Submesoscale coupling of krill and whales revealed by aggregative Lagrangian coherent structures.

In the marine environment, dynamic physical processes shape biological productivity and predator-prey interactions across multiple scales. Identifying pathways of physical-biological coupling is fundamental to understand the functioning of marine ecosystems yet it is challenging because the interactions are difficult to measure. We examined submesoscale (less than 100 km) surface current features using remote sensing techniques alongside ship-based surveys of krill and baleen whale distributions in the California Current System. We found that aggregative surface current features, represented by Lagrangian coherent structures (LCS) integrated over temporal scales between 2 and 10 days, were associated with increased (a) krill density (up to 2.6 times more dense), (b) baleen whale presence (up to 8.3 times more likely) and (c) subsurface seawater density (at depths up to 10 m). The link between physical oceanography, krill density and krill-predator distributions suggests that LCS are important features that drive the flux of energy and nutrients across trophic levels. Our results may help inform dynamic management strategies aimed at reducing large whales ship strikes and help assess the potential impacts of environmental change on this critical ecosystem.

Spin-leap performance by cetaceans is influenced by moment of inertia.

Cetaceans are capable of extraordinary locomotor behaviors in both water and air. Whales and dolphins can execute aerial leaps by swimming rapidly to the water surface to achieve an escape velocity. Previous research on spinner dolphins demonstrated the capability of leaping and completing multiple spins around their longitudinal axis with high angular velocities. This prior research suggested the slender body morphology of spinner dolphins together with the shapes and positions of their appendages allowed for rapid spins in the air. To test whether greater moments of inertia reduced spinning performance, videos and biologging data of cetaceans above and below the water surface were obtained. The principal factors affecting the number of aerial spins a cetacean can execute were moment of inertia and use of control surfaces for subsurface corkscrewing. For spinner dolphin, Pacific striped dolphin, bottlenose dolphin, minke whale and humpback whale, each with swim speeds of 6-7 m s-1, our model predicted that the number of aerial spins executable was 7, 2, 2, 0.76 and 1, respectively, which was consistent with observations. These data implied that the rate of subsurface corkscrewing was limited to 14.0, 6.8, 6.2, 2.2 and 0.75 rad s-1 for spinner dolphins, striped dolphins, bottlenose dolphins, minke whales and humpback whales, respectively. In our study, the moment of inertia of the cetaceans spanned a 21,000-fold range. The greater moments of inertia for the last four species produced large torques on control surfaces that limited subsurface corkscrewing motion and aerial maneuvers compared with spinner dolphins.

Behavioural responses of fin whales to military mid-frequency active sonar.

The effect of active sonars on marine mammal behaviour is a topic of considerable interest and scientific investigation. Some whales, including the largest species (blue whales, Balaenoptera musculus), can be impacted by mid-frequency (1-10 kHz) military sonars. Here we apply complementary experimental methods to provide the first experimentally controlled measurements of behavioural responses to military sonar and similar stimuli for a related endangered species, fin whales (Balaenoptera physalus). Analytical methods include: (i) principal component analysis paired with generalized additive mixed models; (ii) hidden Markov models; and (iii) structured expert elicitation using response severity metrics. These approaches provide complementary perspectives on the nature of potential changes within and across individuals. Behavioural changes were detected in five of 15 whales during controlled exposure experiments using mid-frequency active sonar or pseudorandom noise of similar frequency, duration and source and received level. No changes were detected during six control (no noise) sequences. Overall responses were more limited in occurrence, severity and duration than in blue whales and were less dependent upon contextual aspects of exposure and more contingent upon exposure received level. Quantifying the factors influencing marine mammal responses to sonar is critical in assessing and mitigating future impacts.

Minke whale feeding rate limitations suggest constraints on the minimum body size for engulfment filtration feeding.

