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.

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.

Predator-informed looming stimulus experiments reveal how large filter feeding whales capture highly maneuverable forage fish.

The unique engulfment filtration strategy of microphagous rorqual whales has evolved relatively recently (<5 Ma) and exploits extreme predator/prey size ratios to overcome the maneuverability advantages of swarms of small prey, such as krill. Forage fish, in contrast, have been engaged in evolutionary arms races with their predators for more than 100 million years and have performance capabilities that suggest they should easily evade whale-sized predators, yet they are regularly hunted by some species of rorqual whales. To explore this phenomenon, we determined, in a laboratory setting, when individual anchovies initiated escape from virtually approaching whales, then used these results along with in situ humpback whale attack data to model how predator speed and engulfment timing affected capture rates. Anchovies were found to respond to approaching visual looming stimuli at expansion rates that give ample chance to escape from a sea lion-sized predator, but humpback whales could capture as much as 30-60% of a school at once because the increase in their apparent (visual) size does not cross their prey's response threshold until after rapid jaw expansion. Humpback whales are, thus, incentivized to delay engulfment until they are very close to a prey school, even if this results in higher hydrodynamic drag. This potential exaptation of a microphagous filter feeding strategy for fish foraging enables humpback whales to achieve 7× the energetic efficiency (per lunge) of krill foraging, allowing for flexible foraging strategies that may underlie their ecological success in fluctuating oceanic conditions.

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.

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.

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.

Memory and resource tracking drive blue whale migrations.

In terrestrial systems, the green wave hypothesis posits that migrating animals can enhance foraging opportunities by tracking phenological variation in high-quality forage across space (i.e., "resource waves"). To track resource waves, animals may rely on proximate cues and/or memory of long-term average phenologies. Although there is growing evidence of resource tracking in terrestrial migrants, such drivers remain unevaluated in migratory marine megafauna. Here we present a test of the green wave hypothesis in a marine system. We compare 10 years of blue whale movement data with the timing of the spring phytoplankton bloom resulting in increased prey availability in the California Current Ecosystem, allowing us to investigate resource tracking both contemporaneously (response to proximate cues) and based on climatological conditions (memory) during migrations. Blue whales closely tracked the long-term average phenology of the spring bloom, but did not track contemporaneous green-up. In addition, blue whale foraging locations were characterized by low long-term habitat variability and high long-term productivity compared with contemporaneous measurements. Results indicate that memory of long-term average conditions may have a previously underappreciated role in driving migratory movements of long-lived species in marine systems, and suggest that these animals may struggle to respond to rapid deviations from historical mean environmental conditions. Results further highlight that an ecological theory of migration is conserved across marine and terrestrial systems. Understanding the drivers of animal migration is critical for assessing how environmental changes will affect highly mobile fauna at a global scale.

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.

Lunge Feeding in Rorqual Whales.

The largest animals are baleen filter feeders that exploit large aggregations of small-bodied plankton. Although this feeding mechanism has evolved multiple times in marine vertebrates, rorqual whales exhibit a distinct lunge filter feeding mode that requires extreme physiological adaptations-most of which remain poorly understood. Here, we review the biomechanics of the lunge feeding mechanism in rorqual whales that underlies their extraordinary foraging performance and gigantic body size.

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.

Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar.

This study measured the degree of behavioral responses in blue whales (Balaenoptera musculus) to controlled noise exposure off the southern California coast. High-resolution movement and passive acoustic data were obtained from non-invasive archival tags (n=42) whereas surface positions were obtained with visual focal follows. Controlled exposure experiments (CEEs) were used to obtain direct behavioral measurements before, during and after simulated and operational military mid-frequency active sonar (MFAS), pseudorandom noise (PRN) and controls (no noise exposure). For a subset of deep-feeding animals (n=21), active acoustic measurements of prey were obtained and used as contextual covariates in response analyses. To investigate potential behavioral changes within individuals as a function of controlled noise exposure conditions, two parallel analyses of time-series data for selected behavioral parameters (e.g. diving, horizontal movement and feeding) were conducted. This included expert scoring of responses according to a specified behavioral severity rating paradigm and quantitative change-point analyses using Mahalanobis distance statistics. Both methods identified clear changes in some conditions. More than 50% of blue whales in deep-feeding states responded during CEEs, whereas no changes in behavior were identified in shallow-feeding blue whales. Overall, responses were generally brief, of low to moderate severity, and highly dependent on exposure context such as behavioral state, source-to-whale horizontal range and prey availability. Response probability did not follow a simple exposure-response model based on received exposure level. These results, in combination with additional analytical methods to investigate different aspects of potential responses within and among individuals, provide a comprehensive evaluation of how free-ranging blue whales responded to mid-frequency military sonar.

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.

A Dynamic State Model of Migratory Behavior and Physiology to Assess the Consequences of Environmental Variation and Anthropogenic Disturbance on Marine Vertebrates.

