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.

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.

Legacy and Novel Per- and Polyfluoroalkyl Substances in Juvenile Seabirds from the U.S. Atlantic Coast.

Per- and polyfluoroalkyl substances (PFAS) are anthropogenic, globally distributed chemicals. Legacy PFAS, including perfluorooctane sulfonate (PFOS), have been regularly detected in marine fauna but little is known about their current levels or the presence of novel PFAS in seabirds. We measured 36 emerging and legacy PFAS in livers from 31 juvenile seabirds from Massachusetts Bay, Narragansett Bay, and the Cape Fear River Estuary (CFRE), United States. PFOS was the major legacy perfluoroalkyl acid present, making up 58% of concentrations observed across all habitats (range: 11-280 ng/g). Novel PFAS were confirmed in chicks hatched downstream of a fluoropolymer production site in the CFRE: a perfluorinated ether sulfonic acid (Nafion byproduct 2; range: 1-110 ng/g) and two perfluorinated ether carboxylic acids (PFO4DA and PFO5DoDA; PFO5DoDA range: 5-30 ng/g). PFOS was inversely associated with phospholipid content in livers from CFRE and Massachusetts Bay individuals, while δ 13C, an indicator of marine versus terrestrial foraging, was positively correlated with some long-chain PFAS in CFRE chick livers. There is also an indication that seabird phospholipid dynamics are negatively impacted by PFAS, which should be further explored given the importance of lipids for seabirds.

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.

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.

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.

Deployment of biologging tags on free swimming large whales using uncrewed aerial systems.

Suction-cup-attached biologging tags have led to major advances in our understanding of large whale behaviour. Getting close enough to a whale at sea to safely attach a tag is a major limiting factor when deploying these systems. Here we present an uncrewed aerial system (UAS)-based tagging technique for free-swimming large whales and provide data on efficacy from field testing on blue (Balaenoptera musculus) and fin (B. physalus) whales. Rapid transit speed and the bird's-eye view of the animal during UAS tagging contributed to the technique's success. During 8 days of field testing, we had 29 occasions when a focal animal was identified for attempted tagging and tags were successfully attached 21 times. The technique was efficient, with mean flight time of 2 min 45 s from launch to deployment and a mean distance of 490 m from the launch vessel to tagged animal, reducing potential adverse effects resulting from close approaches for tagging. These data indicate that UAS are capable of attaching biologging tags to free-swimming large whales quickly and from large distances, potentially increasing success rates, decreasing attempt times, and reducing animal disruption during tagging.

Pose-gait analysis for cetacean biologging tag data.

Biologging tags are a key enabling tool for investigating cetacean behavior and locomotion in their natural habitat. Identifying and then parameterizing gait from movement sensor data is critical for these investigations, but how best to characterize gait from tag data remains an open question. Further, the location and orientation of a tag on an animal in the field are variable and can change multiple times during a deployment. As a result, the relative orientation of the tag with respect to (wrt) the animal must be determined for analysis. Currently, custom scripts that involve species-specific heuristics tend to be used in the literature. These methods require a level of knowledge and experience that can affect the reliability and repeatability of the analysis. Swimming gait is composed of a sequence of body poses that have a specific spatial pattern, and tag-based measurements of this pattern can be utilized to determine the relative orientation of the tag. This work presents an automated data processing pipeline (and software) that takes advantage of these patterns to 1) Identify relative motion between the tag and animal; 2) Estimate the relative orientation of the tag wrt the animal using a data-driven approach; and 3) Calculate gait parameters that are stable and invariant to animal pose. Validation results from bottlenose dolphin tag data show that the average relative orientation error (tag wrt the body) after processing was within 11 degrees in roll, pitch, and yaw directions. The average precision and recall for detecting instances of relative motion in the dolphin data were 0.87 and 0.89, respectively. Tag data from humpback and beluga whales were then used to demonstrate how the gait analysis can be used to enhance tag-based investigations of movement and behavior. The MATLAB source code and data presented in the paper are publicly available (https://github.com/ding-z/cetacean-pose-gait-analysis.git), along with suggested best practices.

Specializations of somatosensory innervation in the skin of humpback whales (Megaptera novaeangliae).