Bulk filter feeding has enabled gigantism throughout evolutionary history. The largest animals, extant rorqual whales, utilize intermittent engulfment filtration feeding (lunge feeding), which increases in efficiency with body size, enabling their gigantism. The smallest extant rorquals (7-10 m minke whales), however, still exhibit short-term foraging efficiencies several times greater than smaller non-filter-feeding cetaceans, raising the question of why smaller animals do not utilize this foraging modality. We collected 437 h of bio-logging data from 23 Antarctic minke whales (Balaenoptera bonaerensis) to test the relationship of feeding rates (λf) to body size. Here, we show that while ultra-high nighttime λf (mean ± s.d.: 165 ± 40 lunges h-1; max: 236 lunges h-1; mean depth: 28 ± 46 m) were indistinguishable from predictions from observations of larger species, daytime λf (mean depth: 72 ± 72 m) were only 25-40% of predicted rates. Both λf were near the maxima allowed by calculated biomechanical, physiological and environmental constraints, but these temporal constraints meant that maximum λf was below the expected λf for animals smaller than ~5 m-the length of weaned minke whales. Our findings suggest that minimum size for specific filter-feeding body plans may relate broadly to temporal restrictions on filtration rate and have implications for the evolution of filter feeding.

Formation of a fringe: A look inside baleen morphology using a multimodal visual approach.

Filter-feeding has been present for hundreds of millions of years, independently evolving in aquatic vertebrates' numerous times. Mysticete whales are a group of gigantic, marine filter-feeders that are defined by their fringed baleen and are divided into two groups: balaenids and rorquals. Recent studies have shown that balaenids likely feed using a self-cleaning, cross-flow filtration mechanism where food particles are collected and then swept to the esophagus for swallowing. However, it is unclear how filtering is achieved in the rorquals (Balaenopteridae). Lunging rorqual whales engulf enormous masses of both prey and water; the prey is then separated from the water through baleen plates lining the length of their upper jaw and positioned perpendicular to flow. Rorqual baleen is composed of both major (larger) and minor (smaller) keratin plates containing embedded fringe that extends into the whale's mouth, forming a filtering fringe. We used a multimodal approach, including microcomputed tomography (µCT) and scanning electron microscopy (SEM), to visualize and describe the variability in baleen anatomy across five species of rorqual whales, spanning two orders of magnitude in body length. For most morphological measurements, larger whales exhibited hypoallometry relative to body length. µCT and SEM revealed that the major and minor plates break away from the mineralized fringes at variable distances from the gums. We proposed a model for estimating the effective pore size to determine whether flow scales with body length or prey size across species. We found that pore size is likely not a proxy for prey size but instead, may reflect changes in resistance through the filter that affect fluid flow.

Oceanic giants dance to atmospheric rhythms: Ephemeral wind-driven resource tracking by blue whales.

Trophic transfer of energy through marine food webs is strongly influenced by prey aggregation and its exploitation by predators. Rapid aggregation of some marine fish and crustacean forage species during wind-driven coastal upwelling has recently been discovered, motivating the hypothesis that predators of these forage species track the upwelling circulation in which prey aggregation occurs. We examine this hypothesis in the central California Current Ecosystem using integrative observations of upwelling dynamics, forage species' aggregation, and blue whale movement. Directional origins of blue whale calls repeatedly tracked upwelling plume circulation when wind-driven upwelling intensified and aggregation of forage species was heightened. Our findings illustrate a resource tracking strategy by which blue whales may maximize energy gain amid ephemeral foraging opportunities. These findings have implications for the ecology and conservation of diverse predators that are sustained by forage populations whose behaviour is responsive to episodic environmental dynamics.

Fast and Furious: Energetic Tradeoffs and Scaling of High-Speed Foraging in Rorqual Whales.

