Anatomical Adaptations of AquaticMammals

JOY S. REIDENBERG*

Center for Anatomy and Functional Morphology, Department of Medical Education,Mount Sinai School of Medicine, New York, New York

ABSTRACTThis special issue of the Anatomical Record explores many of the an-

atomical adaptations exhibited by aquatic mammals that enable life inthe water. Anatomical observations on a range of fossil and living marineand freshwater mammals are presented, including sirenians (manateesand dugongs), cetaceans (both baleen whales and toothed whales, includ-ing dolphins and porpoises), pinnipeds (seals, sea lions, and walruses),the sea otter, and the pygmy hippopotamus. A range of anatomical sys-tems 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), digestivetract (teeth/tusks/baleen, tongue, stomach), and respiratory tract (larynx).Emphasis is placed on exploring anatomical function in the context ofaquatic life. The following topics are addressed: evolution, sound produc-tion, sound reception, feeding, locomotion, buoyancy control, thermoregu-lation, cognition, and behavior. A variety of approaches and techniquesare used to examine and characterize these adaptations, ranging fromdissection, 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, hy-pothesis-driven anatomical research, which highlight the special natureof anatomical form and function in aquatic mammals that enables theirexquisite adaptation for life in such a challenging environment. � 2007Wiley-Liss, Inc. Anat Rec, 290:507–513, 2007. � 2007 Wiley-Liss, Inc.

Key words: aquatic; adaptation; anatomy; marine mammal;sirenian; cetacean; pinniped; evolution

Aquatic life poses many challenges for mammals thatwere originally adapted for life on land. As the evolution-ary process of natural selection can only apply to modify-ing present structures, aquatic mammals bring a lot ofterrestrial baggage to their aquatic existence. For onething, they do not breathe water as fish do. Therefore, re-spiratory tract modifications are necessary to protect asystem designed to function in air while excluding theever-present surrounding water. Many of these adapta-tions have been previously described, for example, valvu-lar nostrils that exclude water, and an intranarial larynx(Reidenberg and Laitman, 1987) that further protectsthe respiratory tract from water inundation during swal-lowing. Diving presents additional challenges, as ambi-ent pressure rises with increased depth. Lung volumescollapse under the high pressures of a deep dive (Boyd,

1975; Ridgway and Howard, 1979). A jointed, collapsiblerib cage allows compression of the thorax to accommo-date the shrinking lungs. Skeletal muscles are adaptedto maintain low levels of aerobic metabolism under thehypoxic conditions associated with diving (Kanatous

*Correspondence to: Joy S. Reidenberg, Center for Anatomyand Functional Morphology, Department of Medical Education,Mail Box 1007, Mount Sinai School of Medicine, 1 Gustave L.Levy Place, New York, NY 10029-6574.E-mail: joy.reidenberg@mssm.edu

Received 13 March 2007; Accepted 13 March 2007

DOI 10.1002/ar.20541Published online in Wiley InterScience (www.interscience.wiley.com).

� 2007 WILEY-LISS, INC.

THE ANATOMICAL RECORD 290:507–513 (2007)

et al., 2002). Elevated levels of myoglobin in skeletalmuscles also increase oxygen retention, thus enablinglonger dive times between breaths (Noren et al., 2001;Wright and Davis, 2006). The mass of blood vesselslocated in the dorsum of the thorax (retia thoracica) havebeen proposed to function during diving to accommodatefor the collapsed lung volume, thereby preventing grossdisplacement of abdominal organs (Hui, 1975). Salinitypresents another challenge, as marine mammals mustmain water and salt balance, despite the frequent influxof salt water they consume while swallowing prey. Thekidney structure of cetaceans (whales, including dolphinsand porpoises) and pinnipeds (seals, sea lions, walruses)is unusual, having a reniculate structure (Abdelbakiet al., 1984; Henk et al., 1986) not found in any other ter-restrial mammals except bears, but does not appear tohave a greater ability to concentrate urine (Ortiz, 2001).Rather, the apparent advantage of numerous independ-ent renicules in marine mammals is limited tubulelengths in the necessarily large kidneys of gigantic mam-mals (Maluf and Gassman, 1998).Navigation and prey detection systems are also modi-