Cetacean behavior and life history imply a role for somatosensory detection of critical signals unique to their marine environment. As the sensory anatomy of cetacean glabrous skin has not been fully explored, skin biopsy samples of the flank skin of humpback whales were prepared for general histological and immunohistochemical (IHC) analyses of innervation in this study. Histology revealed an exceptionally thick epidermis interdigitated by numerous, closely spaced long, thin diameter penicillate dermal papillae (PDP). The dermis had a stratified organization including a deep neural plexus (DNP) stratum intermingled with small arteries that was the source of intermingled nerves and arterioles forming a more superficial subepidermal neural plexus (SNP) stratum. The patterns of nerves branching through the DNP and SNP that distribute extensive innervation to arteries and arterioles and to the upper dermis and PDP provide a dense innervation associated through the whole epidermis. Some NF-H+ fibers terminated at the base of the epidermis and as encapsulated endings in dermal papillae similar to Merkel innervation and encapsulated endings seen in terrestrial mammals. However, unlike in all mammalian species assessed to date, an unusual acellular gap was present between the perineural sheaths and the central core of axons in all the cutaneous nerves perhaps as mechanism to prevent high hydrostatic pressure from compressing and interfering with axonal conductance. Altogether the whale skin has an exceptionally dense low-threshold mechanosensory system innervation most likely adapted for sensing hydrodynamic stimuli, as well as nerves that can likely withstand high pressure experienced during deep dives.

Birds of a feather eat plastic together: high levels of plastic ingestion in Great Shearwater adults and juveniles across their annual migratory cycle.

Limited work to date has examined plastic ingestion in highly migratory seabirds like Great Shearwaters (Ardenna gravis) across the their entire migratory range, although this species is prone to ingest plastic as a wide-ranging procellariiform. We examined 217 Great Shearwaters obtained from 2008-2019 at multiple locations spanning their yearly migration cycle across the Northwest and South Atlantic to assess accumulation of ingested plastic as well as trends over time and between locations. A total of 2,328 plastic fragments were documented in the ventriculus portion of the gastrointestinal tract, with an average of 9 plastic fragments per bird. The mass, count, and frequency of plastic occurrence (FO) varied by location, with higher plastic burdens but lower FO in South Atlantic individuals from the breeding colonies. No fragments of the same size or morphology were found in the primary forage fish prey, the sand lance, (Ammodytes spp., n = 202) that supports Great Shearwaters in Massachusetts Bay, USA, suggesting the birds directly ingest the bulk of their plastic loads rather than accumulating via trophic transfer. Fourier-transform infrared spectroscopy indicated that low- and high-density polyethylene were the most common polymers ingested, within all years and locations. Individuals from the South Atlantic contained a higher proportion of larger plastic items and fragments compared to juveniles and non-breeding adults from the NW Atlantic, possibly due to increased use of remote, pelagic areas subject to reduced inputs of smaller, more diverse, and potentially less buoyant plastics found adjacent to coastal margins. Different signatures of polymer type, size, and category between similar life stages at different locations suggests rapid turnover of ingested plastics commensurate with migratory stage and location, though more empirical evidence is needed to ground-truth this hypothesis. This work is the first to comprehensively measure the accumulation of ingested plastics by Great Shearwaters over the last decade and across multiple locations spanning their yearly trans-equatorial migration cycle, and underscores their utility as sentinels of plastic pollution in Atlantic ecosystems.

Common humpback whale (Megaptera novaeangliae) sound types for passive acoustic monitoring.

Humpback whales (Megaptera novaeangliae) are one of several baleen whale species in the Northwest Atlantic that coexist with vessel traffic and anthropogenic noise. Passive acoustic monitoring strategies can be used in conservation management, but the first step toward understanding the acoustic behavior of a species is a good description of its acoustic repertoire. Digital acoustic tags (DTAGs) were placed on humpback whales in the Stellwagen Bank National Marine Sanctuary to record and describe the non-song sounds being produced in conjunction with foraging activities. Peak frequencies of sounds were generally less than 1 kHz, but ranged as high as 6 kHz, and sounds were generally less than 1 s in duration. Cluster analysis distilled the dataset into eight groups of sounds with similar acoustic properties. The two most stereotyped and distinctive types ("wops" and "grunts") were also identified aurally as candidates for use in passive acoustic monitoring. This identification of two of the most common sound types will be useful for moving forward conservation efforts on this Northwest Atlantic feeding ground.

