Anatomical adaptations of aquatic mammals

Authors

  • Joy S. Reidenberg

    Corresponding author
    1. Center for Anatomy and Functional Morphology, Department of Medical Education, Mount Sinai School of Medicine, New York, New York
    • Center for Anatomy and Functional Morphology, Department of Medical Education, Mail Box 1007, Mount Sinai School of Medicine, 1 Gustave L. Levy Place, New York, NY 10029-6574
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Abstract

This special issue of the Anatomical Record explores many of the anatomical adaptations exhibited by aquatic mammals that enable life in the water. Anatomical observations on a range of fossil and living marine and freshwater mammals are presented, including sirenians (manatees and dugongs), cetaceans (both baleen whales and toothed whales, including dolphins and porpoises), pinnipeds (seals, sea lions, and walruses), the sea otter, and the pygmy hippopotamus. A range of anatomical systems are covered in this issue, including the external form (integument, tail shape), nervous system (eye, ear, brain), musculoskeletal systems (cranium, mandible, hyoid, vertebral column, flipper/forelimb), digestive tract (teeth/tusks/baleen, tongue, stomach), and respiratory tract (larynx). Emphasis is placed on exploring anatomical function in the context of aquatic life. The following topics are addressed: evolution, sound production, sound reception, feeding, locomotion, buoyancy control, thermoregulation, cognition, and behavior. A variety of approaches and techniques are used to examine and characterize these adaptations, ranging from dissection, to histology, to electron microscopy, to two-dimensional (2D) and 3D computerized tomography, to experimental field tests of function. The articles in this issue are a blend of literature review and new, hypothesis-driven anatomical research, which highlight the special nature of anatomical form and function in aquatic mammals that enables their exquisite adaptation for life in such a challenging environment. Anat Rec, 290:507–513, 2007. © 2007 Wiley-Liss, Inc.

Aquatic life poses many challenges for mammals that were originally adapted for life on land. As the evolutionary process of natural selection can only apply to modifying present structures, aquatic mammals bring a lot of terrestrial baggage to their aquatic existence. For one thing, they do not breathe water as fish do. Therefore, respiratory tract modifications are necessary to protect a system designed to function in air while excluding the ever-present surrounding water. Many of these adaptations have been previously described, for example, valvular nostrils that exclude water, and an intranarial larynx (Reidenberg and Laitman, 1987) that further protects the respiratory tract from water inundation during swallowing. Diving presents additional challenges, as ambient pressure rises with increased depth. Lung volumes collapse under the high pressures of a deep dive (Boyd, 1975; Ridgway and Howard, 1979). A jointed, collapsible rib cage allows compression of the thorax to accommodate the shrinking lungs. Skeletal muscles are adapted to maintain low levels of aerobic metabolism under the hypoxic conditions associated with diving (Kanatous et al., 2002). Elevated levels of myoglobin in skeletal muscles also increase oxygen retention, thus enabling longer dive times between breaths (Noren et al., 2001; Wright and Davis, 2006). The mass of blood vessels located in the dorsum of the thorax (retia thoracica) have been proposed to function during diving to accommodate for the collapsed lung volume, thereby preventing gross displacement of abdominal organs (Hui, 1975). Salinity presents another challenge, as marine mammals must main water and salt balance, despite the frequent influx of salt water they consume while swallowing prey. The kidney structure of cetaceans (whales, including dolphins and porpoises) and pinnipeds (seals, sea lions, walruses) is unusual, having a reniculate structure (Abdelbaki et al., 1984; Henk et al., 1986) not found in any other terrestrial mammals except bears, but does not appear to have a greater ability to concentrate urine (Ortiz, 2001). Rather, the apparent advantage of numerous independent renicules in marine mammals is limited tubule lengths in the necessarily large kidneys of gigantic mammals (Maluf and Gassman, 1998).