fied. As many aquatic mammals need to hunt at nightor in turbid or deep water, their sensory systems haveaccordingly evolved. Pinnipeds developed longer andmore sensitive vibrissae that can pick up hydrodynamictrails (vibrations in water) of fish swimming, or relay in-formation about water current flow and variations insubstrate surfaces (Dehnhardt et al., 2001). Odontocetes(toothed whales) developed nasal structures that gener-ate echolocation, enabling them to use sound to locateprey 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 loco-motion in water. Seals use alternating horizontal sweepsof their hind flippers (Fish et al., 1988). Fur seals andsea lions ‘‘fly’’ underwater by beating their fore flippers(English, 1977; Feldkamp, 1987). Walruses sometimesuse their tusks to grip the sea floor or ice and push theirbody forward with a downward nod of the head. Sire-nians (manatees and dugongs) have lost their hindlimbs, but can either propel themselves with their tailfluke(s) or walk along the sea or river floor with theirforelimbs. Cetaceans have excelled in the attainment ofstreamlined form, and are thus the fastest swimmers.As with sirenians, cetaceans have lost appendages thatdetract from axial locomotion (hind limbs). Similarly topinnipeds, they have modified extremities that assistwith lift and braking (flippers). Cetaceans have alsoadded new extensions that aid propulsion (flukes) or pre-vent roll or yaw (dorsal fin) while swimming with exag-gerated 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 find-ings regarding aquatic adaptations. This special issuefocuses on a common hypothesis: the described anatomi-cal specialization confers a selective advantage to anaquatic existence. Demonstrating this relationship neces-sarily involves exploring how the adaptation functions inan aquatic environment. The studies presented examinea large array of extant and fossil, marine and freshwater, aquatic mammals. A variety of anatomical sys-tems are explored, including digestive tract (teeth, tusks,

baleen, tongue, pharyngeal spaces, stomach), the exter-nal form (integument and body shape, including flukesand flippers), musculoskeletal systems (cranial, mandib-ular, and cervical regions; postcranial axial and appen-dicular skeleton), nervous system (eye, ear, brain), andrespiratory tract (larynx). Emphasis is placed on explor-ing anatomical function in the context of aquatic life. Arange of techniques are used, including dissection, histol-ogy, electron microscopy, computerized tomography and3D reconstructions, and experimental field work. Thepapers that follow in this issue are a blend of both reviewarticles and new, hypothesis-driven anatomical research.These studies highlight the dramatic anatomical changesseen in the evolution from fossil ancestors to extantaquatic mammals. This special issue is a tribute to theunique anatomical forms and functions of aquatic mam-mals 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 firstplace?’’ Uhen (2007, this issue) discusses the evolution ofaquatic mammals, using both molecular and morphologi-cal data for Cetacea, Sirenia, Desmostylia, and Pinnipe-dia. He notes that re-entering the water occurred on atleast seven different occasions. Specific changes occurredin the axial and appendicular skeleton that improvedlocomotion for aquatic foraging. Nostril, eye placement,rostrum, and dental morphology also changed, depend-ing upon the need to forage while wading versus sub-mersion. Although the end product of each of these evo-lutionary trajectories is vastly different, they all appearto be the result of natural selection for improved aquaticforaging. Terrestrial mammals from seven separate line-ages 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 andBeatty (2007, this issue) compare fossil and moderndugongs in their tusk shape and cranial anatomy, andexplore whether these specializations indicate tusk usein feeding. Fossil dugongines exhibit cranial modifica-tions that may have assisted downward and backwardtusk cutting motions. The larger, more blade-like tusksof fossil dugongines are more effective at harvesting rhi-zomes. However, examination of microwear patterns inmodern dugong tusks do not support that their use isnecessary in feeding, although it does occasionally occurin large adult males. Tusk use in modern dugongs hasthus changed radically from the ancestral pattern. Astusks are not essential for feeding in extant dugongs, thepersistence of erupted tusks in males indicates a possiblerole in sexual selection or other social interactions.Feeding mechanisms are also examined in cetaceans in

this issue. MacLeod et al. (2007, this issue) describe therelationship between prey size and skull asymmetry.While most mammals are bilaterally symmetrical, mostodontocetes are characterized by directional asymmetryof the skull (i.e., the direction of deviation is consistent).The narial apertures are asymmetrically positioned onthe left side of the head (Yurick and Gaskin, 1988). Abovethe skull, this asymmetry is also evident in soft tissuestructures that are used in generating echolocation sig-nals (Cranford et al., 1996). The different sized nasal

