Search

The evolution of lunge feeding in rorqual whales was associated with the evolution of several unique morphological features that include non-synovial ligamentous temporomandibular joints, a tongue that can invert and extend backward to the umbilicus, walls of the oral cavity that can dramatically expand, and muscles and nerves that are stretchy. Also, among the acquired features was an enlargement of the rostral end of the soft palate into an oral plug that occludes the opening between the oral cavity and pharynx and prevents water incursion into the pharynx during the engulfment phase of a feeding lunge. During this engulfment phase of a lunge, the volume of water entering the oral cavity can exceed the volume of the whale itself. Here, using dissection of fetuses and adults and a magnetic resonance imaging dataset of a fetus, we examine the detailed anatomy of the soft palate in fin whales. We describe several innovative features relative to other mammals, including changes in the attachment and positions of the major extrinsic muscles of the palate, alterations in the morphology of the pterygoid processes related to the palate and pharynx, and the presence of distinct muscle layers in the part of the palate caudal to the oral plug. Based on the anatomy, we present a model for how the soft palate is positioned at rest, and how it functions during feeding, breathing, and swallowing., Competing Interests: The authors declare no competing interests., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Lunge feeding rorqual whales feed by engulfing a volume of prey laden water that can be as large as their own body. Multiple feeding lunges occur during a single foraging dive and the time between each lunge can be as short as 30 s (Goldbogen et al. 2013). During this short inter-lunge time, water is filtered out through baleen to concentrate prey in the oral cavity, and then the prey is swallowed prior to initiating the next lunge. Prey density in the ocean varies greatly, and despite the potential of swallowing a massive volume of concentrated prey as a slurry, the esophagus of rorqual whales has been anecdotally described as unexpectedly narrow with a limited capacity to expand. How rorquals swallow large quantities of food down a narrow esophagus during a limited inter-lunge time remains unknown. Here, we show that the small diameter muscular esophagus in the fin whale is optimized to transport a slurry of food to the stomach. A thick wall of striated muscle occurs at the pharyngeal end of the esophagus which, together with the muscular wall of the pharynx, may generate a pressure head for transporting the food down the esophagus to the stomach as a continuous stream rather than separating the food into individual boluses swallowed separately. This simple model is consistent with estimates of prey density and stomach capacity. Rorquals may be the only animals that capture a volume of food too large to swallow as a single intact bolus without oral processing, so the adaptations of the esophagus are imperative for transporting these large volumes of concentrated food to the stomach during a time-limited dive involving multiple lunges., Competing Interests: The authors declare no competing interests., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Cetaceans have massive vascular plexuses (retia mirabilia) whose function is unknown. All cerebral blood flow passes through these retia, and we hypothesize that they protect cetacean brains from locomotion-generated pulsatile blood pressures. We propose that cetaceans have evolved a pulse-transfer mechanism that minimizes pulsatility in cerebral arterial-to-venous pressure differentials without dampening the pressure pulses themselves. We tested this hypothesis using a computational model based on morphology from 11 species and found that the large arterial capacitance in the retia, coupled with the small extravascular capacitance in the cranium and vertebral canal, could protect the cerebral vasculature from 97% of systemic pulsatility. Evolution of the retial complex in cetaceans-likely linked to the development of dorsoventral fluking-offers a distinctive solution to adverse locomotion-generated vascular pulsatility.

The skull of a woodpecker is hypothesized to serve as a shock absorber that minimizes the harmful deceleration of its brain upon impact into trees 1-11 and has inspired the engineering of shock-absorbing materials 12-15 and tools, such as helmets. 16 However, this hypothesis remains paradoxical since any absorption or dissipation of the head's kinetic energy by the skull would likely impair the bird's hammering performance 4 and is therefore unlikely to have evolved by natural selection. In vivo quantification of impact decelerations during pecking in three woodpecker species and biomechanical models now show that their cranial skeleton is used as a stiff hammer to enhance pecking performance, and not as a shock-absorbing system to protect the brain. Numerical simulations of the effect of braincase size and shape on intracranial pressure indicate that the woodpeckers' brains are still safe below the threshold of concussions known for primate brains. These results contradict the currently prevailing conception of the adaptive evolution of cranial function in one of nature's most spectacular behaviors. VIDEO ABSTRACT., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 Elsevier Inc. All rights reserved.)

The apex or apical region of the cochlear spiral within the inner ear encodes for low-frequency sounds. The disposition of sensory hair cells on the organ of Corti is largely variable in the apical region of mammals, and it does not necessarily follow the typical three-row pattern of outer hair cells (OHCs). As most underwater noise sources contain low-frequency components, we expect to find most lesions in the apical region of the cochlea of toothed whales, in cases of permanent noise-induced hearing loss. To further understand how man-made noise might affect cetacean hearing, there is a need to describe normal morphological features of the apex and document interspecific anatomic variations in cetaceans. However, distinguishing between apical normal variability and hair cell death is challenging. We describe anatomical features of the organ of Corti of the apex in 23 ears from five species of toothed whales (harbor porpoise Phocoena phocoena, spinner dolphin Stenella longirostris, pantropical spotted dolphin Stenella attenuata, pygmy sperm whale Kogia breviceps, and beluga whale Delphinapterus leucas) by scanning electron microscopy and immunofluorescence. Our results showed an initial region where the lowest frequencies are encoded with two or three rows of OHCs, followed by the typical configuration of three OHC rows and three rows of supporting Deiters' cells. Whenever two rows of OHCs were detected, there were usually only two corresponding rows of supporting Deiters' cells, suggesting that the number of rows of Deiters' cells is a good indicator to distinguish between normal and pathological features., (© 2021 The Authors. The Anatomical Record published by Wiley Periodicals LLC on behalf of American Association for Anatomy.)