Navigation and prey detection systems are also modified. As many aquatic mammals need to hunt at night or in turbid or deep water, their sensory systems have accordingly evolved. Pinnipeds developed longer and more sensitive vibrissae that can pick up hydrodynamic trails (vibrations in water) of fish swimming, or relay information about water current flow and variations in substrate surfaces (Dehnhardt et al., 2001). Odontocetes (toothed whales) developed nasal structures that generate echolocation, enabling them to use sound to locate prey or navigate past obstacles (Cranford et al., 1996; Au et al., 2006).

Many marine mammals have modified their external shape, developing new propulsion mechanisms for locomotion in water. Seals use alternating horizontal sweeps of their hind flippers (Fish et al., 1988). Fur seals and sea lions “fly” underwater by beating their fore flippers (English, 1977; Feldkamp, 1987). Walruses sometimes use their tusks to grip the sea floor or ice and push their body forward with a downward nod of the head. Sirenians (manatees and dugongs) have lost their hind limbs, but can either propel themselves with their tail fluke(s) or walk along the sea or river floor with their forelimbs. Cetaceans have excelled in the attainment of streamlined form, and are thus the fastest swimmers. As with sirenians, cetaceans have lost appendages that detract from axial locomotion (hind limbs). Similarly to pinnipeds, they have modified extremities that assist with lift and braking (flippers). Cetaceans have also added new extensions that aid propulsion (flukes) or prevent roll or yaw (dorsal fin) while swimming with exaggerated pitch (dorsoventral bending).

Although most of the above-mentioned adaptations have been discussed at length in previous publications, the articles in this special issue present some new findings regarding aquatic adaptations. This special issue focuses on a common hypothesis: the described anatomical specialization confers a selective advantage to an aquatic existence. Demonstrating this relationship necessarily involves exploring how the adaptation functions in an aquatic environment. The studies presented examine a large array of extant and fossil, marine and fresh water, aquatic mammals. A variety of anatomical systems are explored, including digestive tract (teeth, tusks, baleen, tongue, pharyngeal spaces, stomach), the external form (integument and body shape, including flukes and flippers), musculoskeletal systems (cranial, mandibular, and cervical regions; postcranial axial and appendicular skeleton), nervous system (eye, ear, brain), and respiratory tract (larynx). Emphasis is placed on exploring anatomical function in the context of aquatic life. A range of techniques are used, including dissection, histology, electron microscopy, computerized tomography and 3D reconstructions, and experimental field work. The papers that follow in this issue are a blend of both review articles and new, hypothesis-driven anatomical research. These studies highlight the dramatic anatomical changes seen in the evolution from fossil ancestors to extant aquatic mammals. This special issue is a tribute to the unique anatomical forms and functions of aquatic mammals that enables their adaptation to life underwater.

UNDERWATER FORAGING

The first question that naturally comes to mind is “Why did some mammals become aquatic in the first place?” Uhen (2007, this issue) discusses the evolution of aquatic mammals, using both molecular and morphological data for Cetacea, Sirenia, Desmostylia, and Pinnipedia. He notes that re-entering the water occurred on at least seven different occasions. Specific changes occurred in the axial and appendicular skeleton that improved locomotion for aquatic foraging. Nostril, eye placement, rostrum, and dental morphology also changed, depending upon the need to forage while wading versus submersion. Although the end product of each of these evolutionary trajectories is vastly different, they all appear to be the result of natural selection for improved aquatic foraging. Terrestrial mammals from seven separate lineages thus re-invaded the water to fill a vacant niche: feeding in water.

The foraging mechanisms of fossil ancestors, however, do not always match present day species. Domning and Beatty (2007, this issue) compare fossil and modern dugongs in their tusk shape and cranial anatomy, and explore whether these specializations indicate tusk use in feeding. Fossil dugongines exhibit cranial modifications that may have assisted downward and backward tusk cutting motions. The larger, more blade-like tusks of fossil dugongines are more effective at harvesting rhizomes. However, examination of microwear patterns in modern dugong tusks do not support that their use is necessary in feeding, although it does occasionally occur in large adult males. Tusk use in modern dugongs has thus changed radically from the ancestral pattern. As tusks are not essential for feeding in extant dugongs, the persistence of erupted tusks in males indicates a possible role in sexual selection or other social interactions.

