13 whales per km2, CV = 0.38), they fall within an order of magnitude of those derived by traditional line-transect estimates (0.33 whales per km2, CV = 0.09). Satellite surveys represent an exciting development for high-resolution image-based cetacean observation at sea, particularly in inaccessible regions, presenting opportunities for ongoing and future research.

Antarctic Futures: An Assessment of Climate-Driven Changes in Ecosystem Structure, Function, and Service Provisioning in the Southern Ocean.

In this article, we analyze the impacts of climate change on Antarctic marine ecosystems. Observations demonstrate large-scale changes in the physical variables and circulation of the Southern Ocean driven by warming, stratospheric ozone depletion, and a positive Southern Annular Mode. Alterations in the physical environment are driving change through all levels of Antarctic marine food webs, which differ regionally. The distributions of key species, such as Antarctic krill, are also changing. Differential responses among predators reflect differences in species ecology. The impacts of climate change on Antarctic biodiversity will likely vary for different communities and depend on species range. Coastal communities and those of sub-Antarctic islands, especially range-restricted endemic communities, will likely suffer the greatest negative consequences of climate change. Simultaneously, ecosystem services in the Southern Ocean will likely increase. Such decoupling of ecosystem services and endemic species will require consideration in the management of human activities such as fishing in Antarctic marine ecosystems.

Why whales are big but not bigger: Physiological drivers and ecological limits in the age of ocean giants.

The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.

Extreme bradycardia and tachycardia in the world's largest animal.

The biology of the blue whale has long fascinated physiologists because of the animal's extreme size. Despite high energetic demands from a large body, low mass-specific metabolic rates are likely powered by low heart rates. Diving bradycardia should slow blood oxygen depletion and enhance dive time available for foraging at depth. However, blue whales exhibit a high-cost feeding mechanism, lunge feeding, whereby large volumes of prey-laden water are intermittently engulfed and filtered during dives. This paradox of such a large, slowly beating heart and the high cost of lunge feeding represents a unique test of our understanding of cardiac function, hemodynamics, and physiological limits to body size. Here, we used an electrocardiogram (ECG)-depth recorder tag to measure blue whale heart rates during foraging dives as deep as 184 m and as long as 16.5 min. Heart rates during dives were typically 4 to 8 beats min-1 (bpm) and as low as 2 bpm, while after-dive surface heart rates were 25 to 37 bpm, near the estimated maximum heart rate possible. Despite extreme bradycardia, we recorded a 2.5-fold increase above diving heart rate minima during the powered ascent phase of feeding lunges followed by a gradual decrease of heart rate during the prolonged glide as engulfed water is filtered. These heart rate dynamics explain the unique hemodynamic design in rorqual whales consisting of a large-diameter, highly compliant, elastic aortic arch that allows the aorta to accommodate blood ejected by the heart and maintain blood flow during the long and variable pauses between heartbeats.

Body Flexibility Enhances Maneuverability in the World's Largest Predator.

Blue whales are often characterized as highly stable, open-ocean swimmers who sacrifice maneuverability for long-distance cruising performance. However, recent studies have revealed that blue whales actually exhibit surprisingly complex underwater behaviors, yet little is known about the performance and control of these maneuvers. Here, we use multi-sensor biologgers equipped with cameras to quantify the locomotor dynamics and the movement of the control surfaces used by foraging blue whales. Our results revealed that simple maneuvers (rolls, turns, and pitch changes) are performed using distinct combinations of control and power provided by the flippers, the flukes, and bending of the body, while complex trajectories are structured by combining sequences of simple maneuvers. Furthermore, blue whales improve their turning performance by using complex banked turns to take advantage of their substantial dorso-ventral flexibility. These results illustrate the important role body flexibility plays in enhancing control and performance of maneuvers, even in the largest of animals. The use of the body to supplement the performance of the hydrodynamically active surfaces may represent a new mechanism in the control of aquatic locomotion.

Using Digital Tags With Integrated Video and Inertial Sensors to Study Moving Morphology and Associated Function in Large Aquatic Vertebrates.

The anatomy of large cetaceans has been well documented, mostly through dissection of dead specimens. However, the difficulty of studying the world's largest animals in their natural environment means the functions of anatomical structures must be inferred. Recently, non-invasive tracking devices have been developed that measure body position and orientation, thereby enabling the detailed reconstruction of underwater trajectories. The addition of cameras to the whale-borne tags allows the sensor data to be matched with real-time observations of how whales use their morphological structures, such as flukes, flippers, feeding apparatuses, and blowholes for the physiological functions of locomotion, feeding, and breathing. Here, we describe a new tag design with integrated video and inertial sensors and how it can be used to provide insights to the function of whale anatomy. This technology has the potential to facilitate a wide range of discoveries and comparative studies, but many challenges remain to increase the resolution and applicability of the data. Anat Rec, 300:1935-1941, 2017. © 2017 Wiley Periodicals, Inc.

How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration.

Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time.

Prey-mediated behavioral responses of feeding blue whales in controlled sound exposure experiments.