Separation of respiratory and digestive tracts in the mammalian pharynx is critical for survival. Food must be kept out of the respiratory tract, and air must be directed into the respiratory tract when breathing. 1 Cetaceans have the additional problem of feeding while underwater. Lunge-feeding baleen whales (rorquals) open the mouth while swimming at high speeds to engulf a volume of prey-laden water as large as their own body 2 and experience tremendous forces as water floods the mouth. How the respiratory tract is protected in the pharynx during engulfment and while swallowing a massive slurry of tiny living prey remains unknown, despite its importance to survival. By dissecting adult and fetal fin whales, we determined that a large musculo-fatty structure passively seals the oropharyngeal channel. This "oral plug" is not observed in other animals, and its position indicates it must be shifted to allow swallowing; it is a part of the soft palate and can only shift posteriorly and dorsally. Elevation of the oral plug allows food transfer to the pharynx and protects the upper airways from food entry. The laryngeal inlet in the floor of the pharynx is sealed by laryngeal cartilages, and the muscular laryngeal sac moves upward into the laryngeal cavity, completely occluding the airway. The pharynx is dedicated to the digestive tract during swallowing, with no connection between upper and lower airways. These adaptations to facilitate swallowing were a critical development in the evolution of large body size in these, the largest animals on earth., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2021 Elsevier Inc. All rights reserved.)

Congenital hearing loss is recognized in humans and other terrestrial species. However, there is a lack of information on its prevalence or pathophysiology in pinnipeds. It is important to have baseline knowledge on marine mammal malformations in the inner ear, to differentiate between congenital and acquired abnormalities, which may be caused by infectious pathogens, age, or anthropogenic interactions, such as noise exposure. Ultrastructural evaluation of the cochlea of a neonate harbor seal ( Phoca vitulina ) by scanning electron microscopy revealed bilateral loss of inner hair cells with intact outer hair cells. The selective inner hair cell loss was more severe in the basal turn, where high-frequency sounds are encoded. The loss of inner hair cells started around 40% away from the apex or tip of the spiral, reaching a maximum loss of 84.6% of hair cells at 80-85% of the length from the apex. Potential etiologies and consequences are discussed. This is believed to be the first case report of selective inner hair cell loss in a marine mammal neonate, likely congenital.

Evidence of hearing impairment was identified in a harbour porpoise ( Phocoena phocoena ) on the basis of scanning electron microscopy. In addition, based on histopathology and immunohistochemistry, there were signs of unrelated cerebral toxoplasmosis. The six-year old individual live stranded on the Dutch coast at Domburg in 2016 and died a few hours later. The most significant gross lesion was multifocal necrosis and haemorrhage of the cerebrum. Histopathology of the brain revealed extensive necrosis and haemorrhage in the cerebrum with multifocal accumulations of degenerated neutrophils, lymphocytes and macrophages, and perivascular lymphocytic cuffing. The diagnosis of cerebral toxoplasmosis was confirmed by positive staining of protozoa with anti- Toxoplasma gondii antibodies. Tachyzoites were not observed histologically in any of the examined tissues. Ultrastructural evaluation of the inner ear revealed evidence of scattered loss of outer hair cells in a 290 µm long segment of the apical turn of the cochlea, and in a focal region of ~ 1.5 mm from the apex of the cochlea, which was compatible with noise-induced hearing loss. This is the first case of concurrent presumptive noise-induced hearing loss and toxoplasmosis in a free-ranging harbour porpoise from the North Sea.

Humpback and blue whales are large baleen-bearing cetaceans, which use a unique prey-acquisition strategy-lunge feeding-to engulf entire patches of large plankton or schools of forage fish and the water in which they are embedded. Dynamically, and while foraging on krill, lunge-feeding incurs metabolic expenditures estimated at up to 20.0 MJ. Because of prey abundance and its capture in bulk, lunge feeding is carried out at high acquired-to-expended energy ratios of up to 30 at the largest body sizes (∼27 m). We use bio-logging tag data and the work-energy theorem to show that when krill-feeding at depth while using a wide range of prey approach swimming speeds (2-5 m/s), rorquals generate significant and widely varying metabolic power output during engulfment, typically ranging from 10 to 50 times the basal metabolic rate of land mammals. At equal prey field density, such output variations lower their feeding efficiency two- to three-fold at high foraging speeds, thereby allowing slow and smaller rorquals to feed more efficiently than fast and larger rorquals. The analysis also shows how the slowest speeds of harvest so far measured may be connected to the biomechanics of the buccal cavity and the prey's ability to collectively avoid engulfment. Such minimal speeds are important as they generate the most efficient lunges. Sommaire Les rorquals à bosse et rorquals bleus sont des baleines à fanons qui utilisent une technique d'alimentation unique impliquant une approche avec élan pour engouffrer de larges quantités de plancton et bancs de petits poissons, ainsi que la masse d'eau dans laquelle ces proies sont situés. Du point de vue de la dynamique, et durant l'approche et engouffrement de krill, leurs dépenses énergétiques sont estimées jusqu'à 20.0 MJ. À cause de l'abondance de leurs proies et capture en masse, cette technique d'alimentation est effectuée à des rapports d'efficacité énergétique (acquise -versus- dépensée) estimés aux environs de 30 dans le cas des plus grandes baleines (27 m). Nous utilisons les données recueillies par des capteurs de bio-enregistrement ainsi que le théorème reliant l'énergie à l'effort pour démontrer comment les rorquals s'alimentant sur le krill à grandes profondeurs, et à des vitesses variant entre 2 et 5 m/s, maintiennent des taux de dépenses énergétiques entre 10 et 50 fois le taux métabolique basal des mammifères terrestres. À densités de proies égales, ces variations d'énergie utilisée peuvent réduire le rapport d'efficacité énergétique par des facteurs entre 2x et 3x, donc permettant aux petits et plus lents rorquals de chasser avec une efficacité comparable à celle des rorquals les plus grands et rapides. Notre analyse démontre aussi comment des vitesses d'approche plus lentes peuvent être reliées à la biomécanique de leur poche ventrale extensible, et à l'habilitée des proies à éviter d'être engouffrer. Ces minimums de vitesses sont importants car ils permettent une alimentation plus efficace énergétiquement., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Correlations between inner ear morphology and auditory sensitivity in the same individual are extremely difficult to obtain for stranded cetaceans. Animals in captivity and rehabilitation offer the opportunity to combine several techniques to study the auditory system and cases of hearing impairment in a controlled environment. Morphologic and auditory findings from two beluga whales ( Delphinapterus leucas ) in managed care are presented. Cochlear analysis of a 21-year-old beluga whale showed bilateral high-frequency hearing loss. Specifically, scanning electron microscopy of the left ear revealed sensory cell death in the first 4.9 mm of the base of the cochlea with scar formation. Immunofluorescence microscopy of the right ear confirmed the absence of hair cells and type I afferent innervation in the first 6.6 mm of the base of the cochlea, most likely due to an ischemia. Auditory evoked potentials (AEPs) measured 1.5 years prior this beluga's death showed a generalized hearing loss, being more pronounced in the high frequencies. This individual might have had a mixed hearing loss that would explain the generalized hearing impairment. Conversely, based on AEP evaluation, her mother had normal hearing and subsequent cochlear analysis did not feature any apparent sensorineural pathology. This is believed to be the first study to compare two cochlear analysis techniques and hearing sensitivity measurements from AEPs in cetaceans. The ability to combine morphological and auditory data is crucial to validate predictions of cochlear frequency maps based on morphological features. In addition, our study shows that these three complementary analysis techniques lead to comparable results, thus improving our understanding of how hearing impairment can be detected in stranding cases., (Copyright © 2020 Morell, Raverty, Mulsow, Haulena, Barrett-Lennard, Nordstrom, Venail and Shadwick.)