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diverticulae, fat bodies, and valvular flaps may enablegeneration of two different sounds simultaneously. Whilethis asymmetry may be useful for echolocation signal gen-eration, it is suggested that echolocation is an overlay onasymmetry developed initially in conjunction with feedingneeds. Below the skull, the left-shifted nares correspondto a left-shifted larynx. A larynx positioned asymmetri-cally on the left side collapses the left piriform sinus (lat-eral food channel, but simultaneously provides a largerpiriform sinus on the right side; Reidenberg and Laitman,1994). This should enable asymmetric odontocetes toswallow larger prey than their symmetric counterparts.MacLeod et al. (2007, this issue) test this hypothesis byexamining the relationship between skull asymmetry rel-ative to skull size and maximum relative prey size con-sumed. The strong positive correlation indicates that asodontocete nasal asymmetry increases, so does the size ofthe prey they can consume. This is an obvious adaptationto feeding in general, and to aquatic existence in particu-lar, as odontocetes swallow their prey whole without proc-essing. Therefore, more energy is gained by consumingone large prey item for the same amount of effort as isexpended to catch one small prey item.Underwater feeding poses an additional challenge:

predators need to engulf prey while sorting it from thesurrounding aquatic milieu. In cetaceans, movements ofthe hyoid apparatus play an important role in bothdrawing prey into the oral cavity and enlarging the piri-form sinus (particularly on the right side) for swallowingprey whole (Reidenberg and Laitman, 1994). In addition,the tongue plays an important role in squeezing waterout of the mouth. Werth’s (2007, this issue) study of thehyolingual apparatus, particularly the tongue, in ceta-ceans shows aquatic specializations that relate to ther-moregulation. There are counter current vessels in thetongue that control heat loss to the water in the oralcavity. Species-specific differences in musculoskeletalfeatures of the hyolingual apparatus are related to themode of feeding used: suction, raptorial prehension, con-tinuous filtering, and engulfing with straining. Odonto-cetes have a small, rigid mouth, enlarged hyoid appara-tus, and hypertrophied tongue muscles. Grasping prey ismuch like the game ‘‘bobbing for apples’’—and old-fash-ioned New England tradition in which a person dunkstheir face into a bucket of water with floating applesand tries to grasp one with their teeth. In most cases,the smooth-sided apple eludes capture because it simplyslides out of the grasp of the teeth and forward of thewater pressure generated by the closing mouth. Odonto-cetes, faced with a similar problem while feeding under-water, developed a unique mechanism to trap slipperyprey (e.g., fish, squid) in their mouth. They use theirhyoid and tongue as a piston: a sudden retraction gener-ates negative pressure in the mouth which, in turn,draws prey into the oral cavity. In some cetaceans, thelarge tongue is also used for grasping and manipulatingprey. Mysticetes (baleen whales) use two different modesof filter feeding. Balaenid mysticetes (right and bowheadwhales) are continuous strainers. They swim forwardwith their mouth open, constantly taking in water withsmall prey at the front of the mouth while streamingexcess water out of the lateral–caudal edge of the gape.Their tongue is larger and stiff, and may function todirect water flow through the mouth. Balaenopteridmysticetes (rorqual whales, which possess ventral throat

pleats), expand the floor of the oral cavity to engulfwater containing schools of small fish or krill, and thenexpel water through their baleen plates. The baleenserves as a filter, allowing water to pass through whiletrapping the small prey. These whales need a highly mo-bile tongue that can flatten and expand to accommodatethe distention of the oral cavity. The tongue may alsoaid in wiping prey off of the baleen plates.Although baleen is an aquatic adaptation that enables

