Baleen whale prey consumption based on high-resolution foraging measurements.

Baleen whales influence their ecosystems through immense prey consumption and nutrient recycling1-3. It is difficult to accurately gauge the magnitude of their current or historic ecosystem role without measuring feeding rates and prey consumed. To date, prey consumption of the largest species has been estimated using metabolic models3-9 based on extrapolations that lack empirical validation. Here, we used tags deployed on seven baleen whale (Mysticeti) species (n = 321 tag deployments) in conjunction with acoustic measurements of prey density to calculate prey consumption at daily to annual scales from the Atlantic, Pacific, and Southern Oceans. Our results suggest that previous studies3-9 have underestimated baleen whale prey consumption by threefold or more in some ecosystems. In the Southern Ocean alone, we calculate that pre-whaling populations of mysticetes annually consumed 430 million tonnes of Antarctic krill (Euphausia superba), twice the current estimated total biomass of E. superba10, and more than twice the global catch of marine fisheries today11. Larger whale populations may have supported higher productivity in large marine regions through enhanced nutrient recycling: our findings suggest mysticetes recycled 1.2 × 104 tonnes iron yr-1 in the Southern Ocean before whaling compared to 1.2 × 103 tonnes iron yr-1 recycled by whales today. The recovery of baleen whales and their nutrient recycling services2,3,7 could augment productivity and restore ecosystem function lost during 20th century whaling12,13.

The influence of biopsy site and pregnancy on stable isotope ratios in humpback whale skin.

RATIONALE: Stable isotope analysis (SIA) of free-swimming mysticetes using biopsies is often limited in sample size and uses only one sample per individual, failing to capture both intra-individual variability and the influence of demographic and physiological factors on isotope ratios. METHODS: We applied SIA of δ13C and δ15N to humpback whale (Megaptera novaeangliae) biopsies taken during the foraging season along the western Antarctic Peninsula to quantify intra-individual variation from repeatedly sampled individuals, as well as to determine the effect of biopsy collection site, sex, and pregnancy on isotope ratios. RESULTS: There was substantial variability in δ13C from multiple biopsies taken from the same individuals, though δ15N was much more consistent. Side of the body (left versus right) and biopsy location (dorsal, anterior, ventral, and posterior) did marginally affect the isotopic composition of δ15N but not δ13C. Pregnancy had a significant effect on both δ13C and δ15N, where pregnant females were depleted in both when compared to non-pregnant females and males. CONCLUSIONS: These results indicate that isotopic signatures are influenced by multiple endogenous and exogenous factors and emphasize value in accounting for intra-individual variability and pregnancy status within a sampled population. Placed within an ecological context, the endogenous variability in δ13C observed here may be informative for future isotopic analyses.

A surplus no more? Variation in krill availability impacts reproductive rates of Antarctic baleen whales.

The krill surplus hypothesis of unlimited prey resources available for Antarctic predators due to commercial whaling in the 20th century has remained largely untested since the 1970s. Rapid warming of the Western Antarctic Peninsula (WAP) over the past 50 years has resulted in decreased seasonal ice cover and a reduction of krill. The latter is being exacerbated by a commercial krill fishery in the region. Despite this, humpback whale populations have increased but may be at a threshold for growth based on these human-induced changes. Understanding how climate-mediated variation in prey availability influences humpback whale population dynamics is critical for focused management and conservation actions. Using an 8-year dataset (2013-2020), we show that inter-annual humpback whale pregnancy rates, as determined from skin-blubber biopsy samples (n = 616), are positively correlated with krill availability and fluctuations in ice cover in the previous year. Pregnancy rates showed significant inter-annual variability, between 29% and 86%. Our results indicate that krill availability is in fact limiting and affecting reproductive rates, in contrast to the krill surplus hypothesis. This suggests that this population of humpback whales may be at a threshold for population growth due to prey limitations. As a result, continued warming and increased fishing along the WAP, which continue to reduce krill stocks, will likely impact this humpback whale population and other krill predators in the region. Humpback whales are sentinel species of ecosystem health, and changes in pregnancy rates can provide quantifiable signals of the impact of environmental change at the population level. Our findings must be considered paramount in developing new and more restrictive conservation and management plans for the Antarctic marine ecosystem and minimizing the negative impacts of human activities in the region.