Morphometric analysis of the inner ear of mammals can provide information for cochlear frequency mapping, a species-specific designation of locations in the cochlea at which different sound frequencies are encoded. Morphometric variation occurs in the hair cells of the organ of Corti along the cochlea, with the base encoding the highest frequency sounds and the apex encoding the lowest frequencies. Changes in cell shape and spacing can yield additional information about the biophysical basis of cochlear tuning mechanisms. Here, we investigate how morphometric analysis of hair cells in mammals can be used to predict the relationship between frequency and cochlear location. We used linear and geometric morphometrics to analyze scanning electron micrographs of the hair cells of the cochleae in Parnell's mustached bat (Pteronotus parnellii) and Wistar rat (Rattus norvegicus) and determined a relationship between cochlear morphometrics and their frequency map. Sixteen of twenty-two of the morphometric parameters analyzed showed a significant change along the cochlea, including the distance between the rows of hair cells, outer hair cell width, and gap width between hair cells. A multiple linear regression model revealed that nine of these parameters are responsible for 86.9 % of the variation in these morphometric data. Determining the most biologically relevant measurements related to frequency detection can give us a greater understanding of the essential biomechanical characteristics for frequency selectivity during sound transduction in a diversity of animals.

Prestin is an integral membrane motor protein located in outer hair cells of the mammalian cochlea. It is responsible for electromotility and required for cochlear amplification. Although prestin works in a cycle-by-cycle mode up to frequencies of at least 79 kHz, it is not known whether or not prestin is required for the extreme high frequencies used by echolocating species. Cetaceans are known to possess a prestin coding gene. However, the expression and distribution pattern of the protein in the cetacean cochlea has not been determined, and the contribution of prestin to echolocation has not yet been resolved. Here we report the expression of the protein prestin in five species of echolocating whales and two species of echolocating bats. Positive labeling in the basolateral membrane of outer hair cells, using three anti-prestin antibodies, was found all along the cochlear spiral in echolocating species. These findings provide morphological evidence that prestin can have a role in cochlear amplification in the basolateral membrane up to 120-180 kHz. In addition, labeling of the cochlea with a combination of anti-prestin, anti-neurofilament, anti-myosin VI and/or phalloidin and DAPI will be useful for detecting potential recent cases of noise-induced hearing loss in stranded cetaceans. This study improves our understanding of the mechanisms involved in sound transduction in echolocating mammals, as well as describing an optimized methodology for detecting cases of hearing loss in stranded marine mammals., (Copyright © 2020 Morell, Vogl, IJsseldijk, Piscitelli-Doshkov, Tong, Ostertag, Ferreira, Fraija-Fernandez, Colegrove, Puel, Raverty and Shadwick.)

The upper respiratory tract of rorquals, lunge-feeding baleen whales, must be protected against water incursion and the risk of barotrauma at depth, where air-filled spaces like the bony nasal cavities may experience high adverse pressure gradients. We hypothesize these two disparate tasks are accomplished by paired cylindrical nasal plugs that attach on the rostrum and deep inside the nasal cavity. Here, we present evidence that the large size and deep attachment of the plugs is a compromise, allowing them to block the nasal cavities to prevent water entry while also facilitating pressure equilibration between the nasal cavities and ambient hydrostatic pressure ( P amb ) at depth. We investigated nasal plug behaviour using videos of rorquals surfacing, plug morphology from dissections, histology and MRI scans, and plug function by mathematically modelling nasal pressures at depth. We found each nasal plug has three structurally distinct regions: a muscular rostral region, a predominantly fatty mid-section and an elastic tendon that attaches the plug caudally. We propose muscle contraction while surfacing pulls the fatty sections rostrally, opening the nasal cavities to air, while the elastic tendons snap the plugs back into place, sealing the cavities after breathing. At depth, we propose P amb pushes the fatty region deeper into the nasal cavities, decreasing air volume by about half and equilibrating nasal cavity to P amb , preventing barotrauma. The nasal plugs are a unique innovation in rorquals, which demonstrate their importance and novelty during diving, where pressure becomes as important an issue as the danger of water entry., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2020. Published by The Company of Biologists Ltd.)

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.