Tissue-specific distribution of legacy and novel per- and polyfluoroalkyl substances in juvenile seabirds.

Of the thousands of per- and polyfluoroalkyl substances (PFAS) in the environment, few have been investigated in detail. In this study, we analyzed 36 legacy and emerging PFAS in multiple seabird tissues collected from individuals from Massachusetts Bay, Narragansett Bay and the Cape Fear River Estuary. PFOS was the dominant compound across multiple tissues, while long-chain perfluorinated carboxylic acids (PFCAs) dominated in brain (mean = 44% of total concentrations). Emerging perfluoroalkyl ether acids (PFEAs)-Nafion byproduct-2 and PFO5DoDA - were detected in greater than 90% of tissues in birds obtained from a nesting region downstream from a major fluorochemical production site. Compound ratios, relative body burden calculations, and electrostatic surface potential calculations were used to describe partitioning behavior of PFEAs in different tissues. Novel PFEAs preferentially partition into blood compared to liver, and were documented in brain for the first time. PFO5DoDA showed a reduced preference for brain compared to PFCAs and Nafion BP2. These results suggest future monitoring efforts and toxicological studies should focus on novel PFAS and long-chain PFCAs in multiple tissues beyond liver and blood, while exploring the unique binding mechanisms driving uptake of multi-ether PFEAs.

Natural dimethyl sulfide gradients would lead marine predators to higher prey biomass.

Finding prey is essential to survival, with marine predators hypothesised to track chemicals such as dimethyl sulfide (DMS) while foraging. Many predators are attracted to artificially released DMS, and laboratory experiments have shown that zooplankton grazing on phytoplankton accelerates DMS release. However, whether natural DMS concentrations are useful for predators and correlated to areas of high prey biomass remains a fundamental knowledge gap. Here, we used concurrent hydroacoustic surveys and in situ DMS measurements to present evidence that zooplankton biomass is spatially correlated to natural DMS concentration in air and seawater. Using agent simulations, we also show that following gradients of DMS would lead zooplankton predators to areas of higher prey biomass than swimming randomly. Further understanding of the conditions and scales over which these gradients occur, and how they are used by predators, is essential to predicting the impact of future changes in the ocean on predator foraging success.

From a calf's perspective: humpback whale nursing behavior on two US feeding grounds.

Nursing influences growth rate and overall health of mammals; however, the behavior is difficult to study in wild cetaceans because it occurs below the surface and can thus be misidentified from surface observations. Nursing has been observed in humpback whales on the breeding and calving grounds, but the behavior remains unstudied on the feeding grounds. We instrumented three dependent calves (four total deployments) with combined video and 3D-accelerometer data loggers (CATS) on two United States feeding grounds to document nursing events. Two associated mothers were also tagged to determine if behavior diagnostic of nursing was evident in the mother's movement. Animal-borne video was manually analyzed and the average duration of successful nursing events was 23 s (±7 sd, n = 11). Nursing occurred at depths between 4.1-64.4 m (along the seafloor) and in close temporal proximity to foraging events by the mothers, but could not be predicted solely by relative positions of mother and calf. When combining all calf deployments, successful nursing was documented eleven times; totaling only 0.3% of 21.0 hours of video. During nursing events, calves had higher overall dynamic body acceleration (ODBA) and increased fluke-stroke rate (FSR) compared to non-nursing segments (Mixed effect models, ODBA: F1,107 = 13.57756, p = 0.0004, FSR: F1,107 = 32.31018, p < 0.0001). In contrast, mothers had lower ODBA and reduced FSR during nursing events compared to non-nursing segments. These data provide the first characterization of accelerometer data of humpback whale nursing confirmed by animal-borne video tags and the first analysis of nursing events on feeding grounds. This is an important step in understanding the energetic consequences of lactation while foraging.

Energetic and physical limitations on the breaching performance of large whales.