Feeding mechanisms are also examined in cetaceans in this issue. MacLeod et al. (2007, this issue) describe the relationship between prey size and skull asymmetry. While most mammals are bilaterally symmetrical, most odontocetes are characterized by directional asymmetry of the skull (i.e., the direction of deviation is consistent). The narial apertures are asymmetrically positioned on the left side of the head (Yurick and Gaskin, 1988). Above the skull, this asymmetry is also evident in soft tissue structures that are used in generating echolocation signals (Cranford et al., 1996). The different sized nasal diverticulae, fat bodies, and valvular flaps may enable generation of two different sounds simultaneously. While this asymmetry may be useful for echolocation signal generation, it is suggested that echolocation is an overlay on asymmetry developed initially in conjunction with feeding needs. Below the skull, the left-shifted nares correspond to a left-shifted larynx. A larynx positioned asymmetrically on the left side collapses the left piriform sinus (lateral food channel, but simultaneously provides a larger piriform sinus on the right side; Reidenberg and Laitman, 1994). This should enable asymmetric odontocetes to swallow larger prey than their symmetric counterparts. MacLeod et al. (2007, this issue) test this hypothesis by examining the relationship between skull asymmetry relative to skull size and maximum relative prey size consumed. The strong positive correlation indicates that as odontocete nasal asymmetry increases, so does the size of the prey they can consume. This is an obvious adaptation to feeding in general, and to aquatic existence in particular, as odontocetes swallow their prey whole without processing. Therefore, more energy is gained by consuming one large prey item for the same amount of effort as is expended to catch one small prey item.

Underwater feeding poses an additional challenge: predators need to engulf prey while sorting it from the surrounding aquatic milieu. In cetaceans, movements of the hyoid apparatus play an important role in both drawing prey into the oral cavity and enlarging the piriform sinus (particularly on the right side) for swallowing prey whole (Reidenberg and Laitman, 1994). In addition, the tongue plays an important role in squeezing water out of the mouth. Werth's (2007, this issue) study of the hyolingual apparatus, particularly the tongue, in cetaceans shows aquatic specializations that relate to thermoregulation. There are counter current vessels in the tongue that control heat loss to the water in the oral cavity. Species-specific differences in musculoskeletal features of the hyolingual apparatus are related to the mode of feeding used: suction, raptorial prehension, continuous filtering, and engulfing with straining. Odontocetes have a small, rigid mouth, enlarged hyoid apparatus, and hypertrophied tongue muscles. Grasping prey is much like the game “bobbing for apples”—and old-fashioned New England tradition in which a person dunks their face into a bucket of water with floating apples and tries to grasp one with their teeth. In most cases, the smooth-sided apple eludes capture because it simply slides out of the grasp of the teeth and forward of the water pressure generated by the closing mouth. Odontocetes, faced with a similar problem while feeding underwater, developed a unique mechanism to trap slippery prey (e.g., fish, squid) in their mouth. They use their hyoid and tongue as a piston: a sudden retraction generates negative pressure in the mouth which, in turn, draws prey into the oral cavity. In some cetaceans, the large tongue is also used for grasping and manipulating prey. Mysticetes (baleen whales) use two different modes of filter feeding. Balaenid mysticetes (right and bowhead whales) are continuous strainers. They swim forward with their mouth open, constantly taking in water with small prey at the front of the mouth while streaming excess water out of the lateral–caudal edge of the gape. Their tongue is larger and stiff, and may function to direct water flow through the mouth. Balaenopterid mysticetes (rorqual whales, which possess ventral throat pleats), expand the floor of the oral cavity to engulf water containing schools of small fish or krill, and then expel water through their baleen plates. The baleen serves as a filter, allowing water to pass through while trapping the small prey. These whales need a highly mobile tongue that can flatten and expand to accommodate the distention of the oral cavity. The tongue may also aid in wiping prey off of the baleen plates.