Scaling of maneuvering performance in baleen whales: larger whales outperform expectations.

Despite their enormous size, whales make their living as voracious predators. To catch their much smaller, more maneuverable prey, they have developed several unique locomotor strategies that require high energetic input, high mechanical power output and a surprising degree of agility. To better understand how body size affects maneuverability at the largest scale, we used bio-logging data, aerial photogrammetry and a high-throughput approach to quantify the maneuvering performance of seven species of free-swimming baleen whale. We found that as body size increases, absolute maneuvering performance decreases: larger whales use lower accelerations and perform slower pitch-changes, rolls and turns than smaller species. We also found that baleen whales exhibit positive allometry of maneuvering performance: relative to their body size, larger whales use higher accelerations, and perform faster pitch-changes, rolls and certain types of turns than smaller species. However, not all maneuvers were impacted by body size in the same way, and we found that larger whales behaviorally adjust for their decreased agility by using turns that they can perform more effectively. The positive allometry of maneuvering performance suggests that large whales have compensated for their increased body size by evolving more effective control surfaces and by preferentially selecting maneuvers that play to their strengths.

Remoras pick where they stick on blue whales.

Animal-borne video recordings from blue whales in the open ocean show that remoras preferentially adhere to specific regions on the surface of the whale. Using empirical and computational fluid dynamics analyses, we show that remora attachment was specific to regions of separating flow and wakes caused by surface features on the whale. Adhesion at these locations offers remoras drag reduction of up to 71-84% compared with the freestream. Remoras were observed to move freely along the surface of the whale using skimming and sliding behaviors. Skimming provided drag reduction as high as 50-72% at some locations for some remora sizes, but little to none was available in regions where few to no remoras were observed. Experimental work suggests that the Venturi effect may help remoras stay near the whale while skimming. Understanding the flow environment around a swimming blue whale will inform the placement of biosensor tags to increase attachment time for extended ecological monitoring.

The importance of migratory connectivity for global ocean policy.

The distributions of migratory species in the ocean span local, national and international jurisdictions. Across these ecologically interconnected regions, migratory marine species interact with anthropogenic stressors throughout their lives. Migratory connectivity, the geographical linking of individuals and populations throughout their migratory cycles, influences how spatial and temporal dynamics of stressors affect migratory animals and scale up to influence population abundance, distribution and species persistence. Population declines of many migratory marine species have led to calls for connectivity knowledge, especially insights from animal tracking studies, to be more systematically and synthetically incorporated into decision-making. Inclusion of migratory connectivity in the design of conservation and management measures is critical to ensure they are appropriate for the level of risk associated with various degrees of connectivity. Three mechanisms exist to incorporate migratory connectivity into international marine policy which guides conservation implementation: site-selection criteria, network design criteria and policy recommendations. Here, we review the concept of migratory connectivity and its use in international policy, and describe the Migratory Connectivity in the Ocean system, a migratory connectivity evidence-base for the ocean. We propose that without such collaboration focused on migratory connectivity, efforts to effectively conserve these critical species across jurisdictions will have limited effect.

Scaling of swimming performance in baleen whales.

The scale dependence of locomotor factors has long been studied in comparative biomechanics, but remains poorly understood for animals at the upper extremes of body size. Rorqual baleen whales include the largest animals, but we lack basic kinematic data about their movements and behavior below the ocean surface. Here, we combined morphometrics from aerial drone photogrammetry, whale-borne inertial sensing tag data and hydrodynamic modeling to study the locomotion of five rorqual species. We quantified changes in tail oscillatory frequency and cruising speed for individual whales spanning a threefold variation in body length, corresponding to an order of magnitude variation in estimated body mass. Our results showed that oscillatory frequency decreases with body length (∝length-0.53) while cruising speed remains roughly invariant (∝length0.08) at 2 m s-1 We compared these measured results for oscillatory frequency against simplified models of an oscillating cantilever beam (∝length-1) and an optimized oscillating Strouhal vortex generator (∝length-1). The difference between our length-scaling exponent and the simplified models suggests that animals are often swimming non-optimally in order to feed or perform other routine behaviors. Cruising speed aligned more closely with an estimate of the optimal speed required to minimize the energetic cost of swimming (∝length0.07). Our results are among the first to elucidate the relationships between both oscillatory frequency and cruising speed and body size for free-swimming animals at the largest scale.