filter feeding, it has an additional use in humpbackwhales. Air (technically, gas) from the respiratory tractmay be released into the oral cavity and then pushed outthrough the sieve of the baleen plates, resulting in anunderwater visual display called a bubble cloud (Reiden-berg and Laitman, 2007a, this issue). Gas is releasedfrom the respiratory tract by removing the epiglottis ofthe larynx from its normal position behind the soft pal-ate, and instead inserting it into the oral cavity. Gas canthen flow from the lungs, trachea, or laryngeal sac intothe oral cavity. As the floor of the mouth is contracted,and the gape of the mouth is held nearly closed, gas isforced superiorly and laterally against the racks of ba-leen. The criss-crossing fibers on the lingual surface ofthe stacked baleen plates serve to break up the gas pass-ing through it into many small bubbles, which give theappearance of a fine, white mist underwater. This behav-ior is surprising, as it risks the protective arrangement ofthe intranarial larynx designed to keep water out of therespiratory tract. It is thus perhaps a unique example ofan aquatic adaptation that compromises another aquaticadaptation. Despite this risk, there are many potentialadvantages to generating such a display. Bubble cloudsmay be a signal to conspecifics swimming close by—par-ticularly in water with good visibility such as is found inthe tropical areas where mating usually occurs. The bub-bles may also help herd prey into a tighter schooling for-mation, making it easier to engulf larger numbers ofprey during feeding. In addition, bubble clouds may beused as camouflage. In open water, there are no obstaclesto hide behind. A bubble cloud may thus provide a visualbarrier (similar to a bush or a smoke screen), that canblock a predator’s view of the whale while it takes eva-sive action. In addition, the bubbles may serve as anechoic barrier to predatory orcas, causing disruption ordistortion of their echolocation signal (similar to a whitenoise generator or a sonar jamming device).The exploration of digestive tract anatomy continues

in this special issue with an examination of the stomachin the Ziphiidae, the family of rare beaked whales. Mead(2007, this issue) describes three morphological appear-ances of the stomach: generalized ziphiid stomach (1main stomach, 1 pyloric stomach), derived stomach typeI (2 main stomachs, 1 pyloric stomach), and derivedstomach type II (2 main stomachs, 2 pyloric stomachs).A multiple chambered stomach is unusual in carnivores.However, although all cetaceans are carnivores, thepresence of a multichambered stomach should not sur-prise us. Whales are, afterall, closely related to artiodac-tyls, which also have multichambered stomachs. Whiletheir multiple chambers may relate to the mechanicaland enzymatic breakdown of an herbivorous diet (e.g.,separation of food to be regurgitated and re-chewed ascud), it is unclear what functions multiple chambersplay in the carnivorous ziphiids. Nevertheless, differen-ces in the appearance of the three stomach morphologies

509ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS

appear to be useful for elucidating systematic relation-ships among the ziphiids.

EXTERNAL ANATOMY: INTEGUMENT ANDBODY SHAPE

One obvious place to discover adaptations to anaquatic existence is to look at the point of contactbetween the aquatic environment and the aquatic mam-mal. Therefore, the integument and overall body shapeis examined in this special issue. Fur originally func-tioned as a terrestrial modification to trap an insulatinglayer of air, providing camouflage, protection from abra-sion or predatory injury, or shielding from the untravio-let rays of the sun. Fur in water, while providing all ofthe latter features, loses it ability to insulate and alsogenerates increased drag while swimming. Aquaticmammals thus have developed oily furs that are rela-tively waterproof (e.g., polar bears, otters, seals, sealions, beavers). Their fur may trap air, thus continuingto provide insulation even when wet. In some aquaticmammals, fur was lost in favor of a thicker, waterproofepidermis (e.g., whales, dolphins, porpoises, manatees,dugongs, walruses, hippopotomi). This change may be aresponse to hydrodynamic needs, such as drag reduction.The loss of air trapping for insulation necessitated thedevelopment of thickened fat layer called blubber.Vascular plexuses also developed to enable counter

current exchange, which conserves body heat centrallywhile allowing the periphery to remain cold. Cold is notthe only thermal disadvantage to living in the water,however. Heat can also build up in overly insulatedmammals when the ambient temperature rises at thewater’s surface or, in the case of semiaquatic mammals(e.g., pinnipeds), while on land. Heat dissipation is alsonecessary during exertion or during pregnancy. Vascularadaptations channel excess heat from locomotor musclesor 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 regulateheat loss from the oral cavity (Werth, 2007, this issue).Changes in body shape also contribute to heat conser-

