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.
We investigated the possibility that tendons that normally experience relatively high stresses and function as springs during locomotion, such as digital flexors, might develop different mechanical properties from those that experience only relatively low stresses, such as digital extensors. At birth the digital flexor and extensor tendons of pigs have identical mechanical properties, exhibiting higher extensibility and mechanical hysteresis and lower elastic modulus, tensile strength, and elastic energy storage capability than adult tendons. With growth and aging these tendons become much stronger, stiffer, less extensible, and more resilient than at birth. Furthermore, these alterations in elastic properties occur to a significantly greater degree in the high-load-bearing flexors than in the low-stress extensors. At maturity the pig digital flexor tendons have twice the tensile strength and elastic modulus but only half the strain energy dissipation of the corresponding extensor tendons. A morphometric analysis of the digital muscles provides an estimate of maximal in vivo tendon stresses and suggests that the muscle-tendon unit of the digital flexor is designed to function as an elastic energy storage element whereas that of the digital extensor is not. Thus the differences in material properties between mature flexor and extensor tendons are correlated with their physiological functions, i.e., the flexor is much better suited to act as an effective biological spring than is the extensor.
There were several errors published in J. Exp. Biol. 214,[131][132][133][134][135][136][137][138][139][140][141][142][143][144][145][146] In the first line of the 'Kinematics of diving and lunge feeding' section of the Results (p. 134), the number of blue whales that were tagged was incorrectly given as 265 -the correct number is 25.In Fig.A1 (p. 142), two mistakes were introduced. In the 'Energy in' column, krill energy density should have been given as 4600kJkg -1 (rather than 4600kJg -1 ). Also in the 'Energy in' column, the units were missing from the 'Energy obtained from ingested krill'; this should have read 'Energy obtained from ingested krill 4,868,640 kJ'.The correct version of the figure is shown below. Energy in Energy outShape and engulfment drag = 569 kJ Pre-engulfment acceleration = 376 kJ Efficiency = 77 699 ErratumIn Table 3, the data from the 'Net energy gain' column were inadvertently repeated in the 'Energy loss, total' column. The correct version of Table 3, with the original data for the 'Energy loss, total' column, is shown below.We apologise sincerely to authors and readers for any inconvenience these errors may have caused.
Fin whales Balaenoptera physalus exhibit one of the most extreme feeding methods among aquatic vertebrates. Fin whales, and other rorquals (Balaenopteridae), lunge with their mouth fully agape, thereby generating dynamic pressure to stretch their mouth around a large volume of prey-laden water, which is then filtered by racks of baleen. Despite their large body size, fin whales appear to be limited to short dive durations, likely because of the energetic cost associated with large accelerations of the body during several lunges at depth. Here, we incorporate kinematic data from high-resolution digital tags and morphological data of the engulfment apparatus in a simple mechanical model to estimate the drag acting on a lunge-feeding fin whale. This model also allowed us to quantify the amount of water and prey obtained in a single lunge. Our analysis suggests that the reconfiguration and expansion of the buccal cavity enables an adult fin whale to engulf approximately 60 to 82 m 3 of water, a volume greater than its entire body. This large engulfment capacity, however, comes at a high cost because the drag, work against drag, and drag coefficient dramatically increase over the course of a lunge. As a result, kinetic energy is rapidly dissipated from the body, and each subsequent lunge requires acceleration from rest. Despite this high cost, living balaenopterids are not only among the largest animals on earth, but are relatively speciose and exhibit diverse prey preferences. Given this ecological diversity, we frame our results in an evolutionary context, and address the implications of our results for the origin of lunge feeding.
SUMMARYLunge 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.
This paper considers the structural properties of muscle-tendon units in the hindlimbs of mammals as a function of body mass. Morphometric analysis of the ankle extensors, digital flexors, and digital extensors from 35 quadrupedal species, ranging in body mass from 0.04 to 545 kg, was carried out. Tendon dimensions scale nearly isometrically, as does muscle mass. The negative allometry of muscle fiber length results in positive allometric scaling of muscle cross-sectional areas in all but digital extensors. Maximum muscle forces are predicted to increase allometrically, with mass exponents as high as 0.91 in the plantaris, but nearly isometrically (0.69) in the digital extensors. Thus the maximum amount of stress a tendon may experience in vivo, as indicated by the ratio of muscle and tendon cross-sectional areas, increases with body mass in digital flexors and ankle extensors. Consequently, the capacity for elastic energy storage scales with positive allometry in these tendons but is isometric in the digital extensors, which probably do not function as springs in normal locomotion. These results suggest that the springlike tendons of large mammals can potentially store more elastic strain energy than those of smaller mammals because their disproportionately stronger muscles can impose higher tendon stresses.
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 wellcoordinated muscular actions of the tail, mouth and ventral cavity.
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