The tongue of rorqual (balaenopterid) whales slides far down the throat into the expanded oral pouch as an enormous mouthful of water is engulfed during gulp feeding. As the tongue and adjacent oral floor expands and slides caudoventrally, it glides along a more superficial (outer) layer of ventral body wall musculature, just deep to the accordion-like ventral throat pleats. We hypothesize that this sliding movement of adjacent musculature is facilitated by a slick, stretchy layer of loose areolar connective tissue that binds the muscle fibers and reduces friction: fascia. Gross anatomical examination of the gular region of adult minke, fin, and humpback whales confirms the presence of a discrete, three-layered sublingual fascia interposed between adhering fasciae of the tongue and body wall. Histological analysis of this sublingual fascia reveals collagen and elastin fibers loosely organized in a random feltwork along with numerous fibroblasts in a watery extracellular matrix. Biomechanical testing of tissue samples in the field and laboratory, via machine-controlled or manual stretching, demonstrates expansion of the sublingual fascia and its three layers up to 250% beyond resting dimensions, with slightly more extension observed in anteroposterior (rather than mediolateral or oblique) stretching, and with the most superficial of the fascia's three layers. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:735-744, 2019. © 2018 Wiley Periodicals, Inc., (© 2018 Wiley Periodicals, Inc.)

Control of wing shape is believed to be a key feature that allows most birds to produce aerodynamically efficient flight behaviors and high maneuverability. Anatomical organization of intrinsic wing muscles suggests specific roles for the different motor elements in wing shape modulation, but testing these hypothesized functions requires challenging measurements of muscle activation and strain patterns, and force dynamics. The wing muscles that have been best characterized during flight are the elbow muscles of the pigeon ( Columba livia ). In vivo studies during different flight modes revealed variation in strain profile, activation timing and duration, and contractile cycle frequency of the humerotriceps, suggesting that this muscle may alter wing shape in diverse ways. To examine the multifunction potential of the humerotriceps, we developed an in situ work loop approach to measure how activation duration and contractile cycle frequency affected muscle work and power across the full range of activation onset times. The humerotriceps produced predominantly net negative power, likely due to relatively long stimulus durations, indicating that it absorbs work, but the work loop shapes also suggest varying degrees of elastic energy storage and release. The humerotriceps consistently exhibited positive and negative instantaneous power within a single contractile cycle, across all treatments. When combined with previous in vivo studies, our results indicate that both within and across contractile cycles, the humerotriceps can dynamically shift among roles of actuator, brake, and stiff or compliant spring, based on activation properties that vary with flight mode., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

We conducted in vitro inflations of freshly excised ventral aortas of the Greenland shark, Somniosus microcephalus , and used pressure-diameter data to estimate the point of transition from high to low compliance, which has been shown to occur at the mean blood pressure in other vertebrates including fishes. We also determined the pressure at which the modulus of elasticity of the aorta reached 0.4 MPa, as occurs at the compliance transition in other species. From these analyses, we predict the average ventral aortic blood pressure in S. microcephalus to be about 2.3-2.8 kPa, much lower than reported for other sharks. Our results support the idea that this species is slow moving and has a relatively low aerobic metabolism. Histological investigation of the ventral aorta shows that elastic fibres are present in relatively low abundance and loosely connected, consistent with this aorta having high compliance at a relatively low blood pressure., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

A sphincter on the inferior vena cava can protect the heart of a diving mammal from overload when elevated abdominal pressures increase venous return, yet sphincters are reported incompetent or absent in some cetacean species. We previously hypothesized that abdominal pressures are elevated and pulsatile in fluking cetaceans, and that collagen is deposited on the diaphragm according to pressure levels to resist deformation. Here, we tested the hypothesis that cetaceans generating high abdominal pressures need a more robust sphincter than those generating low pressures. We examined diaphragm morphology in seven cetacean and five pinniped species. All odontocetes had morphologically similar sphincters despite large differences in collagen content, and mysticetes had muscle that could modulate caval flow. These findings do not support the hypothesis that sphincter structure correlates with abdominal pressures. To understand why a sphincter is needed, we simulated the impact of oscillating abdominal pressures on caval flow. Under low abdominal pressures, simulated flow oscillated with each downstroke. Under elevated pressures, a vascular waterfall formed, greatly smoothing flow. We hypothesize that cetaceans maintain high abdominal pressures to moderate venous return and protect the heart while fluking, and use their sphincters only during low-fluking periods when abdominal pressures are low. We suggest that pinnipeds, which do not fluke, maintain low abdominal pressures. Simulations also showed that retrograde oscillations could be transmitted upstream from the cetacean abdomen and into the extradural veins, with potentially adverse repercussions for the cerebral circulation. We propose that locomotion-generated pressures have influenced multiple aspects of the cetacean vascular system., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Nerves that supply the floor of the oral cavity in rorqual whales are extensible to accommodate the dramatic changes in tissue dimensions that occur during "lunge feeding" in this group. We report here that the large nerves innervating the muscle component of the ventral grooved blubber (VGB) in fin whales are branches of cranial nerve VII (facial nerve). Therefore, the muscles of the VGB are homologous to second branchial arch derived muscles, which in humans include the muscles of "facial expression." We speculate, based on the presence of numerous foramina on the dorsolateral surface of the mandibular bones, that general sensation from the VGB likely is carried by branches of the mandibular division (V3) of cranial nerve V (trigeminal nerve), and that these small branches travel in the lipid-rich layer directly underlying the skin. We show that intercostal and phrenic nerves, which are not extensible, have a different wall and nerve core morphology than the large VGB nerves that are branches of VII. Although these VGB nerves are known to have two levels of waviness, the intercostal and phrenic nerves have only one in which the nerve fascicles in the nerve core are moderately wavy. In addition, the VGB nerves have inner and outer parts to their walls with numerous large elastin fibers in the outer part, whereas intercostal and phrenic nerves have single walls formed predominantly of collagen. Our results illustrate that overall nerve morphology depends greatly on location and the forces to which the structures are exposed. Anat Rec, 300:1963-1972, 2017. © 2017 Wiley Periodicals, Inc., (© 2017 Wiley Periodicals, Inc.)