Behavioral response studies provide significant insights into the nature, magnitude, and consequences of changes in animal behavior in response to some external stimulus. Controlled exposure experiments (CEEs) to study behavioral response have faced challenges in quantifying the importance of and interaction among individual variability, exposure conditions, and environmental covariates. To investigate these complex parameters relative to blue whale behavior and how it may change as a function of certain sounds, we deployed multi-sensor acoustic tags and conducted CEEs using simulated mid-frequency active sonar (MFAS) and pseudo-random noise (PRN) stimuli, while collecting synoptic, quantitative prey measures. In contrast to previous approaches that lacked such prey data, our integrated approach explained substantially more variance in blue whale dive behavioral responses to mid-frequency sounds (r2 = 0.725 vs. 0.14 previously). Results demonstrate that deep-feeding whales respond more clearly and strongly to CEEs than those in other behavioral states, but this was only evident with the increased explanatory power provided by incorporating prey density and distribution as contextual covariates. Including contextual variables increases the ability to characterize behavioral variability and empirically strengthens previous findings that deep-feeding blue whales respond significantly to mid-frequency sound exposure. However, our results are only based on a single behavioral state with a limited sample size, and this analytical framework should be applied broadly across behavioral states. The increased capability to describe and account for individual response variability by including environmental variables, such as prey, that drive foraging behavior underscores the importance of integrating these and other relevant contextual parameters in experimental designs. Our results suggest the need to measure and account for the ecological dynamics of predator-prey interactions when studying the effects of anthropogenic disturbance in feeding animals.

Discrimination of fast click-series produced by tagged Risso's dolphins (Grampus griseus) for echolocation or communication.

Early studies that categorized odontocete pulsed sounds had few means of discriminating signals used for biosonar-based foraging from those used for communication. This capability to identify the function of sounds is important for understanding and interpreting behavior; it is also essential for monitoring and mitigating potential disturbance from human activities. Archival tags were placed on free-ranging Grampus griseus to quantify and discriminate between pulsed sounds used for echolocation-based foraging and those used for communication. Two types of rapid click-series pulsed sounds, buzzes and burst pulses, were identified as produced by the tagged dolphins and classified using a Gaussian mixture model based on their duration, association with jerk (i.e. rapid change of acceleration) and temporal association with click trains. Buzzes followed regular echolocation clicks and coincided with a strong jerk signal from accelerometers on the tag. They consisted of series averaging 359±210 clicks (mean±s.d.) with an increasing repetition rate and relatively low amplitude. Burst pulses consisted of relatively short click series averaging 45±54 clicks with decreasing repetition rate and longer inter-click interval that were less likely to be associated with regular echolocation and the jerk signal. These results suggest that the longer, relatively lower amplitude, jerk-associated buzzes are used in this species to capture prey, mostly during the bottom phase of foraging dives, as seen in other odontocetes. In contrast, the shorter, isolated burst pulses that are generally emitted by the dolphins while at or near the surface are used outside of a direct, known foraging context.

Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis).

Body size and feeding mode are two fundamental characteristics that determine foraging performance and ecological niche. As the smallest obligate lunge filter feeders, minke whales represent an ideal system for studying the physical and energetic limits of filter feeding in endotherms. We used multi-sensor suction cup tags to quantify the feeding performance of Antarctic minke whales. Foraging dives around and beneath sea ice contained up to 24 lunges per dive, the highest feeding rates for any lunge-feeding whale. Their small size allows minke whales access to krill in sea-ice environments not easily accessible to larger baleen whales. Furthermore, their ability to filter feed provides an advantage over other smaller sympatric krill predators such as penguins and seals that feed on individual prey. The unique combination of body size, feeding mechanism and sea-ice habitat of Antarctic minke whales defines a previously undocumented energetic niche that is unique among aquatic vertebrates.

Using accelerometers to determine the calling behavior of tagged baleen whales.

Low-frequency acoustic signals generated by baleen whales can propagate over vast distances, making the assignment of calls to specific individuals problematic. Here, we report the novel use of acoustic recording tags equipped with high-resolution accelerometers to detect vibrations from the surface of two tagged fin whales that directly match the timing of recorded acoustic signals. A tag deployed on a buoy in the vicinity of calling fin whales and a recording from a tag that had just fallen off a whale were able to detect calls acoustically but did not record corresponding accelerometer signals that were measured on calling individuals. Across the hundreds of calls measured on two tagged fin whales, the accelerometer response was generally anisotropic across all three axes, appeared to depend on tag placement and increased with the level of received sound. These data demonstrate that high-sample rate accelerometry can provide important insights into the acoustic behavior of baleen whales that communicate at low frequencies. This method helps identify vocalizing whales, which in turn enables the quantification of call rates, a fundamental component of models used to estimate baleen whale abundance and distribution from passive acoustic monitoring.

Counting whales in a challenging, changing environment.

Estimating abundance of Antarctic minke whales is central to the International Whaling Commission's conservation and management work and understanding impacts of climate change on polar marine ecosystems. Detecting abundance trends is problematic, in part because minke whales are frequently sighted within Antarctic sea ice where navigational safety concerns prevent ships from surveying. Using icebreaker-supported helicopters, we conducted aerial surveys across a gradient of ice conditions to estimate minke whale density in the Weddell Sea. The surveys revealed substantial numbers of whales inside the sea ice. The Antarctic summer sea ice is undergoing rapid regional change in annual extent, distribution, and length of ice-covered season. These trends, along with substantial interannual variability in ice conditions, affect the proportion of whales available to be counted by traditional shipboard surveys. The strong association between whales and the dynamic, changing sea ice requires reexamination of the power to detect trends in whale abundance or predict ecosystem responses to climate change.