Temporal and Regional Variability in the Skin Microbiome of Humpback Whales along the Western Antarctic Peninsula.

The skin is the first line of defense between an animal and its environment, and disruptions in skin-associated microorganisms can be linked to an animal's health and nutritional state. To better understand the skin microbiome of large whales, high-throughput sequencing of partial small subunit rRNA genes was used to study the skin-associated bacteria of 89 seemingly healthy humpback whales (Megaptera novaeangliae) sampled along the Western Antarctic Peninsula (WAP) during early (2010) and late (2013) austral summers. Six core groups of bacteria were present in 93% or more of all humpback skin samples. A shift was observed in the average relative abundances of these core bacteria over time, with the emergence of four additional core groups of bacteria that corresponded to a decrease in water temperature, possibly caused by season- or foraging-related changes in skin biochemistry that influenced microbial growth, or other temporal factors. The skin microbiome differed between whales sampled at several regional locations along the WAP, suggesting that environmental factors or population may also influence the whale skin microbiome. Overall, the skin microbiome of humpback whales appears to provide insight into animal- and environment-related factors and may serve as a useful indicator for animal health or ecosystem alterations.IMPORTANCE The microbiomes of wild animals are currently understudied but may provide information about animal health and/or animal-environment interactions. In the largest sampling of any marine mammal microbiome, this study demonstrates conservation in the skin microbiome of 89 seemingly healthy humpback whales sampled in the Western Antarctic Peninsula, with shifts in the bacterial community composition related to temporal and regional variability. This study is important because it suggests that the skin microbiome of humpback whales could provide insight into animal nutritional or seasonal/environment-related factors, which are becoming increasingly important to recognize due to unprecedented rates of climate change and anthropogenic impact on ocean ecosystems.

Determining forward speed from accelerometer jiggle in aquatic environments.

How fast animals move is critical to understanding their energetic requirements, locomotor capacity and foraging performance, yet current methods for measuring speed via animal-attached devices are not universally applicable. Here, we present and evaluate a new method that relates forward speed to the stochastic motion of biologging devices as tag jiggle, the amplitude of the tag vibrations as measured by high sample rate accelerometers, increases exponentially with increasing speed. We successfully tested this method in a flow tank using two types of biologging devices and in situ on wild cetaceans spanning ∼3 to >20 m in length using two types of suction cup-attached tag and two types of dart-attached tag. This technique provides some advantages over other approaches for determining speed as it is device-orientation independent and relies only on a pressure sensor and a high sample rate accelerometer, sensors that are nearly universal across biologging device types.

Risso's dolphins plan foraging dives.

Humans remember the past and use that information to plan future actions. Lab experiments that test memory for the location of food show that animals have a similar capability to act in anticipation of future needs, but less work has been done on animals foraging in the wild. We hypothesized that planning abilities are critical and common in breath-hold divers who adjust each dive to forage on prey varying in quality, location and predictability within constraints of limited oxygen availability. We equipped Risso's dolphins with sound-and-motion recording tags to reveal where they focus their attention through their externally observable echolocation and how they fine tune search strategies in response to expected and observed prey distribution. The information from the dolphins was integrated with synoptic prey data obtained from echosounders on an underwater vehicle. At the start of the dives, whales adjusted their echolocation inspection ranges in ways that suggest planning to forage at a particular depth. Once entering a productive prey layer, dolphins reduced their search range comparable to the scale of patches within the layer, suggesting that they were using echolocation to select prey within the patch. On ascent, their search range increased, indicating that they decided to stop foraging within that layer and started searching for prey in shallower layers. Information about prey, learned throughout the dive, was used to plan foraging in the next dive. Our results demonstrate that planning for future dives is modulated by spatial memory derived from multi-modal prey sampling (echoic, visual and capture) during earlier dives.