The mandibles of rorqual whales are highly modified to support loads associated with lunge-feeding, a dynamic filter feeding mechanism that is characterized by rapid changes in gape angle and acceleration. Although these structures are the largest ossified elements in animals and an important part of the rorqual engulfment apparatus, details of internal structure are limited and no direct measurements of mechanical properties exist. Likewise, the forces that are sustained by the mandibles are unknown. Here we report on the structure and mechanical behavior of the mandible of an adult fin whale. A series of transverse sections were cut at locations along the entire length of a 3.6-m left mandible recovered post-mortem from a 16-m fin whale, and CT scanned to make density maps. Cored samples 6-8 mm in diameter were tested in compression to determine the Young's modulus and strength. In addition, wet density, dry density and mineral density were measured. Dense cortical bone occupies only a relatively narrow peripheral layer while much less dense and oil-filled trabecular bone occupies the rest. Mineral density of both types is strongly correlated with dry density and CT Hounsfield units. Compressive strength is strongly correlated with Young's modulus, while strength and stiffness are both correlated with mineral density. It appears that the superficial compact layer is the main load bearing element, and that the mandible is reinforced against dorso-vental flexion that would occur during the peak loads while feeding. Anat Rec, 300:1953-1962, 2017. © 2017 Wiley Periodicals, Inc., (© 2017 Wiley Periodicals, Inc.)

Internal pressures change throughout a cetacean's body during swimming or diving, and uneven pressures between the thoracic and abdominal compartments can affect the cardiovascular system. Pressure differentials could arise from ventral compression on each fluke downstroke or by a faster equilibration of the abdominal compartment with changing ambient ocean pressures compared with the thoracic compartment. If significant pressure differentials do develop, we would expect the morphology of the diaphragm to adapt to its in vivo loading. Here, we tested the hypothesis that significant pressure differentials develop between the thoracic and abdominal cavities in diving cetaceans by examining diaphragms from several cetacean and pinniped species. We found that: (1) regions of cetacean diaphragms possess subserosal collagen fibres that would stabilize the diaphragm against craniocaudal stretch; (2) subserosal collagen covers 5-60% of the thoracic diaphragm surface, and area correlates strongly with published values for swimming speed of each cetacean species ( P <0.001); and (3) pinnipeds, which do not locomote by vertical fluking, do not possess this subserosal collagen. These results strongly suggest that this collagen is associated with loads experienced during a dive, and they support the hypothesis that diving cetaceans experience periods during which abdominal pressures significantly exceed thoracic pressures. Our results are consistent with the generation of pressure differentials by fluking and by different compartmental equilibration rates. Pressure differentials during diving would affect venous and arterial perfusion and alter transmural pressures in abdominal arteries., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Peripheral nerves are susceptible to stretch injury [1-4] and incorporate structural waviness at the level of the axons, fascicles, and nerve trunk to accommodate physiological increases in length [5, 6]. It is unknown whether there are limits to the amount of deformation that waviness can accommodate. In rorqual whales, a sub-group of baleen whales, nerves running through the ventral groove blubber (VGB) associated with the floor of the mouth routinely experience dramatically large deformations. In fact, some of these nerves more than double their length during lunge feeding and then recoil to a short, compressed state after each lunge [7-9]. It is unknown how these nerves have adapted to operate in both extended and recoiled states. Using micro-CT and mechanics, we have discovered that the VGB nerves from fin whales require two levels of waviness to prevent stretch damage in both extended and recoiled states. The entire nerve core itself is highly folded when recoiled and appears buckled. This folding provides slack for extension but unavoidably generates large stretches at the bends that could damage nerve fascicles within the core. The strain at the bends is minimized by the specific waveform adopted by the core [10, 11], while the existing bending strains are accommodated by a second level of waviness in the individual fascicles that avoids stretch of the fascicle itself. Structural hierarchy partitions the waviness between the two length scales, providing a mechanism to maintain total elongation while preventing the stretching of fascicles at the bends when recoiled., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

Assessment of the impact of noise over-exposure in stranded cetaceans is challenging, as the lesions that lead to hearing loss occur at the cellular level and inner ear cells are very sensitive to autolysis. Distinguishing ante-mortem pathology from post-mortem change has been a major constraint in diagnosing potential impact. Here, we outline a methodology applicable to the detection of noise-induced hearing loss in stranded cetaceans. Inner ears from two mass strandings of long-finned pilot whales in Scotland were processed for scanning electron microscopy observation. In one case, a juvenile animal, whose ears were fixed within 4 hours of death, revealed that many sensory cells at the apex of the cochlear spiral were missing. In this case, the absence of outer hair cells would be compatible with overexposure to underwater noise, affecting the region which transduces the lowest frequencies of the pilot whales hearing spectrum. Perfusion of cochlea with fixative greatly improved preservation and enabled diagnostic imaging of the organ of Corti, even 30 hours after death. This finding supports adopting a routine protocol to detect the pathological legacy of noise overexposure in mass stranded cetaceans as a key to understanding the complex processes and implications that lie behind such stranding events., Competing Interests: The authors declare no competing financial interests.

A survey of macroscopic and microscopic wear patterns in the baleen of eight whale species (Cetacea: Mysticeti) discloses structural, functional, and life history properties of this neomorphic keratinous tissue, including evidence of intraoral water flow patterns involved in filter feeding. All baleen demonstrates wear, particularly on its medial and ventral edges, as flat outer layers of cortical keratin erode to reveal horn tubes, also of keratin, which emerge as hair-like fringes. This study quantified five additional categories of specific wear: pitting of plates, scratching of plates, scuffing of fringes, shortening of fringes, and reorientation of fringes (including fringes directed between plates to the exterior of the mouth). Blue whale baleen showed the most pitting and sei whale baleen the most scratching; gray whale baleen had the most fringe wear. The location of worn baleen within the mouth suggests that direct contact with the tongue is not responsible for most wear, and that flowing water as well as abrasive prey or sediment carried by the flowing water likely causes pitting and scratching of plates as well as fringe fraying, scuffing, shortening, and reorientation. Baleen also has elevated vertical and horizontal ridges that are unrelated to wear; these are probably related to growth and may allow for age determination., (© 2016 Wiley Periodicals, Inc.)