Although gigantic body size and obligate filter feeding mechanisms have evolved in multiple vertebrate lineages (mammals and fishes), intermittent ram (lunge) filter feeding is unique to a specific family of baleen whales: rorquals. Lunge feeding is a high cost, high benefit feeding mechanism that requires the integration of unsteady locomotion (i.e., accelerations and maneuvers); the impact of scale on the biomechanics and energetics of this foraging mode continues to be the subject of intense study. The goal of our investigation was to use a combination of multi-sensor tags paired with UAS footage to determine the impact of morphometrics such as body size on kinematic lunging parameters such as fluking timing, maximum lunging speed, and deceleration during the engulfment period for a range of species from minke to blue whales. Our results show that, in the case of krill-feeding lunges and regardless of size, animals exhibit a skewed gradient between powered and fully unpowered engulfment, with fluking generally ending at the point of both the maximum lunging speed and mouth opening. In all cases, the small amounts of propulsive thrust generated by the tail were unable to overcome the high drag forces experienced during engulfment. Assuming this thrust to be minimal, we predicted the minimum speed of lunging across scale. To minimize the energetic cost of lunge feeding, hydrodynamic theory predicts slower lunge feeding speeds regardless of body size, with a lower boundary set by the ability of the prey to avoid capture. We used empirical data to test this theory and instead found that maximum foraging speeds remain constant and high (∼4 m s-1) across body size, even as higher speeds result in lower foraging efficiency. Regardless, we found an increasing relationship between body size and this foraging efficiency, estimated as the ratio of energetic gain from prey to energetic cost. This trend held across timescales ranging from a single lunge to a single day and suggests that larger whales are capturing more prey-and more energy-at a lower cost.

Blue whales increase feeding rates at fine-scale ocean features.

Marine predators face the challenge of reliably finding prey that is patchily distributed in space and time. Predators make movement decisions at multiple spatial and temporal scales, yet we have a limited understanding of how habitat selection at multiple scales translates into foraging performance. In the ocean, there is mounting evidence that submesoscale (i.e. less than 100 km) processes drive the formation of dense prey patches that should hypothetically provide feeding hot spots and increase predator foraging success. Here, we integrated environmental remote-sensing with high-resolution animal-borne biologging data to evaluate submesoscale surface current features in relation to the habitat selection and foraging performance of blue whales in the California Current System. Our study revealed a consistent functional relationship in which blue whales disproportionately foraged within dynamic aggregative submesoscale features at both the regional and feeding site scales across seasons, regions and years. Moreover, we found that blue whale feeding rates increased in areas with stronger aggregative features, suggesting that these features indicate areas of higher prey density. The use of fine-scale, dynamic features by foraging blue whales underscores the need to take these features into account when designating critical habitat and may help inform strategies to mitigate the impacts of human activities for the species.

Baleen whale inhalation variability revealed using animal-borne video tags.

Empirical metabolic rate and oxygen consumption estimates for free-ranging whales have been limited to counting respiratory events at the surface. Because these observations were limited and generally viewed from afar, variability in respiratory properties was unknown and oxygen consumption estimates assumed constant breath-to-breath tidal volume and oxygen uptake. However, evidence suggests that cetaceans in human care vary tidal volume and breathing frequency to meet aerobic demand, which would significantly impact energetic estimates if the findings held in free-ranging species. In this study, we used suction cup-attached video tags positioned posterior to the nares of two humpback whales (Megaptera novaeangliae) and four Antarctic minke whales (Balaenoptera bonaerensis) to measure inhalation duration, relative nares expansion, and maximum nares expansion. Inhalation duration and nares expansion varied between and within initial, middle, and terminal breaths of surface sequences between dives. The initial and middle breaths exhibited the least variability and had the shortest durations and smallest nares expansions. In contrast, terminal breaths were highly variable, with the longest inhalation durations and the largest nares expansions. Our results demonstrate breath-to-breath variability in duration and nares expansion, suggesting differential oxygen exchange in each breath during the surface interval. With future validation, inhalation duration or nares area could be used alongside respiratory frequency to improve oxygen consumption estimates by accounting for breath-to-breath variation in wild whales.

An accelerometer-derived ballistocardiogram method for detecting heart rate in free-ranging marine mammals.