Selective reactions to different killer whale call categories in two delphinid species.

The risk of predation is often invoked as an important factor influencing the evolution of social organization in cetaceans, but little direct information is available about how these aquatic mammals respond to predators or other perceived threats. We used controlled playback experiments to examine the behavioral responses of short-finned pilot whales (Globicephala macrorhynchus) off Cape Hatteras, NC, USA, and Risso's dolphins (Grampus griseus) off the coast of Southern California, USA, to the calls of a potential predator, mammal-eating killer whales. We transmitted calls of mammal-eating killer whales, conspecifics and baleen whales to 10 pilot whales and four Risso's dolphins equipped with multi-sensor archival acoustic recording tags (DTAGs). Only playbacks of killer whale calls resulted in significant changes in tagged animal heading. The strong responses observed in both species occurred only following exposure to a subset of killer whale calls, all of which contained multiple non-linear properties. This finding suggests that these structural features of killer whale calls convey information about predatory risk to pilot whales and Risso's dolphins. The observed responses differed between the two species; pilot whales approached the sound source while Risso's dolphins fled following playbacks. These divergent responses likely reflect differences in anti-predator response mediated by the social structure of the two species.

Dynamic foraging of a top predator in a seasonal polar marine environment.

The seasonal movement of animals at broad spatial scales provides insight into life-history, ecology and conservation. By combining high-resolution satellite-tagged data with hierarchical Bayesian movement models, we can associate spatial patterns of movement with marine animal behavior. We used a multi-state mixture model to describe humpback whale traveling and area-restricted search states as they forage along the West Antarctic Peninsula. We estimated the change in the geography, composition and characteristics of these behavioral states through time. We show that whales later in the austral fall spent more time in movements associated with foraging, traveled at lower speeds between foraging areas, and shifted their distribution northward and inshore. Seasonal changes in movement are likely due to a combination of sea ice advance and regional shifts in the primary prey source. Our study is a step towards dynamic movement models in the marine environment at broad scales.

Hydrodynamic properties of fin whale flippers predict maximum rolling performance.

Maneuverability is one of the most important and least understood aspects of animal locomotion. The hydrofoil-like flippers of cetaceans are thought to function as control surfaces that effect maneuvers, but quantitative tests of this hypothesis have been lacking. Here, we constructed a simple hydrodynamic model to predict the longitudinal-axis roll performance of fin whales, and we tested its predictions against kinematic data recorded by on-board movement sensors from 27 free-swimming fin whales. We found that for a given swimming speed and roll excursion, the roll velocity of fin whales calculated from our field data agrees well with that predicted by our hydrodynamic model. Although fluke and body torsion may further influence performance, our results indicate that lift generated by the flippers is sufficient to drive most of the longitudinal-axis rolls used by fin whales for feeding and maneuvering.

Evidence for ship noise impacts on humpback whale foraging behaviour.

Noise from shipping activity in North Atlantic coastal waters has been steadily increasing and is an area of growing conservation concern, as it has the potential to disrupt the behaviour of marine organisms. This study examines the impacts of ship noise on bottom foraging humpback whales (Megaptera novaeangliae) in the western North Atlantic. Data were collected from 10 foraging whales using non-invasive archival tags that simultaneously recorded underwater movements and the acoustic environment at the whale. Using mixed models, we assess the effects of ship noise on seven parameters of their feeding behaviours. Independent variables included the presence or absence of ship noise and the received level of ship noise at the whale. We found significant effects on foraging, including slower descent rates and fewer side-roll feeding events per dive with increasing ship noise. During 5 of 18 ship passages, dives without side-rolls were observed. These findings indicate that humpback whales on Stellwagen Bank, an area with chronically elevated levels of shipping traffic, significantly change foraging activity when exposed to high levels of ship noise. This measureable reduction in within-dive foraging effort of individual whales could potentially lead to population-level impacts of shipping noise on baleen whale foraging success.

Mysterious bio-duck sound attributed to the Antarctic minke whale (Balaenoptera bonaerensis).

For decades, the bio-duck sound has been recorded in the Southern Ocean, but the animal producing it has remained a mystery. Heard mainly during austral winter in the Southern Ocean, this ubiquitous sound has been recorded in Antarctic waters and contemporaneously off the Australian west coast. Here, we present conclusive evidence that the bio-duck sound is produced by Antarctic minke whales (Balaenoptera bonaerensis). We analysed data from multi-sensor acoustic recording tags that included intense bio-duck sounds as well as singular downsweeps that have previously been attributed to this species. This finding allows the interpretation of a wealth of long-term acoustic recordings for this previously acoustically concealed species, which will improve our understanding of the distribution, abundance and behaviour of Antarctic minke whales. This is critical information for a species that inhabits a difficult to access sea-ice environment that is changing rapidly in some regions and has been the subject of contentious lethal sampling efforts and ongoing international legal action.

Demographic and physiological signals of reproductive events in humpback whales on a southwest pacific breeding ground.

The field of marine mammal conservation has dramatically benefited from the rapid advancement of methods to assess the reproductive physiology of individuals and populations from steroid hormones isolated from minimally invasive skin-blubber biopsy samples. Historically, this vital information was only available from complete anatomical and physiological investigations of samples collected during commercial or indigenous whaling. Humpback whales (Megaptera novaeangliae) are a migratory, cosmopolitan species that reproduce in warm, low-latitude breeding grounds. New Caledonia is seasonally visited by a small breeding sub-stock of humpback whales, forming part of the endangered Oceania subpopulation. To better understand the demographic and seasonal patterns of reproductive physiology in humpback whales, we quantified baseline measurements of reproductive hormones (progesterone-P4, testosterone-T and 17ß-estradiol-E2) using an extensive archive of skin-blubber biopsy samples collected from female humpback whales in New Caledonia waters between 2016 and 2019 (n = 194). We observed significant differences in the P4, T and E2 concentrations across different demographic groups of female humpback whales, and we described some of the first evidence of the endocrine patterns of estrous in live free-ranging baleen whales. This study is fundamental in its methodological approach to a wild species that has a global distribution, with seasonally distinct life histories. This information will assist in monitoring, managing and conserving this population as global ecological changes continue to occur unhindered.

Historical baleen plates indicate that once abundant Antarctic blue and fin whales demonstrated distinct migratory and foraging strategies.

Southern hemisphere blue (Balaenoptera musculus intermedia) and fin (Balaenoptera physalus) whales are the largest predators in the Southern Ocean, with similarities in morphology and distribution. Yet, understanding of their life history and foraging is limited due to current low abundances and limited ecological data. To address these gaps, historic Antarctic blue (n = 5) and fin (n = 5) whale baleen plates, collected in 1947-1948 and recently rediscovered in the Smithsonian National Museum of Natural History, were analyzed for bulk (δ13C and δ15N) stable isotopes. Regular oscillations in isotopic ratios, interpreted as annual cycles, revealed that baleen plates contain approximately 6 years (14.35 ± 1.20 cm year-1) of life history data in blue whales and 4 years (16.52 ± 1.86 cm year-1) in fin whales. Isotopic results suggest that: (1) while in the Southern Ocean, blue and fin whales likely fed at the same trophic level but demonstrated niche differentiation; (2) fin whales appear to have had more regular annual migrations; and (3) fin whales may have migrated to ecologically distinct sub-Antarctic waters annually while some blue whales may have resided year-round in the Southern Ocean. These results reveal differences in ecological niche and life history strategies between Antarctic blue and fin whales during a time period when their populations were more abundant than today, and before major human-driven climatic changes occurred in the Southern Ocean.

Caller identification and characterization of individual humpback whale acoustic behaviour.