The mechanical properties of aortic elastin vary regionally, but the microstructural basis for this variation is unknown. This study was designed to identify the relative contributions of lamellar and interlamellar elastin to circumferential load bearing in the mouse thoracic and abdominal aortas. Forces developed in uniaxial tests of samples of fresh and autoclaved aorta were correlated with elastin content and morphology obtained from histology and multiphoton laser scanning microscopy. Autoclaving should render much of the interlamellar elastin mechanically incompetent. In autoclaved tissue force per unit sample width correlated with lamellar elastin content (P≪0.001) but not total elastin content. In fresh tissue at low strain where elastin dominates the mechanical response, forces were higher than in the autoclaved tissue, but force did not correlate with total elastin content. Therefore although interlamellar elastin likely contributed to the stiffness in the fresh aorta, its contribution appeared not in proportion to its quantity. In both fresh and autoclaved tissue, elastin stiffness consistently decreased along the abdominal aorta, a key area for aneurysm development, and this difference could not be fully accounted for on the basis of either lamellar or total elastin content. These findings are relevant to the development of mathematical models of arterial mechanics, particularly for mouse models of arterial diseases involving elastic tissue. In microstructural based models the quantity of each mural constituent determines its contribution to the total response. This study shows elastin's mechanical response cannot necessarily be accounted for on the basis of fibre quantity, orientation, and modulus., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

The morphological study of the Odontocete organ of Corti, together with possible alterations associated with damage from sound exposure, represents a key conservation approach to assess the effects of acoustic pollution on marine ecosystems. By collaborating with stranding networks from several European countries, 150 ears from 13 species of Odontocetes were collected and analyzed by scanning (SEM) and transmission (TEM) electron microscopy. Based on our analyses, we first describe and compare Odontocete cochlear structures and then propose a diagnostic method to identify inner ear alterations in stranded individuals. The two species analyzed by TEM (Phocoena phocoena and Stenella coeruleoalba) showed morphological characteristics in the lower basal turn of high-frequency hearing species. Among other striking features, outer hair cell bodies were extremely small and were strongly attached to Deiters cells. Such morphological characteristics, shared with horseshoe bats, suggest that there has been convergent evolution of sound reception mechanisms among echolocating species. Despite possible autolytic artifacts due to technical and experimental constraints, the SEM analysis allowed us to detect the presence of scarring processes resulting from the disappearance of outer hair cells from the epithelium. In addition, in contrast to the rapid decomposition process of the sensory epithelium after death (especially of the inner hair cells), the tectorial membrane appeared to be more resistant to postmortem autolysis effects. Analysis of the stereocilia imprint pattern at the undersurface of the tectorial membrane may provide a way to detect possible ultrastructural alterations of the hair cell stereocilia by mirroring them on the tectorial membrane., (© 2014 Wiley Periodicals, Inc.)

Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species-specific anatomy, mechanics, and behavior., (Copyright © 2013 Wiley Periodicals, Inc.)

The oral anatomy of the fin whale (Balaenoptera physalus) consists of several major structures crucial to its engulfment method of feeding, such as stiff keratinized baleen plates, a large flaccid tongue, and a prominent vomer. One under-documented part of this anatomy is the cream white Zwischensubstanz that holds the baleen plates to the rostrum at their dorsal base. The mechanical and structural properties of Zwischensubstanz play a key role in baleen plate dynamics and, on the grand scale, contribute to baleen whales' filtration efficiency and attainment of large body size. Compression and tensile tests on the Zwischensubstanz sampled from an 18 m fin whale showed that this material unexpectedly exhibits linear isotropic behaviour with Elastic Modulus of 2.56 ± 0.60 MPa and hysteresis of 0.44 ± 0.02 in compression despite apparent unidirectional growth. Acting similar to a soft rubber, the Zwischensubstanz absorbs and dissipates the enormous forces acting on baleen plates during engulfment feeding while maintaining spacing between the plates to maximize filtration efficiency. Microscopic analysis provided images of connective tissue papillae penetrating the base of the Zwischensubstanz and developing within it to emerge as fully formed, keratinized baleen plates. The plates develop from the papillae and a connective tissue sheet within the 5-7 cm deep Zwischensubstanz. The Zwischensubstanz provides a keratin matrix of concentrically oriented fibers around each papilla forming the hard baleen plates and frayed fringes used for filter feeding. During this formation, the Zwischensubstanz remains unchanged and appears to slough away to allow the baleen plate to grow unhindered., (Copyright © 2013 Wiley Periodicals, Inc.)

Muscle serves a wide variety of mechanical functions during animal feeding and locomotion, but the performance of this tissue is limited by how far it can be extended. In rorqual whales, feeding and locomotion are integrated in a dynamic process called lunge feeding, where an enormous volume of prey-laden water is engulfed into a capacious ventral oropharyngeal cavity that is bounded superficially by skeletal muscle and ventral groove blubber (VGB). The great expansion of the cavity wall presents a mechanical challenge for the physiological limits of skeletal muscle, yet its role is considered fundamental in controlling the flux of water into the mouth. Our analyses of the functional properties and mechanical behaviour of VGB muscles revealed a crimped microstructure in an unstrained, non-feeding state that is arranged in parallel with dense and straight elastin fibres. This allows the muscles to accommodate large tissue deformations of the VGB yet still operate within the known strain limits of vertebrate skeletal muscle. VGB transverse strains in routine-feeding rorquals were substantially less than those observed in dead ones, where decomposition gas stretched the VGB to its elastic limit, evidence supporting the idea that eccentric muscle contraction modulates the rate of expansion and ultimate size of the ventral cavity during engulfment.