Physio-logging methods, which use animal-borne devices to record physiological variables, are entering a new era driven by advances in sensor development. However, existing datasets collected with traditional bio-loggers, such as accelerometers, still contain untapped eco-physiological information. Here, we present a computational method for extracting heart rate from high-resolution accelerometer data using a ballistocardiogram. We validated our method with simultaneous accelerometer-electrocardiogram tag deployments in a controlled setting on a killer whale (Orcinus orca) and demonstrate the predictions correspond with previously observed cardiovascular patterns in a blue whale (Balaenoptera musculus), including the magnitude of apneic bradycardia and increase in heart rate prior to and during ascent. Our ballistocardiogram method may be applied to mine heart rates from previously collected accelerometery data and expand our understanding of comparative cardiovascular physiology.

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.

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.

Too big to study? The biologging approach to understanding the behavioural energetics of ocean giants.

Wild animals are under selective pressure to optimise energy budgets; therefore, quantifying energy expenditure, intake and allocation to specific activities is important if we are to understand how animals survive in their environment. One approach toward estimating energy budgets has involved measuring oxygen consumption rates under controlled conditions and constructing allometric relationships across species. However, studying 'giant' marine vertebrates (e.g. pelagic sharks, whales) in this way is logistically difficult or impossible. An alternative approach involves the use of increasingly sophisticated electronic tags that have allowed recordings of behaviour, internal states and the surrounding environment of marine animals. This Review outlines how we could study the energy expenditure and intake of free-living ocean giants using this 'biologging' technology. There are kinematic, physiological and theoretical approaches for estimating energy expenditure, each of which has merits and limitations. Importantly, tag-derived energy proxies can hardly be validated against oxygen consumption rates for giant species. The proxies are thus qualitative, rather than quantitative, estimates of energy expenditure, and have more limited utilities. Despite this limitation, these proxies allow us to study the energetics of ocean giants in their behavioural context, providing insight into how these animals optimise their energy budgets under natural conditions. We also outline how information on energy intake and foraging behaviour can be gained from tag data. These methods are becoming increasingly important owing to the natural and anthropogenic environmental changes faced by ocean giants that can alter their energy budgets, fitness and, ultimately, population sizes.

Scaling of oscillatory kinematics and Froude efficiency in baleen whales.

High efficiency lunate-tail swimming with high-aspect-ratio lifting surfaces has evolved in many vertebrate lineages, from fish to cetaceans. Baleen whales (Mysticeti) are the largest swimming animals that exhibit this locomotor strategy, and present an ideal study system to examine how morphology and the kinematics of swimming scale to the largest body sizes. We used data from whale-borne inertial sensors coupled with morphometric measurements from aerial drones to calculate the hydrodynamic performance of oscillatory swimming in six baleen whale species ranging in body length from 5 to 25 m (fin whale, Balaenoptera physalus; Bryde's whale, Balaenoptera edeni; sei whale, Balaenoptera borealis; Antarctic minke whale, Balaenoptera bonaerensis; humpback whale, Megaptera novaeangliae; and blue whale, Balaenoptera musculus). We found that mass-specific thrust increased with both swimming speed and body size. Froude efficiency, defined as the ratio of useful power output to the rate of energy input ( Sloop, 1978), generally increased with swimming speed but decreased on average with increasing body size. This finding is contrary to previous results in smaller animals, where Froude efficiency increased with body size. Although our empirically parameterized estimates for swimming baleen whale drag were higher than those of a simple gliding model, oscillatory locomotion at this scale exhibits generally high Froude efficiency as in other adept swimmers. Our results quantify the fine-scale kinematics and estimate the hydrodynamics of routine and energetically expensive swimming modes at the largest scale.

Microplastics and microfibers in surface waters of Monterey Bay National Marine Sanctuary, California.