vation/radiation. Terrestrial mammals living in cold envi-ronments tend to have shortened extremities (e.g., limbs,ears, muzzles) to restrict heat radiation, while the oppo-site is true in hot environments. There are several exam-ples of cold water adapted marine mammals that also dis-play 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 wateradapted marine mammals. Southern right whales havehairs, but they no longer function to trap air. Rather,they may have a tactile function and are probably usedas vibrissae to detect changes in prey density. Epidermalspecializations (e.g., callosities) provide barriers againstmechanical injury. There were lipid droplets associatedwith the nucleus, which may facilitate the energetics ofnuclear metabolism. This may be an adaptation to sup-port cellular metabolism during extreme cold exposure(e.g., deep diving, polar waters) when the arterial supplyof nutrients to the skin is reduced to conserve heat. Notsurprisingly, these whales also have a thick, insulatoryintegument, which acts as a thermoregulatory adapta-tion to a cold environment. There is a highly folded junc-

tion between the epidermis and the dermis, a fat-freezone of collagen fibers in the reticular dermal layer, andelastic fiber networks within the dermal and hypodermallayers. These features may reduce hydrodynamic fric-tion, enabling the skin to deform under pressure toincrease hydrodynamic flow of water over the body dur-ing high speed swimming.

LOCOMOTION

The thicker substrate of water creates resistance tolocomotion compared with air, thus necessitating theneed for a fusiform body shape that decreases drag inpelagic marine mammals. Aquatic adaptations can alsobe seen in the hydrodynamic shapes of the structuresused to generate thrust in cetaceans: tail flukes. Fishet al. (2007, this issue) uses CT scans to describe thethickness ratios of cetacean flukes. He found that theirshape was effective at reducing drag while moving athigh speeds. Fluke shapes were also found to be idealfor reducing the tendency for flow to separate from thefluke surface. This feature, combined with the relativelylarge leading edge radius, results in a shape that gener-ates greater lift and helps to delay stall. Interestingly,cetacean flukes were better at generating lift than engi-neered foils, thus showing that we still have a lot tolearn from nature.Sirenians also use a tail for propulsion which, simi-

larly to cetaceans, consists of a fluke (or flukes) that aresupported only by a midline skeleton of caudal verte-brae. Dugongs have two mirror-image flukes, similar inshape to the double flukes of cetaceans. Manatees havea single, paddle-shaped fluke. Of interest, the evolutionof tail flukes in sirenians is convergent with the evolu-tion of tail flukes in cetaceans. Buchholtz et al. (2007,this issue) indicates that fluke evolution developedbefore the separation of manatees and dugongs.Caudal propulsion in manatees is facilitated by

changes in both the shape and number of bones in theaxial skeleton. Buchholtz et al. (2007, this issue)describe the anatomy of the Florida manatee vertebralcolumn in comparison to those of African manatees anddugongs. Manatee vertebral counts and morphology areunusual compared with both terrestrial mammals andother sirenians. Aquatic adaptations can be seen in thecompressed cervical and elongate thoracic vertebrae,short neural spine length, variation and reduction of thelumbus, low precaudal count, lack of a sacral series, anddiscontinuity within the caudal series. These traits allcontribute to aquatic locomotion. The shortened necklimits head mobility, decreases drag, and effectivelyrepositions the flippers more anteriorly. Reduction inprecaudal vertebrae count and elongation of dorsal ver-tebrae lowers the number of intervertebral flexionpoints, thus stabilizing the column while elongating thebody. Short neural spines and flat centrum faces alsodecrease vertebral flexion and increase stability. Caudalvertebrae have smaller centra and neural spines, whichincrease flexibility, and small posteriorly inclined trans-verse processes, which serve as an anchor for muscles oflocomotion. Rounded centrum faces, absent zygapophy-ses, and reduction of both neural spines and transverseprocesses facilitate flexibility in the fluke region, a traitnecessary for caudal propulsion. These traits enableaxial locomotion, specifically dorsoventral bending.