Fin whales have an incompliant aorta, which, we hypothesize, represents an adaptation to large, depth-induced variations in arterial transmural pressures. We hypothesize these variations arise from a limited ability of tissues to respond to rapid changes in ambient ocean pressures during a dive. We tested this hypothesis by measuring arterial mechanics experimentally and modelling arterial transmural pressures mathematically. The mechanical properties of mammalian arteries reflect the physiological loads they experience, so we examined a wide range of fin whale arteries. All arteries had abundant adventitial collagen that was usually recruited at very low stretches and inflation pressures (2-3 kPa), making arterial diameter largely independent of transmural pressure. Arteries withstood significant negative transmural pressures (-7 to -50 kPa) before collapsing. Collapse was resisted by recruitment of adventitial collagen at very low stretches. These findings are compatible with the hypothesis of depth-induced variation of arterial transmural pressure. Because transmural pressures depend on thoracic pressures, we modelled the thorax of a diving fin whale to assess the likelihood of significant variation in transmural pressures. The model predicted that deformation of the thorax body wall and diaphragm could not always equalize thoracic and ambient pressures because of asymmetrical conditions on dive descent and ascent. Redistribution of blood could partially compensate for asymmetrical conditions, but inertial and viscoelastic lag necessarily limits tissue response rates. Without pressure equilibrium, particularly when ambient pressures change rapidly, internal pressure gradients will develop and expose arteries to transient pressure fluctuations, but with minimal hemodynamic consequence due to their low compliance.

This study was undertaken to understand elastin's role in the mechanical homeostasis of the arterial wall. The mechanical properties of elastin vary along the aorta, and we hypothesized this maintained a uniform mechanical environment for the elastin, despite regional variation in loading. Elastin's physiological loading was determined by comparing the inflation response of intact and autoclave purified elastin aortas from the proximal and distal thoracic aorta. Elastin's stretch and stress depend on collagen recruitment. Collagen recruitment started in the proximal aorta at systolic pressures (13.3 to 14.6 kPa) and in the distal at sub-diastolic pressures (9.3 to 10.6 kPa). In the proximal aorta collagen did not contribute significantly to the stress or stiffness, indicating that elastin determined the vessel properties. In the distal aorta, the circumferential incremental modulus was 70% higher than in the proximal aorta, half of which (37%) was due to a stiffening of the elastin. Compared to the elastin tissue in the proximal aorta, the distal elastin suffered higher physiological circumferential stretch (29%, P=0.03), circumferential stress (39%, P=0.02), and circumferential stiffness (37%, P=0.006). Elastin's physiological axial stresses were also higher (67%, P=0.003). These findings do not support the hypothesis that the loading on elastin is constant along the aorta as we expected from homeostasis., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

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.

The locomotor system in sharks has been investigated for many decades, starting with the earliest kinematic studies by Sir James Gray in the 1930s. Early work on axial muscle anatomy also included sharks, and the first demonstration of the functional significance of red and white muscle fibre types was made on spinal preparations in sharks. Nevertheless, studies on teleosts dominate the literature on fish swimming. The purpose of this article is to review the current knowledge of muscle function and swimming in sharks, by considering their morphological features related to swimming, the anatomy and physiology of the axial musculature, kinematics and muscle dynamics, and special features of warm-bodied lamnids. In addition, new data are presented on muscle activation in fast-starts. Finally, recent developments in tracking technology that provide insights into shark swimming performance in their natural environment are highlighted., (© 2012 The Authors. Journal of Fish Biology © 2012 The Fisheries Society of the British Isles.)

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 VO2 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 VO2|max. 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.

The feeding apparatuses of rorqual whales and pelicans exhibit a number of similarities, including long, kinetic jaws that increase gape size, and extensible tissue comprising the floor of the mouth. These specializations enable the engulfment of large volumes of prey-laden water in both taxa. However, the mechanics of engulfment feeding in rorquals and pelicans have never been quantitatively compared. Here, we use "BendCT," a novel analytical program, to investigate the mechanical design of rorqual and pelican mandibles, to understand whether these bones show comparable designs for resisting similar hydrodynamical loads. We also compare the mechanical properties of the extensible tissue used during engulfment in rorquals and pelicans. We demonstrate that the evolutionary convergence in the feeding apparatus of rorquals and pelicans is more pronounced than has been recognized previously; both taxa exhibit mandibular flexural rigidity distributions suited for resisting dorsoventral bending stresses encountered while feeding, and possess similarly extensible tissue on the floor of their mouths., (Copyright © 2011 Wiley-Liss, Inc.)

Fishes with internalized and endothermic red muscles (i.e. tunas and lamnid sharks) are known for a stiff-bodied form of undulatory swimming, based on unique muscle-tendon architecture that limits lateral undulation to the tail region even though the red muscle is shifted anteriorly. A strong convergence between lamnid sharks and tunas in these features suggests that thunniform swimming might be evolutionarily tied to this specialization of red muscle, but recent observations on the common thresher shark (Alopias vulpinus) do not support this view. Here, we review the fundamental features of the locomotor systems in lamnids and tunas, and present data on in vivo muscle function and swimming mechanics in thresher sharks. These results suggest that the presence of endothermic and internalized red muscles alone in a fish does not predict or constrain the swimming mode to be thunniform and, indeed, that the benefits of this type of muscle may vary greatly as a consequence of body size.

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.