Although baleen is an aquatic adaptation that enables filter feeding, it has an additional use in humpback whales. Air (technically, gas) from the respiratory tract may be released into the oral cavity and then pushed out through the sieve of the baleen plates, resulting in an underwater visual display called a bubble cloud (Reidenberg and Laitman, 2007a, this issue). Gas is released from the respiratory tract by removing the epiglottis of the larynx from its normal position behind the soft palate, and instead inserting it into the oral cavity. Gas can then flow from the lungs, trachea, or laryngeal sac into the oral cavity. As the floor of the mouth is contracted, and the gape of the mouth is held nearly closed, gas is forced superiorly and laterally against the racks of baleen. The criss-crossing fibers on the lingual surface of the stacked baleen plates serve to break up the gas passing through it into many small bubbles, which give the appearance of a fine, white mist underwater. This behavior is surprising, as it risks the protective arrangement of the intranarial larynx designed to keep water out of the respiratory tract. It is thus perhaps a unique example of an aquatic adaptation that compromises another aquatic adaptation. Despite this risk, there are many potential advantages to generating such a display. Bubble clouds may be a signal to conspecifics swimming close by—particularly in water with good visibility such as is found in the tropical areas where mating usually occurs. The bubbles may also help herd prey into a tighter schooling formation, making it easier to engulf larger numbers of prey during feeding. In addition, bubble clouds may be used as camouflage. In open water, there are no obstacles to hide behind. A bubble cloud may thus provide a visual barrier (similar to a bush or a smoke screen), that can block a predator's view of the whale while it takes evasive action. In addition, the bubbles may serve as an echoic barrier to predatory orcas, causing disruption or distortion of their echolocation signal (similar to a white noise generator or a sonar jamming device).

The exploration of digestive tract anatomy continues in this special issue with an examination of the stomach in the Ziphiidae, the family of rare beaked whales. Mead (2007, this issue) describes three morphological appearances of the stomach: generalized ziphiid stomach (1 main stomach, 1 pyloric stomach), derived stomach type I (2 main stomachs, 1 pyloric stomach), and derived stomach type II (2 main stomachs, 2 pyloric stomachs). A multiple chambered stomach is unusual in carnivores. However, although all cetaceans are carnivores, the presence of a multichambered stomach should not surprise us. Whales are, afterall, closely related to artiodactyls, which also have multichambered stomachs. While their multiple chambers may relate to the mechanical and enzymatic breakdown of an herbivorous diet (e.g., separation of food to be regurgitated and re-chewed as cud), it is unclear what functions multiple chambers play in the carnivorous ziphiids. Nevertheless, differences in the appearance of the three stomach morphologies appear to be useful for elucidating systematic relationships among the ziphiids.

EXTERNAL ANATOMY: INTEGUMENT AND BODY SHAPE

One obvious place to discover adaptations to an aquatic existence is to look at the point of contact between the aquatic environment and the aquatic mammal. Therefore, the integument and overall body shape is examined in this special issue. Fur originally functioned as a terrestrial modification to trap an insulating layer of air, providing camouflage, protection from abrasion or predatory injury, or shielding from the untraviolet rays of the sun. Fur in water, while providing all of the latter features, loses it ability to insulate and also generates increased drag while swimming. Aquatic mammals thus have developed oily furs that are relatively waterproof (e.g., polar bears, otters, seals, sea lions, beavers). Their fur may trap air, thus continuing to provide insulation even when wet. In some aquatic mammals, fur was lost in favor of a thicker, waterproof epidermis (e.g., whales, dolphins, porpoises, manatees, dugongs, walruses, hippopotomi). This change may be a response to hydrodynamic needs, such as drag reduction. The loss of air trapping for insulation necessitated the development of thickened fat layer called blubber.

Vascular plexuses also developed to enable counter current exchange, which conserves body heat centrally while allowing the periphery to remain cold. Cold is not the only thermal disadvantage to living in the water, however. Heat can also build up in overly insulated mammals when the ambient temperature rises at the water's surface or, in the case of semiaquatic mammals (e.g., pinnipeds), while on land. Heat dissipation is also necessary during exertion or during pregnancy. Vascular adaptations channel excess heat from locomotor muscles or the reproductive organs to large flat surfaces (flukes, flippers, fin) which act as radiators (Rommel et al., 1992, 1993, 1995, 2001). Oral rete allow cetaceans to regulate heat loss from the oral cavity (Werth, 2007, this issue).

