THE ANATOMICAL RECORD 290:507–513 (2007) Anatomical Adaptations of Aquatic Mammals JOY S. REIDENBERG* Center for Anatomy and Functional Morphology, Department of Medical Education, Mount Sinai School of Medicine, New York, New York ABSTRACT This special issue of the Anatomical Record explores many of the an- atomical 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, 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), 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 produc- tion, sound reception, feeding, locomotion, buoyancy control, thermoregu- lation, 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, hy- pothesis-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. Ó 2007 Wiley-Liss, Inc. Anat Rec, 290:507–513, 2007. Ó 2007 Wiley-Liss, Inc. Key words: aquatic; adaptation; anatomy; marine mammal; sirenian; cetacean; pinniped; evolution Aquatic life poses many challenges for mammals that 1975; Ridgway and Howard, 1979). A jointed, collapsible were originally adapted for life on land. As the evolution- rib cage allows compression of the thorax to accommo- ary process of natural selection can only apply to modify- date the shrinking lungs. Skeletal muscles are adapted ing present structures, aquatic mammals bring a lot of to maintain low levels of aerobic metabolism under the terrestrial baggage to their aquatic existence. For one hypoxic conditions associated with diving (Kanatous thing, they do not breathe water as fish do. Therefore, re- spiratory tract modifications are necessary to protect a system designed to function in air while excluding the *Correspondence to: Joy S. Reidenberg, Center for Anatomy ever-present surrounding water. Many of these adapta- and Functional Morphology, Department of Medical Education, tions have been previously described, for example, valvu- Mail Box 1007, Mount Sinai School of Medicine, 1 Gustave L. lar nostrils that exclude water, and an intranarial larynx Levy Place, New York, NY 10029-6574. (Reidenberg and Laitman, 1987) that further protects E-mail: [email protected] the respiratory tract from water inundation during swal- Received 13 March 2007; Accepted 13 March 2007 lowing. Diving presents additional challenges, as ambi- DOI 10.1002/ar.20541 ent pressure rises with increased depth. Lung volumes Published online in Wiley InterScience (www.interscience.wiley. collapse under the high pressures of a deep dive (Boyd, com). Ó 2007 WILEY-LISS, INC. 508 REIDENBERG et al., 2002). Elevated levels of myoglobin in skeletal baleen, tongue, pharyngeal spaces, stomach), the exter- muscles also increase oxygen retention, thus enabling nal form (integument and body shape, including flukes longer dive times between breaths (Noren et al., 2001; and flippers), musculoskeletal systems (cranial, mandib- Wright and Davis, 2006). The mass of blood vessels ular, and cervical regions; postcranial axial and appen- located in the dorsum of the thorax (retia thoracica) have dicular skeleton), nervous system (eye, ear, brain), and been proposed to function during diving to accommodate respiratory tract (larynx). Emphasis is placed on explor- for the collapsed lung volume, thereby preventing gross ing anatomical function in the context of aquatic life. A displacement of abdominal organs (Hui, 1975). Salinity range of techniques are used, including dissection, histol- presents another challenge, as marine mammals must ogy, electron microscopy, computerized tomography and main water and salt balance, despite the frequent influx 3D reconstructions, and experimental field work. The of salt water they consume while swallowing prey. The papers that follow in this issue are a blend of both review kidney structure of cetaceans (whales, including dolphins articles and new, hypothesis-driven anatomical research. and porpoises) and pinnipeds (seals, sea lions, walruses) These studies highlight the dramatic anatomical changes is unusual, having a reniculate structure (Abdelbaki seen in the evolution from fossil ancestors to extant et al., 1984; Henk et al., 1986) not found in any other ter- aquatic mammals. This special issue is a tribute to the restrial mammals except bears, but does not appear to unique anatomical forms and functions of aquatic mam- have a greater ability to concentrate urine (Ortiz, 2001). mals that enables their adaptation to life underwater. Rather, the apparent advantage of numerous independ- ent renicules in marine mammals is limited tubule lengths in the necessarily large kidneys of gigantic mam- UNDERWATER FORAGING mals (Maluf and Gassman, 1998). The first question that naturally comes to mind is Navigation and prey detection systems are also modi- ‘‘Why did some mammals become aquatic in the first fied. As many aquatic mammals need to hunt at night place?’’ Uhen (2007, this issue) discusses the evolution of or in turbid or deep water, their sensory systems have aquatic mammals, using both molecular and morphologi- accordingly evolved. Pinnipeds developed longer and cal data for Cetacea, Sirenia, Desmostylia, and Pinnipe- more sensitive vibrissae that can pick up hydrodynamic dia. He notes that re-entering the water occurred on at trails (vibrations in water) of fish swimming, or relay in- least seven different occasions. Specific changes occurred formation about water current flow and variations in in the axial and appendicular skeleton that improved substrate surfaces (Dehnhardt et al., 2001). Odontocetes locomotion for aquatic foraging. Nostril, eye placement, (toothed whales) developed nasal structures that gener- rostrum, and dental morphology also changed, depend- ate echolocation, enabling them to use sound to locate ing upon the need to forage while wading versus sub- prey or navigate past obstacles (Cranford et al., 1996; mersion. Although the end product of each of these evo- Au et al., 2006). lutionary trajectories is vastly different, they all appear Many marine mammals have modified their external to be the result of natural selection for improved aquatic shape, developing new propulsion mechanisms for loco- foraging. Terrestrial mammals from seven separate line- motion in water. Seals use alternating horizontal sweeps ages thus re-invaded the water to fill a vacant niche: of their hind flippers (Fish et al., 1988). Fur seals and feeding in water. sea lions ‘‘fly’’ underwater by beating their fore flippers The foraging mechanisms of fossil ancestors, however, (English, 1977; Feldkamp, 1987). Walruses sometimes do not always match present day species. Domning and use their tusks to grip the sea floor or ice and push their Beatty (2007, this issue) compare fossil and modern body forward with a downward nod of the head. Sire- dugongs in their tusk shape and cranial anatomy, and nians (manatees and dugongs) have lost their hind explore whether these specializations indicate tusk use limbs, but can either propel themselves with their tail in feeding. Fossil dugongines exhibit cranial modifica- fluke(s) or walk along the sea or river floor with their tions that may have assisted downward and backward forelimbs. Cetaceans have excelled in the attainment of tusk cutting motions. The larger, more blade-like tusks streamlined form, and are thus the fastest swimmers. of fossil dugongines are more effective at harvesting rhi- As with sirenians, cetaceans have lost appendages that zomes. However, examination of microwear patterns in detract from axial locomotion (hind limbs). Similarly to modern dugong tusks do not support that their use is pinnipeds, they have modified extremities that assist necessary in feeding, although it does occasionally occur with lift and braking (flippers). Cetaceans have also in large adult males. Tusk use in modern dugongs has added new extensions that aid propulsion (flukes) or pre- thus changed radically from the ancestral pattern. As vent roll or yaw (dorsal fin) while swimming with exag- tusks are not essential for feeding in extant dugongs, the gerated pitch (dorsoventral bending). persistence of erupted tusks in males indicates a possible Although most of the above-mentioned adaptations role in sexual selection or other social interactions. have been discussed at length in previous publications, Feeding mechanisms are also examined in cetaceans in the articles in this special issue present some new find- this issue. MacLeod et al. (2007, this issue) describe the ings regarding aquatic adaptations. This special issue relationship between prey size and skull asymmetry.