Rorqual whales (Balaenopteridae) obtain their food by lunge feeding, a dynamic process that involves the intermittent engulfment and filtering of large amounts of water and prey. During a lunge, whales accelerate to high speed and open their mouth wide, thereby exposing a highly distensible buccal cavity to the flow and facilitating its inflation. Unsteady hydrodynamic models suggest that the muscles associated with the ventral groove blubber undergo eccentric contraction in order to stiffen and control the inflation of the buccal cavity; in doing so the engulfed water mass is accelerated forward as the whale's body slows down. Although the basic mechanics of lunge feeding are relatively well known, the scaling of this process remains poorly understood, particularly with regards to its duration (from mouth opening to closure). Here we formulate a new theory of engulfment time which integrates prey escape behavior with the mechanics of the whale's body, including lunge speed and acceleration, gape angle dynamics, and the controlled inflation of the buccal cavity. Given that the complex interaction between these factors must be highly coordinated in order to maximize engulfment volume, the proposed formulation rests on the scenario of Synchronized Engulfment, whereby the filling of the cavity (posterior to the temporomandibular joint) coincides with the moment of maximum gape. When formulated specifically for large rorquals feeding on krill, our analysis predicts that engulfment time increases with body size, but in amounts dictated by the specifics of krill escape and avoidance kinematics. The predictions generated by the model are corroborated by limited empirical data on a species-specific basis, particularly for humpback and blue whales chasing krill. A sensitivity analysis applied to all possible sized fin whales also suggests that engulfment duration and lunge speed will increase intra-specifically with body size under a wide range of predator-prey scenarios. This study provides the theoretical framework required to estimate the scaling of the mass-specific drag being generated during engulfment, as well as the energy expenditures incurred., (Copyright © 2010 Elsevier Ltd. All rights reserved.)

Uniaxial and biaxial mechanical properties of purified elastic tissue from the proximal thoracic aorta were studied to understand physiological load distributions within the arterial wall. Stress-strain behaviour was non-linear in uniaxial and inflation tests. Elastic tissue was 40% stiffer in the circumferential direction compared to axial in uniaxial tests and approximately 100% stiffer in vessels at an axial stretch ratio of 1.2 or 1.3 and inflated to physiological pressure. Poisson's ratio v(thetaz) averaged 0.2 and v(ztheta) increased with circumferential stretch from approximately 0.2 to approximately 0.4. Axial stretch had little impact on circumferential behaviour. In intact (unpurified) vessels at constant length, axial forces decreased with pressure at low axial stretches but remained constant at higher stretches. Such a constant axial force is characteristic of incrementally isotropic arteries at their in vivo dimensions. In purified elastic tissue, force decreased with pressure at all axial strains, showing no trend towards isotropy. Analysis of the force-length-pressure data indicated a vessel with v(thetaz) approximately 0.2 would stretch axially 2-4% with the cardiac pulse yet maintain constant axial force. We compared the ability of 4 mathematical models to predict the pressure-circumferential stretch behaviour of tethered, purified elastic tissue. Models that assumed isotropy could not predict the stretch at zero pressure. The neo-Hookean model overestimated the non-linearity of the response and two non-linear models underestimated it. A model incorporating contributions from orthogonal fibres captured the non-linearity but not the zero-pressure response. Models incorporating anisotropy and non-linearity should better predict the mechanical behaviour of elastic tissue of the proximal thoracic aorta., (Copyright 2010 Elsevier Ltd. All rights reserved.)

Rorqual whales (Balaenopteridae) lunge at high speed with mouth open to nearly 90 degrees to engulf large volumes of prey-laden water. This feeding process is enabled by extremely large skulls and mandibles that increase mouth area, thereby facilitating the flux of water into the mouth. When these mandibles are lowered during lunge-feeding, they are exposed to high drag, and therefore, may be subject to significant bending forces. We hypothesized that these mandibles exhibited a mechanical design (shape and density distribution) that enables these bones to accommodate high loads during lunge-feeding without exceeding their breaking strength. We used quantitative computed tomography (QCT) to determine the three-dimensional geometry and density distribution of a pair of subadult humpback whale (Megaptera novaeangliae) mandibles (length = 2.10 m). QCT data indicated highest bone density and cross-sectional area, and therefore, high resistance to bending and deflection, from the coronoid process to the middle of the dentary, which then decreased towards the anterior end of the mandible. These results differ from the caudorostral trends of increasing mandibular bone density in mammals, such as humans and the right whale, Eubalaena glacialis, indicating that adaptive bone remodeling is a significant contributing factor in establishing mandibular bone density distributions in rorquals.

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 L(3.5)(body). 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.

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.

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.

We studied the mechanical properties of deep red aerobic muscle of yellowfin tuna (Thunnus albacares), using both in vivo and in vitro methods. In fish swimming in a water tunnel at 1-3 L s(-1) (where L is fork length), muscle length changes were recorded by sonomicrometry, and activation timing was quantified by electromyography. In some fish a tendon buckle was also implanted on the caudal tendon to measure instantaneous muscle forces transmitted to the tail. Between measurement sites at 0.45 to 0.65 L, the wave of muscle shortening progressed along the body at a relatively high velocity of 1.7 L per tail beat period, and a significant phase shift (31+/-4 degrees ) occurred between muscle shortening and local midline curvature, both suggesting red muscle power is directed posteriorly, rather than causing local body bending, which is a hallmark of thunniform swimming. Muscle activation at 0.53 L was initiated at about 50 degrees of the tail beat period and ceased at about 160 degrees , where 90 degrees is peak muscle length and 180 degrees is minimum length. Strain amplitude in the deep red fibres at 0.5 L was +/-5.4%, double that predicted from midline curvature analysis. Work and power production were measured in isolated bundles of red fibres from 0.5 L by the work loop technique. Power was maximal at 3-4 Hz and fell to less than 50% of maximum after 6 Hz. Based on the timing of activation, muscle strain, tail beat frequencies and forces in the caudal tendon while swimming, we conclude that yellowfin tuna, like skipjack, use their red muscles under conditions that produce near-maximal power output while swimming. Interestingly, the red muscles of yellowfin tuna are slower than those of skipjack, which corresponds with the slower tail beat frequencies and cruising speeds in yellowfin.