Jeremy A. Goldbogen

Kinematics of foraging dives and lunge-feeding in fin whales

SUMMARY Fin whales are among the largest predators on earth, yet little is known about their foraging behavior at depth. These whales obtain their prey by lunge-feeding, an extraordinary biomechanical event where large amounts of water and prey are engulfed and filtered. This process entails a high energetic cost that effectively decreases dive duration and increases post-dive recovery time. To examine the body mechanics of fin whales during foraging dives we attached high-resolution digital tags, equipped with a hydrophone, a depth gauge and a dual-axis accelerometer, to the backs of surfacing fin whales in the Southern California Bight. Body pitch and roll were estimated by changes in static gravitational acceleration detected by orthogonal axes of the accelerometer, while higher frequency, smaller amplitude oscillations in the accelerometer signals were interpreted as bouts of active fluking. Instantaneous velocity of the whale was determined from the magnitude of turbulent flow noise measured by the hydrophone and confirmed by kinematic analysis. Fin whales employed gliding gaits during descent, executed a series of lunges at depth and ascended to the surface by steady fluking. Our examination of body kinematics at depth reveals variable lunge-feeding behavior in the context of distinct kinematic modes, which exhibit temporal coordination of rotational torques with translational accelerations. Maximum swimming speeds during lunges match previous estimates of the flow-induced pressure needed to completely expand the buccal cavity during feeding.

Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density.

SUMMARY Lunge feeding by rorqual whales (Balaenopteridae) is associated with a high energetic cost that decreases diving capacity, thereby limiting access to dense prey patches at depth. Despite this cost, rorquals exhibit high rates of lipid deposition and extremely large maximum body size. To address this paradox, we integrated kinematic data from digital tags with unsteady hydrodynamic models to estimate the energy budget for lunges and foraging dives of blue whales (Balaenoptera musculus), the largest rorqual and living mammal. Our analysis suggests that, despite the large amount of mechanical work required to lunge feed, a large amount of prey and, therefore, energy is obtained during engulfment. Furthermore, we suggest that foraging efficiency for blue whales is significantly higher than for other marine mammals by nearly an order of magnitude, but only if lunges target extremely high densities of krill. The high predicted efficiency is attributed to the enhanced engulfment capacity, rapid filter rate and low mass-specific metabolic rate associated with large body size in blue whales. These results highlight the importance of high prey density, regardless of prey patch depth, for efficient bulk filter feeding in baleen whales and may explain some diel changes in foraging behavior in rorqual whales.

Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge

SUMMARY Lunge feeding in rorqual whales is a drag-based feeding mechanism that is thought to entail a high energetic cost and consequently limit the maximum dive time of these extraordinarily large predators. Although the kinematics of lunge feeding in fin whales supports this hypothesis, it is unclear whether respiratory compensation occurs as a consequence of lunge-feeding activity. We used high-resolution digital tags on foraging humpback whales (Megaptera novaengliae) to determine the number of lunges executed per dive as well as respiratory frequency between dives. Data from two whales are reported, which together performed 58 foraging dives and 451 lunges. During one study, we tracked one tagged whale for approximately 2 h and examined the spatial distribution of prey using a digital echosounder. These data were integrated with the dive profile to reveal that lunges are directed toward the upper boundary of dense krill aggregations. Foraging dives were characterized by a gliding descent, up to 15 lunges at depth, and an ascent powered by steady swimming. Longer dives were required to perform more lunges at depth and these extended apneas were followed by an increase in the number of breaths taken after a dive. Maximum dive durations during foraging were approximately half of those previously reported for singing (i.e. non-feeding) humpback whales. At the highest lunge frequencies (10 to 15 lunges per dive), respiratory rate was at least threefold higher than that of singing humpback whales that underwent a similar degree of apnea. These data suggest that the high energetic cost associated with lunge feeding in blue and fin whales also occurs in intermediate sized rorquals.

Anatomic geometry of sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris).

This study uses remote imaging technology to quantify, compare, and contrast the cephalic anatomy between a neonate female and a young adult male Cuviers beaked whale. Primary results reveal details of anatomic geometry with implications for acoustic function and diving. Specifically, we describe the juxtaposition of the large pterygoid sinuses, a fibrous venous plexus, and a lipid-rich pathway that connects the acoustic environment to the bony ear complex. We surmise that the large pterygoid air sinuses are essential adaptations for maintaining acoustic isolation and auditory acuity of the ears at depth. In the adult male, an acoustic waveguide lined with pachyosteosclerotic bones is apparently part of a novel transmission pathway for outgoing biosonar signals. Substitution of dense tissue boundaries where we normally find air sacs in delphinoids appears to be a recurring theme in deep-diving beaked whales and sperm whales. The anatomic configuration of the adult male Ziphius forehead resembles an upside-down sperm whale nose and may be its functional equivalent, but the homologous relationships between forehead structures are equivocal.

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.