The considerable power needed for large whales to leap out of the water may represent the single most expensive burst maneuver found in nature. However, the mechanics and energetic costs associated with the breaching behaviors of large whales remain poorly understood. In this study we deployed whale-borne tags to measure the kinematics of breaching to test the hypothesis that these spectacular aerial displays are metabolically expensive. We found that breaching whales use variable underwater trajectories, and that high-emergence breaches are faster and require more energy than predatory lunges. The most expensive breaches approach the upper limits of vertebrate muscle performance, and the energetic cost of breaching is high enough that repeated breaching events may serve as honest signaling of body condition. Furthermore, the confluence of muscle contractile properties, hydrodynamics, and the high speeds required likely impose an upper limit to the body size and effectiveness of breaching whales.

Effectiveness of voluntary conservation agreements: case study of endangered whales and commercial whale watching.

The use of voluntary approaches to achieve conservation goals is becoming increasingly popular. Nevertheless, few researchers have quantitatively evaluated their efficacy. In 1998 industry, government agencies, and nongovernmental organizations established a voluntary conservation program for whale watching in the northeast region of the United States, with the intent to avoid collisions with and harassment of endangered whales by commercial and recreational whale-watching vessels. One important aspect of the program was the establishment of 3 speed zones within specific distances of whales. We wanted to determine the level of compliance with this aspect of the program to gauge its efficacy and gain insights into the effectiveness of voluntary measures as a conservation tool. Inconspicuous observers accompanied 46 commercial whale-watching trips from 12 companies in 2003 (n= 35) and 2004 (n= 11). During each trip, vessel position and speed were collected at 5-second intervals with a GPS receiver. Binoculars with internal laser rangefinders and digital compasses were used to record range and bearing to sighted whales. We mapped whale locations with ArcGIS. We created speed-zone buffers around sighted whales and overlaid them with vessel-track and speed data to evaluate compliance. Speeds in excess of those recommended by the program were considered noncompliant. We judged the magnitude of noncompliance by comparing a vessel's maximum speed within a zone to its maximum recorded trip speed. The level of noncompliance was high (mean 0.78; company range 0.74-0.88), some companies were more compliant than others (p= 0.02), noncompliance was significantly higher in zones farther from whales (p < 0.001), and operators approached the maximum speed capabilities of their vessel in all zones. The voluntary conservation program did not achieve the goal of substantially limiting vessel speed near whales. Our results support the need for conservation programs to have quantifiable metrics and frequent evaluation to ensure efficacy.

Evidence for acoustic communication among bottom foraging humpback whales.

Humpback whales (Megaptera novaeangliae), a mysticete with a cosmopolitan distribution, demonstrate marked behavioural plasticity. Recent studies show evidence of social learning in the transmission of specific population level traits ranging from complex singing to stereotyped prey capturing behaviour. Humpback whales have been observed to employ group foraging techniques, however details on how individuals coordinate behaviour in these groups is challenging to obtain. This study investigates the role of a novel broadband patterned pulsed sound produced by humpback whales engaged in bottom-feeding behaviours, referred to here as a 'paired burst' sound. Data collected from 56 archival acoustic tag deployments were investigated to determine the functional significance of these signals. Paired burst sound production was associated exclusively with bottom feeding under low-light conditions, predominantly with evidence of associated conspecifics nearby suggesting that the sound likely serves either as a communicative signal to conspecifics, a signal to affect prey behaviour, or possibly both. This study provides additional evidence for individual variation and phenotypic plasticity of foraging behaviours in humpback whales and provides important evidence for the use of acoustic signals among foraging individuals in this species.

'Megapclicks': acoustic click trains and buzzes produced during night-time foraging of humpback whales (Megaptera novaeangliae).

Humpback whales (Megaptera novaeangliae) exhibit a variety of foraging behaviours, but neither they nor any baleen whale are known to produce broadband clicks in association with feeding, as do many odontocetes. We recorded underwater behaviour of humpback whales in a northwest Atlantic feeding area using suction-cup attached, multi-sensor, acoustic tags (DTAGs). Here we describe the first recordings of click production associated with underwater lunges from baleen whales. Recordings of over 34000 'megapclicks' from two whales indicated relatively low received levels at the tag (between 143 and 154dB re 1 microPa pp), most energy below 2kHz, and interclick intervals often decreasing towards the end of click trains to form a buzz. All clicks were recorded during night-time hours. Sharp body rolls also occurred at the end of click bouts containing buzzes, suggesting feeding events. This acoustic behaviour seems to form part of a night-time feeding tactic for humpbacks and also expands the known acoustic repertoire of baleen whales in general.