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Changes in buoyancy are a challenge for aquatic loco-motion: a shallow-water wading or bottom-feeding ani-mal needs to be heavier than water to retain traction onthe substrate (e.g., moose) or stay submerged to feed(e.g., manatee), an animal living at the surface needs tofloat (e.g., sea otter), and an open-water free-swimminganimal needs to be neutrally buoyant to rise and fallwithin the water column (e.g., dolphin). Gray et al.(2007, this issue) discuss the evolution of buoyancy con-trol mechanisms as evidenced by microstructuralchanges in the skeletal system, from analysis of ribs infive fossil cetacean families. Paradoxically, this aquaticspecialization predates gross anatomical changes associ-ated with swimming in archaeocetes. There was a shiftfrom the typical terrestrial form, to osteopetrosis andpachyosteosclerosis, and then to osteoporosis in the firstquarter of cetacean evolutionary history. High bone den-sity is a static buoyancy mechanism that provides bal-last and is found in bottom feeders such as sirenians.Low bone density is associated with dynamic buoyancycontrol 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 onlyhave midline skeletal support, the external form of aflipper is dependent upon its underlying skeletal struc-ture. Flipper shape reflects functional locomotor require-ments to increase lift, reduce drag, execute turns, andenable braking. Narrow, elongate flippers facilitate fastswimming while broad flippers aid in slow turns. Cooperet al. (2007, this issue) show that digit loss and digitpositioning appear to underlie these disparate flippershapes. The osteology of the cetacean flipper (consistingof the humerus, radius, ulna, carpals, metacarpals, andphalanges) also provides many clues regarding their evo-lution from a terrestrial ancestor with five digits. Cooperet al. (2007, this issue) describe differences in the num-ber of digital rays in the two suborders of mysticetesand odontocetes. Digital ray I is reduced in most penta-dactylous cetaceans and is completely lost in tetradacty-lous mysticetes. Five digits help support a broad flipper(e.g., right whales), while four digits closely appressedare seen in narrow, elongated flippers (e.g., humpbackwhales). Most odontocetes also reduce the number ofphalangeal elements in digit V, while mysticetes typi-cally retain the plesiomorphic condition of three pha-langes. All cetaceans, however, exhibit an increasednumber of phalanges (hyperphalangy). Hyperphalangyand associated multiple interphalangeal joints maysmooth the leading edge contour of the flipper, therebyhelping to distribute leading edge forces.Flippers are also found in other marine mammals,

including sirenians and pinnipeds. Sirenians may usethem to crawl along the river bed or the sea floor. Unlikecetaceans and sirenians, the pinnipeds are among thegroup of amphibious mammals (i.e., mammals that regu-larly leave the water for extended periods of time). Assuch, these aquatic mammals must adapt to the changein substrate while entering or exiting water, and thusretain the ability to locomote both on land and in water.Sea lions, walruses, and seals all possess both fore andhind flippers that contain many of the same, althoughhighly modified, musculoskeletal elements as terrestrialforelimbs (English, 1976). Sea lions, despite their highlymodified extremities, can still raise themselves on both

their fore and hind flippers to walk and even run onland. Seals, however, do not usually use their extremitieson land. Rather, they use an unusual rolling motion, pro-pelling their body forward through the progression of adorsoventral body wave—similar to the alternating side-ways movements of a snake, but turned 90 degrees intothe vertical plane. Their movement is reminiscent of theup-and-down body wave many aquatic mammals use toswim underwater (e.g., dolphins, manatees). Nonflip-pered 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 theirfully terrestrial relatives (Tarasoff et al., 1972). Somemammals limit their aquatic exposure only to wading inwater (e.g., moose). This allows them to reduce theeffects of friction by keeping their trunk out of the water(enabled by having long limbs) and reducing the surfacearea of the limbs (i.e., skinny legs). Hippos, however,keep most of their body submerged while in water andhave rather thick extremities.Fisher et al. (2007, this issue) discuss adaptations in

forelimb of the pygmy hippo that enable them to movequickly in water despite their rotund habitus. Unlikemost other aquatic mammals, pygmy hippos do notswim, but rather walk on muddy substrates. Propellingthe trunk through the high frictional resistance of waterthus requires robust musculature, compared with that ofquadrupedal land mammals such as the closely relatedartiodactyls. In addition, pygmy hippos bear weight onall of their toes and can prevent the toes from splaying.These adaptations enable them to walk on the soft sur-faces of a muddy substrate, as is found on the bottomsor edges of lakes or rivers. Hippos retain several primi-tive muscles, thus indicating their early evolutionarydivergence from Artiodactyla. This divergence may alsobe closely allied to the divergence of Cetacea, thusexplaining the molecular data linking hippos and ceta-ceans as closely related groups.