Changes in body shape also contribute to heat conservation/radiation. Terrestrial mammals living in cold environments tend to have shortened extremities (e.g., limbs, ears, muzzles) to restrict heat radiation, while the opposite is true in hot environments. There are several examples of cold water adapted marine mammals that also display shortened extremities and rotund body shapes (e.g., walrus, bowhead whale, right whale, beluga whale).

Reeb et al. (2007, this issue) examine the integument of the southern right whale, one of the cold water adapted marine mammals. Southern right whales have hairs, but they no longer function to trap air. Rather, they may have a tactile function and are probably used as vibrissae to detect changes in prey density. Epidermal specializations (e.g., callosities) provide barriers against mechanical injury. There were lipid droplets associated with the nucleus, which may facilitate the energetics of nuclear metabolism. This may be an adaptation to support cellular metabolism during extreme cold exposure (e.g., deep diving, polar waters) when the arterial supply of nutrients to the skin is reduced to conserve heat. Not surprisingly, these whales also have a thick, insulatory integument, which acts as a thermoregulatory adaptation to a cold environment. There is a highly folded junction between the epidermis and the dermis, a fat-free zone of collagen fibers in the reticular dermal layer, and elastic fiber networks within the dermal and hypodermal layers. These features may reduce hydrodynamic friction, enabling the skin to deform under pressure to increase hydrodynamic flow of water over the body during high speed swimming.

LOCOMOTION

The thicker substrate of water creates resistance to locomotion compared with air, thus necessitating the need for a fusiform body shape that decreases drag in pelagic marine mammals. Aquatic adaptations can also be seen in the hydrodynamic shapes of the structures used to generate thrust in cetaceans: tail flukes. Fish et al. (2007, this issue) uses CT scans to describe the thickness ratios of cetacean flukes. He found that their shape was effective at reducing drag while moving at high speeds. Fluke shapes were also found to be ideal for reducing the tendency for flow to separate from the fluke surface. This feature, combined with the relatively large leading edge radius, results in a shape that generates greater lift and helps to delay stall. Interestingly, cetacean flukes were better at generating lift than engineered foils, thus showing that we still have a lot to learn from nature.

Sirenians also use a tail for propulsion which, similarly to cetaceans, consists of a fluke (or flukes) that are supported only by a midline skeleton of caudal vertebrae. Dugongs have two mirror-image flukes, similar in shape to the double flukes of cetaceans. Manatees have a single, paddle-shaped fluke. Of interest, the evolution of tail flukes in sirenians is convergent with the evolution of tail flukes in cetaceans. Buchholtz et al. (2007, this issue) indicates that fluke evolution developed before the separation of manatees and dugongs.

Caudal propulsion in manatees is facilitated by changes in both the shape and number of bones in the axial skeleton. Buchholtz et al. (2007, this issue) describe the anatomy of the Florida manatee vertebral column in comparison to those of African manatees and dugongs. Manatee vertebral counts and morphology are unusual compared with both terrestrial mammals and other sirenians. Aquatic adaptations can be seen in the compressed cervical and elongate thoracic vertebrae, short neural spine length, variation and reduction of the lumbus, low precaudal count, lack of a sacral series, and discontinuity within the caudal series. These traits all contribute to aquatic locomotion. The shortened neck limits head mobility, decreases drag, and effectively repositions the flippers more anteriorly. Reduction in precaudal vertebrae count and elongation of dorsal vertebrae lowers the number of intervertebral flexion points, thus stabilizing the column while elongating the body. Short neural spines and flat centrum faces also decrease vertebral flexion and increase stability. Caudal vertebrae have smaller centra and neural spines, which increase flexibility, and small posteriorly inclined transverse processes, which serve as an anchor for muscles of locomotion. Rounded centrum faces, absent zygapophyses, and reduction of both neural spines and transverse processes facilitate flexibility in the fluke region, a trait necessary for caudal propulsion. These traits enable axial locomotion, specifically dorsoventral bending.