Despite a recent report of high concentrations of microplastics and microfibers in the mesopelagic waters of Monterey Bay National Marine Sanctuary (MBNMS), little is known about these particles in surface waters. From 2017 to 2019, we sampled two nearshore and two offshore locations within MBNMS using a manta trawl and analyzed these samples for microplastics and microfibers. We found an average concentration of 1.32 ± 0.70 (SE) particles per m3. We found the highest concentration of particles closest to shore, and the lowest concentration above the remote Davidson Seamount. Fiber-like debris was more common in offshore, as compared to nearshore, sites. Overall, particles in our samples were primarily buoyant synthetic polymers, including polypropylene and polyethylene. Our results provide baseline data on the degree of microplastic and microfiber pollution in MBNMS surface waters and confirm that this pollution can be found in waters from the surface to at least 1000 m depth.

Context-dependent variability in the predicted daily energetic costs of disturbance for blue whales.

Assessing the long-term consequences of sub-lethal anthropogenic disturbance on wildlife populations requires integrating data on fine-scale individual behavior and physiology into spatially and temporally broader, population-level inference. A typical behavioral response to disturbance is the cessation of foraging, which can be translated into a common metric of energetic cost. However, this necessitates detailed empirical information on baseline movements, activity budgets, feeding rates and energy intake, as well as the probability of an individual responding to the disturbance-inducing stressor within different exposure contexts. Here, we integrated data from blue whales (Balaenoptera musculus) experimentally exposed to military active sonar signals with fine-scale measurements of baseline behavior over multiple days or weeks obtained from accelerometry loggers, telemetry tracking and prey sampling. Specifically, we developed daily simulations of movement, feeding behavior and exposure to localized sonar events of increasing duration and intensity and predicted the effects of this disturbance source on the daily energy intake of an individual. Activity budgets and movements were highly variable in space and time and among individuals, resulting in large variability in predicted energetic intake and costs. In half of our simulations, an individual's energy intake was unaffected by the simulated source. However, some individuals lost their entire daily energy intake under brief or weak exposure scenarios. Given this large variation, population-level models will have to assess the consequences of the entire distribution of energetic costs, rather than only consider single summary statistics. The shape of the exposure-response functions also strongly influenced predictions, reinforcing the need for contextually explicit experiments and improved mechanistic understanding of the processes driving behavioral and physiological responses to disturbance. This study presents a robust approach for integrating different types of empirical information to assess the effects of disturbance at spatio-temporal and ecological scales that are relevant to management and conservation.

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.

Animal-Borne Metrics Enable Acoustic Detection of Blue Whale Migration.

Linking individual and population scales is fundamental to many concepts in ecology [1], including migration [2, 3]. This behavior is a critical [4] yet increasingly threatened [5] part of the life history of diverse organisms. Research on migratory behavior is constrained by observational scale [2], limiting ecological understanding and precise management of migratory populations in expansive, inaccessible marine ecosystems [6]. This knowledge gap is magnified for dispersed oceanic predators such as endangered blue whales (Balaenoptera musculus). As capital breeders, blue whales migrate vast distances annually between foraging and breeding grounds, and their population fitness depends on synchrony of migration with phenology of prey populations [7, 8]. Despite previous studies of individual-level blue whale vocal behavior via bio-logging [9, 10] and population-level acoustic presence via passive acoustic monitoring [11], detection of the life history transition from foraging to migration remains challenging. Here, we integrate direct high-resolution measures of individual behavior and continuous broad-scale acoustic monitoring of regional song production (Figure 1A) to identify an acoustic signature of the transition from foraging to migration in the Northeast Pacific population. We find that foraging blue whales sing primarily at night, whereas migratory whales sing primarily during the day. The ability to acoustically detect population-level transitions in behavior provides a tool to more comprehensively study the life history, fitness, and plasticity of population behavior in a dispersed, capital breeding population. Real-time detection of this behavioral signal can also inform dynamic management efforts [12] to mitigate anthropogenic threats to this endangered population [13, 14]).

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.