BRAIN, EYE, AND COMMUNICATIONSYSTEMS

Cetaceans possess among the largest brains, both inabsolute mass and relative to body size. It has been sug-gested that the large brains are an aquatic adaptation,particularly in echolocating odontocetes. Marino (2007,this issue) addresses this relationship in a study compar-ing brain size (as measured by encephalization quotient,which accounts for body size) in fossil and modernaquatic mammals. She concludes that brain size is inde-pendent of aquatic existence, as large brains developed incetaceans well after they became aquatic. Furthermore,other aquatic mammals (e.g., pinnipeds, sirenians) do notpossess markedly enlarged brains, complex gyrificationpatterns, or high encephalization levels compared withodontocete brains. Echolocation alone cannot account forall of these changes, as terrestrial echolocators (e.g., bats)are not highly encephalized. Rather, Marino postulatesthat the high encephalization level of odontocetes is morelikely related to their complex social structure.While brain size may not reflect aquaticism, other

nervous tissues do. The eye, which is technically anextension of the brain, exhibits several specializations inaquatic mammals. Mass and Supin (2007, this issue)review eye anatomy in four aquatic groups: cetaceans,

511ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS

pinnipeds, sirenians, and sea otters. They found anatom-ical differences that correspond to species-specificaquatic adaptations and behaviors. Aquatic mammalsuse different mechanisms to achieve aerial versus sub-merged emmetropia (refraction of light to focus on theretina). These corrections occur due to species-specificdifferences at the cornea or the lens. Pupil shapes corre-spond with variations in depth-dependent light expo-sure. Retina composition is similar to nocturnal terres-trial mammals, which is not surprising because aquaticmammals are exposed to low light conditions under-water. Cetaceans exhibit two areas of ganglion-cell con-centration (the best-vision areas) located in the temporaland nasal quadrants, while pinnipeds, sirenians, andsea otters have only one such area.Aquatic specializations are also apparent in the hear-

ing apparatus of aquatic mammals. The terrestrial eardepends upon sound waves in air being collected by thepinna, traveling though the auditory meatus, causingvibrating of a tympanic membrane. These vibrations arethen transmitted through an ossicular chain to the ovalwindow, where vibrations set the inner ear membranesand fluid into motion, causing bending of hair cells,which in turn, transmit an electrical signal that thebrain interprets as sound. Underwater hearing posestechnical challenges, as sound waves are propagated in afluid medium. Submerged terrestrial mammals primarilyhear through bone conduction. However, as terrestrialears are not acoustically isolated from the skull, theycannot distinguish directionality of sound under water.Nummela at al. (2007, this issue) describe the evolutionof underwater hearing in cetaceans, particularly thesound transmission mechanisms in six archaeocete fami-lies. They show that the pinna and external auditory me-atus were replaced by the mandible and its associated fatpad, which transmit sound pressures to the tympanicplate (lateral wall of the bulla). Other changes includemedial thickening of the tympanic bulla, functionalreplacement of the tympanic membrane by a bony plate,and changes in the orientation and shapes of the ossicles.In addition, the tympanoperiotic complex becomes acous-tically isolated from the skull by means of the develop-ment of air sinuses. This acoustic isolation prevents bonyconduction and, therefore, preserves stereo hearing bymeans of mandibular transmission.Hearing sensitivity is examined in a particularly rare