Integrative Approaches to the Study of Baleen Whale Diving Behavior, Feeding Performance, and Foraging Ecology

For many marine organisms, especially large whales that cannot be studied in laboratory settings, our ability to obtain basic behavioral and physiological data is limited, because these organisms occupy offshore habitats and spend a majority of their time underwater. A class of multisensor, suction-cup-attached archival tags has revolutionized the study of large baleen whales, particularly with respect to the predatory strategies used by these gigantic bulk filter feeders to exploit abundant oceanic resources. By integrating these data with those from other disciplines, researchers have uncovered a diverse and extraordinary set of underwater behaviors, ranging from acrobatic diving maneuvers to extreme feeding events during which whales engulf volumes of prey-laden water that are much larger than their own body. This research framework not only improves our knowledge of the individual performance and behavior of these keystone predators but also informs our ability to understand the dynamics of complex marine ecosystems.

Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus

Lunge-feeding in rorqual whales represents the largest biomechanical event on Earth and one of the most extreme feeding methods among aquatic vertebrates. By accelerating to high speeds and by opening their mouth to large gape angles, these whales generate the water pressure required to expand their mouth around a large volume of prey-laden water. Such large influx is facilitated by highly extensible ventral groove blubber (VGB) associated with the walls of the throat (buccal cavity). Based on the mechanical properties of this tissue, previous studies have assumed lunge-feeding to be an entirely passive process, where the flow-induced pressure driving the expansion of the VGB is met with little resistance. Such compliant engulfment would be facilitated by the compliant properties of the VGB that have been measured on dead specimens. However, adjoining the ventral blubber are several layers of well-developed muscle embedded with mechanoreceptors, thereby suggesting a capability to gauge the magnitude of engulfed water and use eccentric muscle action to control the flux of water into the mouth. An unsteady hydrodynamic model of fin whale lunge-feeding is presented here to test whether engulfment is exclusively passive and compliant or involves muscle action. The model is based on the explicit simulation of the engulfed water as it interacts with the buccal cavity walls of the whale, under different heuristically motivated cavity forces. Our results, together with their comparison with velocity data collected in the field, suggest that adult rorquals actively push engulfed water forward from the very onset of mouth opening in order to successfully complete a lunge. Interestingly, such an action involves a reflux of the engulfed mass rather than the oft-assumed rebound, which would occur mainly at the very end of a lunge sequence dominated by compliant engulfment. Given the great mass of the engulfed water, reflux creation adds a significant source of hydrodynamic drag to the lunge process, but with the benefit of helping to circumvent the problem of removing prey from baleen by enhancing the efficiency of cross-flow filtration after mouth closing. Reflux management for a successful lunge will therefore demand well-coordinated muscular actions of the tail, mouth and ventral cavity.

Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales

Rorqual whales (Balaenopteridae) represent not only some of the largest animals of all time, but also exhibit a wide range in intraspecific and interspecific body size. Balaenopterids are characterized by their extreme lunge-feeding behaviour, a dynamic process that involves the engulfment of a large volume of prey-laden water at a high energetic cost. To investigate the consequences of scale and morphology on lunge-feeding performance, we determined allometric equations for fin whale body dimensions and engulfment capacity. Our analysis demonstrates that larger fin whales have larger skulls and larger buccal cavities relative to body size. Together, these data suggest that engulfment volume is also allometric, increasing with body length as . The positive allometry of the skull is accompanied by negative allometry in the tail region. The relative shortening of the tail may represent a trade-off for investing all growth-related resources in the anterior region of the body. Although enhanced engulfment volume will increase foraging efficiency, the work (energy) required to accelerate the engulfed water mass during engulfment will be relatively higher in larger rorquals. If the mass-specific energetic cost of a lunge increases with body size, it will have major consequences for rorqual foraging ecology and evolution.

Underwater acrobatics by the world's largest predator: 360° rolling manoeuvres by lunge-feeding blue whales

The extreme body size of blue whales requires a high energy intake and therefore demands efficient foraging strategies. As an obligate lunge feeder on aggregations of small zooplankton, blue whales engulf a large volume of prey-laden water in a single, rapid gulp. The efficiency of this feeding mechanism is strongly dependent on the amount of prey that can be captured during each lunge, yet food resources tend to be patchily distributed in both space and time. Here, we measured the three-dimensional kinematics and foraging behaviour of blue whales feeding on krill, using suction-cup attached multi-sensor tags. Our analyses revealed 360° rolling lunge-feeding manoeuvres that reorient the body and position the lower jaws so that a krill patch can be engulfed with the whales body inverted. We also recorded these rolling behaviours when whales were in a searching mode in between lunges, suggesting that this behaviour also enables the whale to visually process the prey field and maximize foraging efficiency by surveying for the densest prey aggregations. These results reveal the complex manoeuvrability that is required for large rorqual whales to exploit prey patches and highlight the need to fully understand the three-dimensional interactions between predator and prey in the natural environment.

Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size

Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations.