Cetacean tongue mobility and function: A comparative review.

Cetaceans are atypical mammals whose tongues often depart from the typical (basal) mammalian condition in structure, mobility, and function. Their tongues are dynamic, innovative multipurpose tools that include the world's largest muscular structures. These changes reflect the evolutionary history of cetaceans' secondary adaptation to a fully aquatic environment. Cetacean tongues play no role in mastication and apparently a greatly reduced role in nursing (mainly channeling milk ingestion), two hallmarks of Mammalia. Cetacean tongues are not involved in drinking, breathing, vocalizing, and other non-feeding activities; they evidently play no or little role in taste reception. Although cetaceans do not masticate or otherwise process food, their tongues retain key roles in food ingestion, transport, securing/positioning, and swallowing, though by different means than most mammals. This is due to cetaceans' aquatic habitat, which in turn altered their anatomy (e.g., the intranarial larynx and consequent soft palate alteration). Odontocetes ingest prey via raptorial biting or tongue-generated suction. Odontocete tongues expel water and possibly uncover benthic prey via hydraulic jetting. Mysticete tongues play crucial roles driving ram, suction, or lunge ingestion for filter feeding. The uniquely flaccid rorqual tongue, not a constant volume hydrostat (as in all other mammalian tongues), invaginates into a balloon-like pouch to temporarily hold engulfed water. Mysticete tongues also create hydrodynamic flow regimes and hydraulic forces for baleen filtration, and possibly for cleaning baleen. Cetacean tongues lost or modified much of the mobility and function of generic mammal tongues, but took on noteworthy morphological changes by evolving to accomplish new tasks.

Case studies on longitudinal mercury content in humpback whale (Megaptera novaeangliae) baleen.

Quantification of contaminant concentrations in baleen whales is important for individual and population level health assessments but is difficult due to large migrations and infrequent resighings. The use of baleen allows for a multiyear retrospective analysis of contaminant concentrations without having to collect repeated samples from the same individual. Here we provide case studies of mercury analysis using cold vapor atomic absorption spectroscopy in three individual humpback whales (Megaptera novaeangliae), a 44.5-year-old female and two males aged ≥35 and 66 years, over approximately three years of baleen growth. Mercury concentrations in the female's baleen were consistently 2-3 times higher than in either male. Age did not affect mercury concentrations in baleen; the younger male had comparable levels to the older male. In the female, mercury concentrations in the baleen did not change markedly during pregnancy but mercury did spike during the first half of lactation. Stable isotope profiles suggest that diet likely drove the female's high mercury concentrations. In conclusion, variations in baleen mercury content can be highly individualistic. Future studies should compare sexes as well as different populations and species to determine how the concentrations of mercury and other contaminants vary by life history parameters and geography.

The brain limit.

How fast the brain and muscles can respond to information about prey location constrains visual and echolocating predators in similar ways.

Structure and properties of baleen in the Southern right (Eubalaena australis) and Pygmy right whales (Caperea marginata).

Baleen is a resilient and keratinised filter-feeding structure attached to the maxilla of mysticete whales. It is strong and tough, yet a pliant and resilient material, that withstands extreme pressures in the oral cavity during feeding. We investigated the structure, water content, wettability and mechanical properties of baleen of the Southern right (SRW) and Pygmy right whales (PRW), to understand the effects of hydration on the physical and mechanical properties of baleen. Sixty 25 × 15mm baleen subsamples were prepared from one individual of SRW and PRW. Half were hydrated in circulated natural seawater for 21 days and half were dry. Water content analysis showed that SRW baleen was 21.2% water weight and PRW was 26.1%. Wettability testing indicated that surfaces of both hydrated and dried SRW and PRW baleen were hydrophilic, with hydrated samples of both species having lower contact angle values. For the SRW, the average contact angle of hydrated baleen was 40° ± 13.2 and 73° ± 6 for dried samples. Hydrated PRW baleen had an average contact angle of 44° ± 15.3, which was lower than in dried samples (74° ± 2.9). Three-point bending mechanical tests showed that the average maximum flexural stress of dried SRW (134.1 ± 34.3 MPa) and PRW samples (117.8 ± 22.3 MPa) were significantly higher than those of hydrated SRW (25.7 ± 6.3 MPa) and PRW (19.7 ± 4.8 MPa) baleen. Scanning electron microscope images showed the stratification of the outer cortical layer, with cross-linked keratin fibres observed within and between baleen keratin sheets. Hydrated baleen, as in its natural and functional behaviour, has greater flexibility and strength, attributes necessary for the complex filter feeding mechanism characteristic of whales. Hydration must be considered when addressing the physical and mechanical properties of baleen, especially when using dried museum specimens.

Whale jaw joint is a shock absorber.

The non-synovial temporomandibular jaw joint of rorqual whales is presumed to withstand intense stresses when huge volumes of water are engulfed during lunge feeding. Examination and manipulation of temporomandibular joints (TMJs) in fresh carcasses, plus CT scans and field/lab mechanical testing of excised tissue blocks, reveals that the TMJ's fibrocartilage pad fully and quickly rebounds after shrinking by 68-88% in compression (by axis) and stretching 176-230%. It is more extensible along the mediolateral axis and less extensible dorsoventrally, but mostly isotropic, with collagen and elastin fibers running in all directions. The rorqual TMJ pad compresses as gape increases. Its stiffness is hypothesized to damp acceleration, whereas its elasticity is hypothesized to absorb shock during engulfment, allow for rotation or other jaw motion during gape opening/closure, and aid in returning jaws to their closed position during filtration via elastic recoil with conversion of stored potential energy into kinetic energy.

Whale breaching says it loud and clear.

A whale leaping above the surface expends an enormous amount of energy, displaying its health and strength to peers and potential mates.

Multiaxial movements at the minke whale temporomandibular joint.

Mandibular mobility accompanying gape change in Northern and Antarctic minke whales was investigated by manipulating jaws of carcasses, recording jaw movements via digital instruments (inclinometers, accelerometers, and goniometers), and examining osteological and soft tissue movements via computed tomography (CT)-scans. We investigated longitudinal (α) rotation of the mandible and mediolateral displacement at the symphysis (Ω1 ) and temporomandibular joint (Ω2 ) as the mouth opened (Δ). Results indicated three phases of jaw opening. In the first phase, as gape increased from zero to 8°, there was slight (<1°) α and Ω rotation. As gape increased between 20 and 30°, the mandibles rotated slightly laterally (Mean 3°), the posterior condyles were slightly medially displaced (Mean 4°), and the anterior ends at the symphysis were laterally displaced (Mean 3°). In the third phase of jaw opening, from 30° to full (≥90°) gape, these motions reversed: mandibles rotated medially (Mean 29°), condyles were laterally displaced (Mean 14°), and symphyseal ends were medially displaced (Mean 1°). Movements were observed during jaw manipulation and analyzed with CT-images that confirmed quantitative inclinometer/accelerometer data, including the unstable intermediate (Phase 2) position. Together these shifting movements maintain a constant distance for adductor muscles stretched between the skull's temporal fossa and mandible's coronoid process. Mandibular rotation enlarges the buccal cavity's volume as much as 36%, likely to improve prey capture in rorqual lunge feeding; it may strengthen and stabilize jaw opening or closure, perhaps via a simple locking or unlocking mechanism. Rotated lips may brace baleen racks during filtration. Mandibular movements may serve a proprioceptive mechanosensory function, perhaps via the symphyseal organ, to guide prey engulfment and water expulsion for filtration.

Pectoral herding: an innovative tactic for humpback whale foraging.

Humpback whales (Megaptera novaeangliae) have exceptionally long pectorals (i.e. flippers) that aid in shallow water navigation, rapid acceleration and increased manoeuvrability. The use of pectorals to herd or manipulate prey has been hypothesized since the 1930s. We combined new technology and a unique viewing platform to document the additional use of pectorals to aggregate prey during foraging events. Here, we provide a description of 'pectoral herding' and explore the conditions that may promote this innovative foraging behaviour. Specifically, we analysed aerial videos and photographic sequences to assess the function of pectorals during feeding events near salmon hatchery release sites in Southeast Alaska (2016-2018). We observed the use of solo bubble-nets to initially corral prey, followed by calculated movements to establish a secondary boundary with the pectorals-further condensing prey and increasing foraging efficiency. We found three ways in which humpback whales use pectorals to herd prey: (i) create a physical barrier to prevent evasion, (ii) cause water motion to guide prey towards the mouth, and (iii) position the ventral side to reflect light and alter prey movement. Our findings suggest that behavioural plasticity may aid foraging in changing environments and shifts in prey availability. Further study would clarify if 'pectoral herding' is used as a principal foraging tool by the broader humpback whale population and the conditions that promote its use.

Oil adsorption does not structurally or functionally alter whale baleen.

Mysticete whales filter small prey from seawater using baleen, a unique keratinous oral tissue that grows from the palate, from which it hangs in hundreds of serial plates. Laboratory experiments testing effects of oils on material strength and flexibility, particle capture and tissue architecture of baleen from four mysticete species (bowhead, Balaena mysticetus; North Atlantic right, Eubalaena glacialis; fin, Balaenoptera physalus; humpback, Megaptera novaeangliae) indicate that baleen is hydrophilic and oleophobic, shedding rather than adsorbing oil. Oils of different weights and viscosities were tested, including six petroleum-based oils and two fish or plankton oils of common whale prey. No notable differences were found by oil type or whale species. Baleen did not adsorb oil; oil was readily rinsed from baleen by flowing water, especially from moving fringes. Microscopic examination shows minimal wrinkling or peeling of baleen's cortical keratin layers, probably due to oil repelling infiltrated water. Combined results cast doubt on fears of baleen fouling by oil; filter porosity is not appreciably affected, but oil ingestion risks remain. Particle capture studies suggest potentially greater danger to mysticetes from plastic pollution than oil.

New views of humpback whale flow dynamics and oral morphology during prey engulfment.

The rise of inexpensive, user-friendly cameras and editing software promises to revolutionize data collection with minimal disturbance to marine mammals. Video sequences recorded by aerial drones and GoPro cameras provided close-up views and unique perspectives of humpback whales engulfing juvenile salmon at or just below the water surface in Southeast Alaska and Prince William Sound. Although humpback feeding is famous for its flexibility, several stereotyped events were noted in the 47 lunges we analyzed. Engulfment was rapid (mean 2.07 s), and the entrance through which the tongue inverts into the ventral pouch was seen as water rushes in. Cranial elevation was a major contributor to gape, and pouch contraction sometimes began before full gape closure, with reverberating waves indicating rebounding flow of water within the expanded pouch. Expulsion of filtered water began with a small splash at the anterior of the mouth, followed by sustained excurrent flow in the mouth's central or posterior regions. Apart from a splash of rebounding water, water within the mouth was surprisingly turbulence-free during engulfment, but submersion of the whale's head created visible surface whirlpools and vortices which may aggregate prey for subsequent engulfment.

Slick, Stretchy Fascia Underlies the Sliding Tongue of Rorquals.

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.

How do baleen whales stow their filter? A comparative biomechanical analysis of baleen bending.

Bowhead and right whale (balaenid) baleen filtering plates, longer in vertical dimension (≥3-4 m) than the closed mouth, presumably bend during gape closure. This has not been observed in live whales, even with scrutiny of video-recorded feeding sequences. To determine what happens to the baleen during gape closure, we conducted an integrative, multifactorial study including materials testing, functional (flow tank and kinematic) testing and histological examination. We measured baleen bending properties along the dorsoventral length of plates and anteroposterior location within a rack of plates via mechanical (axial bending, composite flexure, compression and tension) tests of hydrated and air-dried tissue samples from balaenid and other whale baleen. Balaenid baleen is remarkably strong yet pliable, with ductile fringes, and low stiffness and high elasticity when wet; it likely bends in the closed mouth when not used for filtration. Calculation of flexural modulus from stress/strain experiments shows that the balaenid baleen is slightly more flexible where it emerges from the gums and at its ventral terminus, but kinematic analysis indicates plates bend evenly along their whole length. Fin and humpback whale baleen has similar material properties but less flexibility, with no dorsoventral variation. The internal horn tubes have greater external and hollow luminal diameter but lower density in the lateral relative to medial baleen of bowhead and fin whales, suggesting a greater capacity for lateral bending. Baleen bending has major consequences not only for feeding morphology and energetics but also for conservation given that entanglement in fishing gear is a leading cause of whale mortality.

Oral cavity hydrodynamics and drag production in Balaenid whale suspension feeding.

Balaenid whales feed on large aggregates of small and slow-moving prey (predominantly copepods) through a filtration process enabled by baleen. These whales exhibit continuous filtration, namely, with the mouth kept partially opened and the baleen exposed to oncoming prey-laden waters while fluking. The process is an example of crossflow filtration (CFF) in which most of the particulates (prey) are separated from the substrate (water) without ever coming into contact with the filtering surface (baleen). This paper discusses the simulation of baleen filtration hydrodynamics based on a type of hydraulic circuit modeling commonly used in microfluidics, but adapted to the much higher Reynolds number flows typical of whale hydrodynamics. This so-called Baleen Hydraulic Circuit (BHC) model uses as input the basic characteristics of the flows moving through a section of baleen observed in a previous flume study by the authors. The model has low-spatial resolution but incorporates the effects of fluid viscosity, which doubles or more a whale's total body drag in comparison to non-feeding travel. Modeling viscous friction is crucial here since exposing the baleen system to the open ocean ends up tripling a whale's total wetted surface area. Among other findings, the BHC shows how CFF is enhanced by a large filtration surface and hence large body size; how it is carried out via the establishment of rapid anteroposterior flows transporting most of the prey-water slurry towards the oropharyngeal wall; how slower intra-baleen flows manage to transfer most of the substrate out of the mouth, all the while contributing only a fraction to overall oral cavity drag; and how these anteroposterior and intra-baleen flows lose speed as they approach the oropharyngeal wall.

Sling, Scoop, and Squirter: Anatomical Features Facilitating Prey Transport, Processing, and Swallowing in Rorqual Whales (Mammalia: Balaenopteridae).

Much is known about lunge feeding in balaenopterid whales, but many key aspects of structure, function, and behavior have not yet been explained in detail, especially with regard to concentrating, positioning, and swallowing large aggregations of prey. We describe a novel system of three integrated structural components, all of which are involved in sequential feeding activities (intraoral transport, filtration, and swallowing of prey) that follow lunge-feeding engulfment of prey-laden water in rorquals: (1) a hammock-like muscular sling comprising extrinsic lingual musculature along the midline of the ventral pouch; (2) the flattened scoop-like arrangement of caudal-most baleen plates converging in the oropharynx adjacent to the esophageal opening; and (3) a flow-diverting flange at the posterior dorsum of the lip, by a flow channel at the angle of the mouth. Subsequent to contraction of the ventral pouch and concomitant expulsion of the mouthful of ingested water, these three structures together, we contend, aid in (1) channeling prey posteriorly toward the esophageal opening; (2) concentrating prey as excess water is squeezed from (what is presumed to be) the slurry-like mixture of nektonic and/or planktonic prey and water; and (3) guiding prey into the isthmus of the fauces while simultaneously (4) facilitating expulsion of water. These related functions occur along with, and are in part achieved by, elevation and retraction of the tongue and oral floor. Given their presumed functional role, these systems are best described as a suite of integrated structural adaptations. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 300:2070-2086, 2017. © 2017 Wiley Periodicals, Inc.

Hydration affects the physical and mechanical properties of baleen tissue.

Baleen, an anisotropic oral filtering tissue found only in the mouth of mysticete whales and made solely of alpha-keratin, exhibits markedly differing physical and mechanical properties between dried or (as in life) hydrated states. On average baleen is 32.35% water by weight in North Atlantic right whales (Eubalaena glacialis) and 34.37% in bowhead whales (Balaena mysticetus). Baleen's wettability measured by water droplet contact angles shows that dried baleen is hydrophobic whereas hydrated baleen is highly hydrophilic. Three-point flexural bending tests of mechanical strength reveal that baleen is strong yet ductile. Dried baleen is brittle and shatters at about 20-30 N mm-2 but hydrated baleen is less stiff; it bends with little force and absorbed water is squeezed out when force is applied. Maximum recorded stress was 4× higher in dried (mean 14.29 N mm-2) versus hydrated (mean 3.69 N mm-2) baleen, and the flexural stiffness was >10× higher in dried (mean 633N mm-2) versus hydrated (mean 58 N mm-2) baleen. In addition to documenting hydration's powerful effects on baleen, this study indicates that baleen is far more pliant and malleable than commonly supposed, with implications for studies of baleen's structure and function as well as its susceptibility to oil or other hydrophobic pollutants.

Baleen Hydrodynamics and Morphology of Cross-Flow Filtration in Balaenid Whale Suspension Feeding.

The traditional view of mysticete feeding involves static baleen directly sieving particles from seawater using a simple, dead-end flow-through filtration mechanism. Flow tank experiments on bowhead (Balaena mysticetus) baleen indicate the long-standing model of dead-end filtration, at least in balaenid (bowhead and right) whales, is not merely simplistic but wrong. To recreate continuous intraoral flow, sections of baleen were tested in a flume through which water and buoyant particles circulated with variable flow velocity. Kinematic sequences were analyzed to investigate movement and capture of particles by baleen plates and fringes. Results indicate that very few particles flow directly through the baleen rack; instead much water flows anteroposteriorly along the interior (lingual) side of the rack, allowing items to be carried posteriorly and accumulate at the posterior of the mouth where they might readily be swallowed. Since water flows mainly parallel to rather than directly through the filter, the cross-flow mechanism significantly reduces entrapment and tangling of minute items in baleen fringes, obviating the need to clean the filter. The absence of copepods or other prey found trapped in the baleen of necropsied right and bowhead whales supports this hypothesis. Reduced through-baleen flow was observed with and without boundaries modeling the tongue and lips, indicating that baleen itself is the main if not sole agent of crossflow. Preliminary investigation of baleen from balaenopterid whales that use intermittent filter feeding suggests that although the biomechanics and hydrodynamics of oral flow differ, cross-flow filtration may occur to some degree in all mysticetes.

Baleen wear reveals intraoral water flow patterns of mysticete filter feeding.

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.

An intraoral thermoregulatory organ in the bowhead whale (Balaena mysticetus), the corpus cavernosum maxillaris.

The novel observation of a palatal retial organ in the bowhead whale (Balaena mysticetus) is reported, with characterization of its form and function. This bulbous ridge of highly vascularized tissue, here designated the corpus cavernosum maxillaris, runs along the center of the hard palate, expanding cranially to form two large lobes that terminate under the tip of the rostral palate, with another enlarged node at the caudal terminus. Gross anatomical and microscopic observation of tissue sections discloses a web-like internal mass with a large blood volume. Histological examination reveals large numbers of blood vessels and vascular as well as extravascular spaces resembling a blood-filled, erectile sponge. These spaces, as well as accompanying blood vessels, extend to the base of the epithelium. We contend that this organ provides a thermoregulatory adaptation by which bowhead whales (1) control heat loss by transferring internal, metabolically generated body heat to cold seawater and (2) protect the brain from hyperthermia. We postulate that this organ may play additional roles in baleen growth and in detecting prey, and that its ability to dissipate heat might maintain proper operating temperature for palatal mechanoreceptors or chemoreceptors to detect the presence and density of intraoral prey.

Flow-dependent porosity and other biomechanical properties of mysticete baleen.

Despite its vital function in a highly dynamic environment, baleen is typically assumed to be a static material. Its biomechanical and material properties have not previously been explored. Thus I tested sections of baleen from bowhead whales, Balaena mysticetus, and humpback whales, Megaptera novaeangliae, alone or in groups representing miniature 'racks', in a flow tank through which water and buoyant particles circulated with variable flow velocity. Kinematic sequences were recorded through an endoscopic camera or viewing window. One set of experiments investigated particle capture; another series analyzed biomechanical behavior, including fringe spacing, movement and interaction. Baleen fringe porosity directly correlates, in a mostly linear fashion, with velocity of incident water flow. However, undulation and interaction of fringes (especially of bowheads) at higher flow velocities can decrease porosity. Fringe porosity depends on distance from the baleen plate. Porosity also varies, with fringe length, by position along the length of an individual plate. Plate orientation, which varied from 0 to 90 deg relative to water flow, is crucial in fringe spacing and particle capture. At all flow velocities, porosity is lowest with plates aligned parallel to water flow. Turbulence introduced when plates rotate perpendicular to flow (as in cross-flow filtration) increases fringe interaction, so that particles more easily strike fringes yet more readily dislodge. Baleen of bowhead whales, which feed by continuous ram filtration, differs biomechanically from that of humpbacks, which use intermittent lunge filtration. The longer, finer fringes of bowhead baleen readily form a mesh-like mat, especially at higher flow velocities, to trap tiny particles.