Changes in buoyancy are a challenge for aquatic locomotion: a shallow-water wading or bottom-feeding animal needs to be heavier than water to retain traction on the substrate (e.g., moose) or stay submerged to feed (e.g., manatee), an animal living at the surface needs to float (e.g., sea otter), and an open-water free-swimming animal needs to be neutrally buoyant to rise and fall within the water column (e.g., dolphin). Gray et al. (2007, this issue) discuss the evolution of buoyancy control mechanisms as evidenced by microstructural changes in the skeletal system, from analysis of ribs in five fossil cetacean families. Paradoxically, this aquatic specialization predates gross anatomical changes associated with swimming in archaeocetes. There was a shift from the typical terrestrial form, to osteopetrosis and pachyosteosclerosis, and then to osteoporosis in the first quarter of cetacean evolutionary history. High bone density is a static buoyancy mechanism that provides ballast and is found in bottom feeders such as sirenians. Low bone density is associated with dynamic buoyancy control mechanisms (e.g., amount of gas in the lungs), and is found in mammals living in deep water.

Appendicular osteology is also highly modified in aquatic mammals. Unlike caudal flukes, which only have midline skeletal support, the external form of a flipper is dependent upon its underlying skeletal structure. Flipper shape reflects functional locomotor requirements to increase lift, reduce drag, execute turns, and enable braking. Narrow, elongate flippers facilitate fast swimming while broad flippers aid in slow turns. Cooper et al. (2007, this issue) show that digit loss and digit positioning appear to underlie these disparate flipper shapes. The osteology of the cetacean flipper (consisting of the humerus, radius, ulna, carpals, metacarpals, and phalanges) also provides many clues regarding their evolution from a terrestrial ancestor with five digits. Cooper et al. (2007, this issue) describe differences in the number of digital rays in the two suborders of mysticetes and odontocetes. Digital ray I is reduced in most pentadactylous cetaceans and is completely lost in tetradactylous mysticetes. Five digits help support a broad flipper (e.g., right whales), while four digits closely appressed are seen in narrow, elongated flippers (e.g., humpback whales). Most odontocetes also reduce the number of phalangeal elements in digit V, while mysticetes typically retain the plesiomorphic condition of three phalanges. All cetaceans, however, exhibit an increased number of phalanges (hyperphalangy). Hyperphalangy and associated multiple interphalangeal joints may smooth the leading edge contour of the flipper, thereby helping to distribute leading edge forces.

Flippers are also found in other marine mammals, including sirenians and pinnipeds. Sirenians may use them to crawl along the river bed or the sea floor. Unlike cetaceans and sirenians, the pinnipeds are among the group of amphibious mammals (i.e., mammals that regularly leave the water for extended periods of time). As such, these aquatic mammals must adapt to the change in substrate while entering or exiting water, and thus retain the ability to locomote both on land and in water. Sea lions, walruses, and seals all possess both fore and hind flippers that contain many of the same, although highly modified, musculoskeletal elements as terrestrial forelimbs (English, 1976). Sea lions, despite their highly modified extremities, can still raise themselves on both their fore and hind flippers to walk and even run on land. Seals, however, do not usually use their extremities on land. Rather, they use an unusual rolling motion, propelling their body forward through the progression of a dorsoventral body wave—similar to the alternating sideways movements of a snake, but turned 90 degrees into the vertical plane. Their movement is reminiscent of the up-and-down body wave many aquatic mammals use to swim underwater (e.g., dolphins, manatees). Nonflippered aquatic mammals that have retained four weight-bearing limbs (e.g., polar bear, otter, beaver, muskrat) can walk on land with a quadrupedal gait similar to their fully terrestrial relatives (Tarasoff et al., 1972). Some mammals limit their aquatic exposure only to wading in water (e.g., moose). This allows them to reduce the effects of friction by keeping their trunk out of the water (enabled by having long limbs) and reducing the surface area of the limbs (i.e., skinny legs). Hippos, however, keep most of their body submerged while in water and have rather thick extremities.

Fisher et al. (2007, this issue) discuss adaptations in forelimb of the pygmy hippo that enable them to move quickly in water despite their rotund habitus. Unlike most other aquatic mammals, pygmy hippos do not swim, but rather walk on muddy substrates. Propelling the trunk through the high frictional resistance of water thus requires robust musculature, compared with that of quadrupedal land mammals such as the closely related artiodactyls. In addition, pygmy hippos bear weight on all of their toes and can prevent the toes from splaying. These adaptations enable them to walk on the soft surfaces of a muddy substrate, as is found on the bottoms or edges of lakes or rivers. Hippos retain several primitive muscles, thus indicating their early evolutionary divergence from Artiodactyla. This divergence may also be closely allied to the divergence of Cetacea, thus explaining the molecular data linking hippos and cetaceans as closely related groups.

BRAIN, EYE, AND COMMUNICATION SYSTEMS

Cetaceans possess among the largest brains, both in absolute mass and relative to body size. It has been suggested that the large brains are an aquatic adaptation, particularly in echolocating odontocetes. Marino (2007, this issue) addresses this relationship in a study comparing brain size (as measured by encephalization quotient, which accounts for body size) in fossil and modern aquatic mammals. She concludes that brain size is independent of aquatic existence, as large brains developed in cetaceans well after they became aquatic. Furthermore, other aquatic mammals (e.g., pinnipeds, sirenians) do not possess markedly enlarged brains, complex gyrification patterns, or high encephalization levels compared with odontocete brains. Echolocation alone cannot account for all of these changes, as terrestrial echolocators (e.g., bats) are not highly encephalized. Rather, Marino postulates that the high encephalization level of odontocetes is more likely related to their complex social structure.

While brain size may not reflect aquaticism, other nervous tissues do. The eye, which is technically an extension of the brain, exhibits several specializations in aquatic mammals. Mass and Supin (2007, this issue) review eye anatomy in four aquatic groups: cetaceans, pinnipeds, sirenians, and sea otters. They found anatomical differences that correspond to species-specific aquatic adaptations and behaviors. Aquatic mammals use different mechanisms to achieve aerial versus submerged emmetropia (refraction of light to focus on the retina). These corrections occur due to species-specific differences at the cornea or the lens. Pupil shapes correspond with variations in depth-dependent light exposure. Retina composition is similar to nocturnal terrestrial mammals, which is not surprising because aquatic mammals are exposed to low light conditions underwater. Cetaceans exhibit two areas of ganglion-cell concentration (the best-vision areas) located in the temporal and nasal quadrants, while pinnipeds, sirenians, and sea otters have only one such area.

Aquatic specializations are also apparent in the hearing apparatus of aquatic mammals. The terrestrial ear depends upon sound waves in air being collected by the pinna, traveling though the auditory meatus, causing vibrating of a tympanic membrane. These vibrations are then transmitted through an ossicular chain to the oval window, where vibrations set the inner ear membranes and fluid into motion, causing bending of hair cells, which in turn, transmit an electrical signal that the brain interprets as sound. Underwater hearing poses technical challenges, as sound waves are propagated in a fluid medium. Submerged terrestrial mammals primarily hear through bone conduction. However, as terrestrial ears are not acoustically isolated from the skull, they cannot distinguish directionality of sound under water. Nummela at al. (2007, this issue) describe the evolution of underwater hearing in cetaceans, particularly the sound transmission mechanisms in six archaeocete families. They show that the pinna and external auditory meatus were replaced by the mandible and its associated fat pad, which transmit sound pressures to the tympanic plate (lateral wall of the bulla). Other changes include medial thickening of the tympanic bulla, functional replacement of the tympanic membrane by a bony plate, and changes in the orientation and shapes of the ossicles. In addition, the tympanoperiotic complex becomes acoustically isolated from the skull by means of the development of air sinuses. This acoustic isolation prevents bony conduction and, therefore, preserves stereo hearing by means of mandibular transmission.