cetacean, the North Atlantic right whale. As traditionalbehavioral or physiological hearing tests are not feasiblewith right whales, a functional model was developedbased upon the ear anatomy. Parks et al. (2007, thisissue) examined right whale ears by means of histologicmeasurements of the basilar membrane and 2D and 3Dcomputerized tomography reconstructions of the cochlea.An estimated hearing range of 10 Hz–22 kHz based onestablished marine mammal models was obtained. Thisknowledge of the sound reception abilities of rightwhales is an important beginning to understanding theiracoustic communication system and possible impacts ofanthropogenic 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 thediscovery of a mysticete homolog of the vocal folds (thestructures responsible for sound production in terrestrialmammals). This is a particularly exciting finding, as the

sound source has remained undescribed for mysticetes.While vocal fold homologs have been identified in odonto-cetes (Reidenberg and Laitman, 1988), vocal folds werethought to be absent in baleen whales. Homology wasdetermined by criteria that define vocal folds in terres-trial mammals. The vocal fold homologue is described asa U-shaped fold that is (1) able to function as a valve toregulate gas flow, (2) supported by arytenoid cartilages,(3) controlled by muscles that either directly insert on itor move the arytenoid cartilages, (4) is connected acrossthe midline by a ligament, (5) receives motor and sensoryinnervation from the recurrent laryngeal nerve for thecontrolling musculature and mucosa caudal to the fold,and sensory innervation from the superior laryngealnerve for the mucosa rostral and ventral to the fold, and(6) is located adjacent to a diverticulum called the laryn-geal sac (likely derived from the laryngeal ventricles).Unlike the vocal folds of terrestrial mammals, which areperpendicular to airflow, the mysticete U-fold is orientedparallel to airflow. In this position, it can regulate airflowinto/out of the laryngeal sac, and vibration of its edgesmay generate sounds. The size and complexity of themysticete larynx indicates an organ with multiple func-tions in addition to sound generation, including protec-tion during breathing/swallowing, and airflow/gas pres-sure control in the respiratory spaces.

CONCLUSIONS

The articles in this special issue draw from several an-atomical disciplines to present both the latest discoveriesin aquatic mammal research as well as some thoughtfuland thorough evolutionary and systems-based reviews.It is hoped that, after reading this collection, one willhave a greater understanding of how much these ani-mals have changed through the effects of natural selec-tion from their terrestrial ancestors, through the variousfossil intermediate forms to the diversity of extantaquatic mammals we have today. Knowledge of their un-usual specializations will hopefully inspire us to copy na-ture in the development of new technologies. For exam-ple, continued investigations on flukes, flippers, axialmovements, feeding mechanics, skin, and body shapemay lead to development of more efficient hydrodynamicdesigns for water- and aircraft. Further study of howaquatic mammals regulate buoyancy, control bone den-sity, or manage dramatic changes in temperature andpressure as they rise and fall in the water column maylead to new treatments for osteoporosis or the inventionof protective gear for exposure to the extreme environ-mental changes of high and low altitude, space, or oceandepths. A more complete understanding of neural orga-nization, underwater vision, or sound generation andsound reception mechanisms may lead to the creation ofbetter artificial sensory systems. There is so much westill have to learn about aquatic mammals. This is anexciting time to be a marine mammal scientist.A brief note about conservation. Many of the aquatic

mammals discussed in this issue are critically endan-gered. Unfortunately, people only protect what theyknow. Publications such as this, however, enable us tofulfill our duty as scientists to help educate the publicwith scientific facts about these splendid animals. Afterreading about all the phenomenal adaptations of aquaticmammals presented here, I hope you will join me not

512 REIDENBERG

only in a new appreciation for how special these animalstruly are, but also in a renewed commitment to help pro-tect them from extinction.

ACKNOWLEDGMENTS

I thank the contributors to this issue for all their hardwork in producing outstanding pieces. I am in debt tothose reviewers who spent numerous hours reviewingand providing helpful critiques of the papers, therebyvastly improving the content of this special issue. A spe-cial thank you goes to the editor, Kurt Albertine, forencouraging and promoting publication of high quality,hypothesis-driven anatomical research. My deepest grat-itude goes to Jeff Laitman, Associate Editor, for hisinvaluable guidance, helpful advice, immeasurable sup-port, abounding encouragement, and enthusiastic faithin my ability to ‘‘pull off ’’ this endeavor. He continues tobe a never-failing lighthouse, mentoring my scientific ca-reer through the turbulent waters of academic life.

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