Acoustic recording tags provide fine-scale data linking acoustic signalling with individual behaviour; however, when an animal is in a group, it is challenging to tease apart calls of conspecifics and identify which individuals produce each call. This, in turn, prohibits a robust assessment of individual acoustic behaviour including call rates and silent periods, call bout production within and between individuals, and caller location. To overcome this challenge, we simultaneously instrumented small groups of humpback whales on a western North Atlantic feeding ground with sound and movement recording tags. This approach enabled a comparison of the relative amplitude of each call across individuals to infer caller identity for 97% of calls. We recorded variable call rates across individuals (mean = 23 calls/h) and groups (mean = 55 calls/h). Calls were produced throughout dives, and most calls were produced in bouts with short inter-call intervals of 2.2 s. Most calls received a likely response from a conspecific within 100 s. This caller identification (ID) method facilitates studying both individual- and group-level acoustic behaviour, yielding novel results about the nature of sequence production and vocal exchanges in humpback whale social calls. Future studies can expand on these caller ID methods for understanding intra-group communication across taxa.

Acoustic behavior of humpback whale calves on the feeding ground: Comparisons across age and implications for vocal development.

Studying sound production at different developmental stages can provide insight into the processes involved in vocal ontogeny. Humpback whales (Megaptera novaeangliae) are a known vocal learning species, but their vocal development is poorly understood. While studies of humpback whale calves in the early stages of their lives on the breeding grounds and migration routes exist, little is known about the behavior of these immature, dependent animals by the time they reach the feeding grounds. In this study, we used data from groups of North Atlantic humpback whales in the Gulf of Maine in which all members were simultaneously carrying acoustic recording tags attached with suction cups. This allowed for assignment of likely caller identity using the relative received levels of calls across tags. We analyzed data from 3 calves and 13 adults. There were high levels of call rate variation among these individuals and the results represent preliminary descriptions of calf behavior. Our analysis suggests that, in contrast to the breeding grounds or on migration, calves are no longer acoustically cryptic by the time they reach their feeding ground. Calves and adults both produce calls in bouts, but there may be some differences in bout parameters like inter-call intervals and bout durations. Calves were able to produce most of the adult vocal repertoire but used different call types in different proportions. Finally, we found evidence of immature call types in calves, akin to protosyllables used in babbling in other mammals, including humans. Overall, the sound production of humpback whale calves on the feeding grounds appears to be already similar to that of adults, but with differences in line with ontogenetic changes observed in other vocal learning species.

No distinct local cuisines among humpback whales: A population diet comparison in the Southern Hemisphere.

Southern hemisphere humpback whale (Megaptera novaeangliae, SHHW) breeding populations follow a high-fidelity Antarctic krill (Euphausia superba) diet while feeding in distinct sectors of the Southern Ocean. Their capital breeding life history requires predictable ecosystem productivity to fuel migration and migration-related behaviours. It is therefore postulated that populations feeding in areas subject to the strongest climate change impacts are more likely to show the first signs of a departure from a high-fidelity krill diet. We tested this hypothesis by investigating blubber fatty acid profiles and skin stable isotopes obtained from five SHHW populations in 2019, and comparing them to Antarctic krill stable isotopes sampled in three SHHW feeding areas in the Southern Ocean in 2019. Fatty acid profiles and δ13C and δ15N varied significantly among all five populations, however, calculated trophic positions did not (2.7 to 3.1). Similarly, fatty acid ratios, 16:1ω7c/16:0 and 20:5ω3/22:6ω3 were above 1, showing that whales from all five populations are secondary heterotrophs following an omnivorous diet with a diatom-origin. Thus, evidence for a potential departure from a high-fidelity Antarctic krill diet was not seen in any population. δ13C of all populations were similar to δ13C of krill sampled in productive upwelling areas or the marginal sea-ice zone. Consistency in trophic position and diet origin but significant fatty acid and stable isotope differences demonstrate that the observed variability arises at lower trophic levels. Our results indicate that, at present, there is no evidence of a divergence from a high-fidelity krill diet. Nevertheless, the characteristic isotopic signal of whales feeding in productive upwelling areas, or in the marginal sea-ice zone, implies that future cryosphere reductions could impact their feeding ecology.