Hearing sensitivity is examined in a particularly rare cetacean, the North Atlantic right whale. As traditional behavioral or physiological hearing tests are not feasible with right whales, a functional model was developed based upon the ear anatomy. Parks et al. (2007, this issue) examined right whale ears by means of histologic measurements of the basilar membrane and 2D and 3D computerized tomography reconstructions of the cochlea. An estimated hearing range of 10 Hz–22 kHz based on established marine mammal models was obtained. This knowledge of the sound reception abilities of right whales is an important beginning to understanding their acoustic communication system and possible impacts of anthropogenic noise.

The last article of the special issue addresses the other end of the communication spectrum: sound generation. Reidenberg and Laitman (2007b, this issue) describe the discovery of a mysticete homolog of the vocal folds (the structures responsible for sound production in terrestrial mammals). This is a particularly exciting finding, as the sound source has remained undescribed for mysticetes. While vocal fold homologs have been identified in odontocetes (Reidenberg and Laitman, 1988), vocal folds were thought to be absent in baleen whales. Homology was determined by criteria that define vocal folds in terrestrial mammals. The vocal fold homologue is described as a U-shaped fold that is (1) able to function as a valve to regulate gas flow, (2) supported by arytenoid cartilages, (3) controlled by muscles that either directly insert on it or move the arytenoid cartilages, (4) is connected across the midline by a ligament, (5) receives motor and sensory innervation from the recurrent laryngeal nerve for the controlling musculature and mucosa caudal to the fold, and sensory innervation from the superior laryngeal nerve for the mucosa rostral and ventral to the fold, and (6) is located adjacent to a diverticulum called the laryngeal sac (likely derived from the laryngeal ventricles). Unlike the vocal folds of terrestrial mammals, which are perpendicular to airflow, the mysticete U-fold is oriented parallel to airflow. In this position, it can regulate airflow into/out of the laryngeal sac, and vibration of its edges may generate sounds. The size and complexity of the mysticete larynx indicates an organ with multiple functions in addition to sound generation, including protection during breathing/swallowing, and airflow/gas pressure control in the respiratory spaces.

CONCLUSIONS

The articles in this special issue draw from several anatomical disciplines to present both the latest discoveries in aquatic mammal research as well as some thoughtful and thorough evolutionary and systems-based reviews. It is hoped that, after reading this collection, one will have a greater understanding of how much these animals have changed through the effects of natural selection from their terrestrial ancestors, through the various fossil intermediate forms to the diversity of extant aquatic mammals we have today. Knowledge of their unusual specializations will hopefully inspire us to copy nature in the development of new technologies. For example, continued investigations on flukes, flippers, axial movements, feeding mechanics, skin, and body shape may lead to development of more efficient hydrodynamic designs for water- and aircraft. Further study of how aquatic mammals regulate buoyancy, control bone density, or manage dramatic changes in temperature and pressure as they rise and fall in the water column may lead to new treatments for osteoporosis or the invention of protective gear for exposure to the extreme environmental changes of high and low altitude, space, or ocean depths. A more complete understanding of neural organization, underwater vision, or sound generation and sound reception mechanisms may lead to the creation of better artificial sensory systems. There is so much we still have to learn about aquatic mammals. This is an exciting time to be a marine mammal scientist.

A brief note about conservation. Many of the aquatic mammals discussed in this issue are critically endangered. Unfortunately, people only protect what they know. Publications such as this, however, enable us to fulfill our duty as scientists to help educate the public with scientific facts about these splendid animals. After reading about all the phenomenal adaptations of aquatic mammals presented here, I hope you will join me not only in a new appreciation for how special these animals truly are, but also in a renewed commitment to help protect them from extinction.

Acknowledgements

I thank the contributors to this issue for all their hard work in producing outstanding pieces. I am in debt to those reviewers who spent numerous hours reviewing and providing helpful critiques of the papers, thereby vastly improving the content of this special issue. A special thank you goes to the editor, Kurt Albertine, for encouraging and promoting publication of high quality, hypothesis-driven anatomical research. My deepest gratitude goes to Jeff Laitman, Associate Editor, for his invaluable guidance, helpful advice, immeasurable support, abounding encouragement, and enthusiastic faith in my ability to “pull off” this endeavor. He continues to be a never-failing lighthouse, mentoring my scientific career through the turbulent waters of academic life.

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