Integrating behavior and physiology is critical to formulating new hypotheses on the evolution of animal life-history strategies. Migratory capital breeders acquire most of the energy they need to sustain migration, gestation, and lactation before parturition. Therefore, when predicting the impact of environmental variation on such species, a mechanistic understanding of the physiology of their migratory behavior is required. Using baleen whales as a model system, we developed a dynamic state variable model that captures the interplay among behavioral decisions, energy, reproductive needs, and the environment. We applied the framework to blue whales (Balaenoptera musculus) in the eastern North Pacific Ocean and explored the effects of environmental and anthropogenic perturbations on female reproductive success. We demonstrate the emergence of migration to track prey resources, enabling us to quantify the trade-offs among capital breeding, body condition, and metabolic expenses. We predict that periodic climatic oscillations affect reproductive success less than unprecedented environmental changes do. The effect of localized, acute anthropogenic impacts depended on whales' behavioral response to the disturbance; chronic, but weaker, disturbances had little effect on reproductive success. Because we link behavior and vital rates by modeling individuals' energetic budgets, we provide a general framework to investigate the ecology of migration and assess the population consequences of disturbance, while identifying critical knowledge gaps.

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.

Discovery of a sensory organ that coordinates lunge feeding in rorqual whales.

Top ocean predators have evolved multiple solutions to the challenges of feeding in the water. At the largest scale, rorqual whales (Balaenopteridae) engulf and filter prey-laden water by lunge feeding, a strategy that is unique among vertebrates. Lunge feeding is facilitated by several morphological specializations, including bilaterally separate jaws that loosely articulate with the skull, hyper-expandable throat pleats, or ventral groove blubber, and a rigid y-shaped fibrocartilage structure branching from the chin into the ventral groove blubber. The linkages and functional coordination among these features, however, remain poorly understood. Here we report the discovery of a sensory organ embedded within the fibrous symphysis between the unfused jaws that is present in several rorqual species, at both fetal and adult stages. Vascular and nervous tissue derived from the ancestral, anterior-most tooth socket insert into this organ, which contains connective tissue and papillae suspended in a gel-like matrix. These papillae show the hallmarks of a mechanoreceptor, containing nerves and encapsulated nerve termini. Histological, anatomical and kinematic evidence indicate that this sensory organ responds to both the dynamic rotation of the jaws during mouth opening and closure, and ventral groove blubber expansion through direct mechanical linkage with the y-shaped fibrocartilage structure. Along with vibrissae on the chin, providing tactile prey sensation, this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment, a paradigm that is consistent with unsteady hydrodynamic models and tag data from lunge-feeding rorquals. Despite the antiquity of unfused jaws in baleen whales since the late Oligocene (∼23-28 million years ago), this organ represents an evolutionary novelty for rorquals, based on its absence in all other lineages of extant baleen whales. This innovation has a fundamental role in one of the most extreme feeding methods in aquatic vertebrates, which facilitated the evolution of the largest vertebrates ever.

Physical trade-offs shape the evolution of buoyancy control in sharks.

Buoyancy control is a fundamental aspect of aquatic life that has major implications for locomotor performance and ecological niche. Unlike terrestrial animals, the densities of aquatic animals are similar to the supporting fluid, thus even small changes in body density may have profound effects on locomotion. Here, we analysed the body composition (lipid versus lean tissue) of 32 shark species to study the evolution of buoyancy. Our comparative phylogenetic analyses indicate that although lean tissue displays minor positive allometry, liver volume exhibits pronounced positive allometry, suggesting that larger sharks evolved bulkier body compositions by adding lipid tissue to lean tissue rather than substituting lean for lipid tissue, particularly in the liver. We revealed a continuum of buoyancy control strategies that ranged from more buoyant sharks with larger livers in deeper ecosystems to relatively denser sharks with small livers in epipelagic habitats. Across this eco-morphological spectrum, our hydrodynamic modelling suggests that neutral buoyancy yields lower drag and more efficient steady swimming, whereas negative buoyancy may be more efficient during accelerated movements. The evolution of buoyancy control in sharks suggests that ecological and physiological factors mediate the selective pressures acting on these traits along two major gradients, body size and habitat depth.

Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics.

Vertebrates have evolved to gigantic sizes repeatedly over the past 250 Myr, reaching their extreme in today's baleen whales (Mysticeti). Hypotheses for the evolution of exceptionally large size in mysticetes range from niche partitioning to predator avoidance, but there has been no quantitative examination of body size evolutionary dynamics in this clade and it remains unclear when, why or how gigantism evolved. By fitting phylogenetic macroevolutionary models to a dataset consisting of living and extinct species, we show that mysticetes underwent a clade-wide shift in their mode of body size evolution during the Plio-Pleistocene. This transition, from Brownian motion-like dynamics to a trended random walk towards larger size, is temporally linked to the onset of seasonally intensified upwelling along coastal ecosystems. High prey densities resulting from wind-driven upwelling, rather than abundant resources alone, are the primary determinant of efficient foraging in extant mysticetes and Late Pliocene changes in ocean dynamics may have provided an ecological pathway to gigantism in multiple independent lineages.