Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation

Foraging methods vary considerably among semiaquatic and fully aquatic mammals. Semiaquatic animals often find food in water yet consume it on land, but as truly obligate aquatic mammals, cetaceans (whales, dolphins, and porpoises) must acquire and ingest food underwater. It is hypothesized that differences in foraging methods are reflected in cetacean hyolingual apparatus anatomy. This study compares the musculoskeletal anatomy of the hyolingual apparatus in 91 cetacean specimens, including 8 mysticetes (baleen whales) in two species and 91 odontocetes (toothed whales) in 11 species. Results reveal specific adaptations for aquatic life. Intrinsic fibers are sparser and extrinsic musculature comprises a significantly greater proportion of the cetacean tongue relative to terrestrial mammals and other aquatic mammals such as pinnipeds and sirenians. Relative sizes and connections of cetacean tongue muscles to the hyoid apparatus relate to differences in feeding methods used by cetaceans, specifically filtering, suction, and raptorial prehension. In odontocetes and eschrichtiids (gray whales), increased tongue musculature and enlarged hyoids allow grasping and/or lingual depression to generate intraoral suction for prey ingestion. In balaenopterids (rorqual whales), loose and flaccid tongues enable great distention of the oral cavity for prey engulfing. In balaenids (right and bowhead whales), large but stiffer tongues direct intraoral water flow for continuous filtration feeding. Balaenid and eschrichtiid (and possibly balaenopterid) mysticete tongues possess vascular retial adaptations for thermoregulation and large amounts of submucosal adipose tissue for nutritional storage. All cetacean tongues also function in prey transport and swallowing. These hyolingual musculoskeletal differences are unique cetacean anatomical adaptations for foraging entirely in an aquatic environment. Anat Rec, 290:546–568, 2007. © 2007 Wiley‐Liss, Inc.

[1]  Jeffrey T Laitman,et al.  Discovery of a low frequency sound source in Mysticeti (baleen whales): Anatomical establishment of a vocal fold homolog , 2007, Anatomical record.

[2]  J. Laitman,et al.  Blowing bubbles: An aquatic adaptation that risks protection of the respiratory tract in humpback whales (Megaptera novaeangliae) , 2007, Anatomical record.

[3]  G. Pierce,et al.  Breaking symmetry: The marine environment, prey size, and the evolution of asymmetry in cetacean skulls , 2007, Anatomical record.

[4]  Alexander J Werth,et al.  Odontocete suction feeding: Experimental analysis of water flow and head shape , 2006, Journal of morphology.

[5]  A. Werth.  MANDIBULAR AND DENTAL VARIATION AND THE EVOLUTION OF SUCTION FEEDING IN ODONTOCETI , 2006 .

[6]  P. Arnold,et al.  Gulping behaviour in rorqual whales: underwater observations and functional interpretation , 2005 .

[7]  R. J. Hintz,et al.  FUNCTIONAL MORPHOLOGY OF THE MOUTH OF THE BOWHEAD WHALE AND ITS IMPLICATIONS FOR CONSERVATION , 2005 .

[8]  P. Tyack,et al.  Biosonar performance of foraging beaked whales (Mesoplodon densirostris) , 2005, Journal of Experimental Biology.

[9]  A. Werth.  Functional Morphology of the Sperm Whale (Physeter macrocephalus) Tongue, with Reference to Suction Feeding , 2004 .

[10]  A. Werth.  Models of hydrodynamic flow in the bowhead whale filter feeding apparatus , 2004, Journal of Experimental Biology.

[11]  A. Sokoloff.  Activity of tongue muscles during respiration: it takes a village? , 2004, Journal of applied physiology.

[12]  R. Fregosi,et al.  Coordination of intrinsic and extrinsic tongue muscles during spontaneous breathing in the rat. , 2004, Journal of applied physiology.

[13]  Lance Hosey.  Whales , 2002 .

[14]  A. Wang,et al.  Lingual Ultrastructure of the Long‐Finned Pilot Whale (Globicephala melas) , 2001, Anatomia, histologia, embryologia.

[15]  A. Sokoloff,et al.  Localization and contractile properties of intrinsic longitudinal motor units of the rat tongue. , 2000, Journal of neurophysiology.

[16]  A. Werth.  A KINEMATIC STUDY OF SUCTION FEEDING AND ASSOCIATED BEHAVIOR IN THE LONG‐FINNED PILOT WHALE, GLOBICEPHALA MELAS (TRAILL) , 2000 .

[17]  D. Fuller,et al.  Effect of co‐activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat , 1999, The Journal of physiology.

[18]  M. Heath.  Gray Whales in Cold Water , 1998, Science.

[19]  J. Heyning,et al.  Thermoregulation in the mouths of feeding gray whales. , 1997, Science.

[20]  J. Heyning,et al.  Suction feeding in beaked whales: morphological and observational evidence , 1996, Contributions in science.

[21]  J. Laitman,et al.  Anatomy of the hyoid apparatus in odontoceli (toothed whales): Specializations of their skeleton and musculature compared with those of terrestrial mammals , 1994, The Anatomical record.

[22]  J. Heyning,et al.  A palatal rete in the right whale? , 1993, Nature.

[23]  Marilyn K. Marx,et al.  Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis, and associated zooplankton characteristics , 1990 .

[24]  Anthony R. Martin.  Illustrated Encyclopedia of Whales and Dolphins , 1990 .

[25]  Lisa Schichtel Orton,et al.  Engulfing mechanics of fin whales , 1987 .

[26]  J. Laitman,et al.  Position of the larynx in odontoceti (toothed whales) , 1987, The Anatomical record.

[27]  C. Nelson,et al.  Whales and Walruses as Tillers of the Sea Floor , 1987 .

[28]  H. Oelschläger.  Tympanohyal bone in toothed whales and the formation of the tympano‐periotic complex (Mammalia: Cetacea) , 1986, Journal of morphology.

[29]  J. Oliver,et al.  Destruction and Opportunity on the Sea Floor: Effects of Gray Whale Feeding , 1985 .

[30]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[31]  K. R. Gordon.  Models of tongue movement in the walrus (Odobenus rosmarus) , 1984, Journal of morphology.

[32]  J. T. Staley,et al.  Baleen whales: preliminary evidence for forestomach microbial fermentation , 1984, Applied and environmental microbiology.

[33]  Kenneth S. Norris,et al.  Can Odontocetes Debilitate Prey with Sound? , 1983, The American Naturalist.

[34]  Richard H. Lambertsen,et al.  Internal Mechanism of Rorqual Feeding , 1983 .

[35]  D. E. Gaskin.  Ecology of Whales and Dolphins , 1982 .

[36]  August Pivorunas,et al.  The Feeding Mechanisms of Baleen Whales , 1979 .

[37]  William A. Watkins,et al.  Aerial Observation of Feeding Behavior in Four Baleen Whales: Eubalaena glacialis, Balaenoptera borealis, Megaptera novaeangliae, and Balaenoptera physalus , 1979 .

[38]  A. Pivorunas,et al.  The fibrocartilage skeleton and related structures of the ventral pouch of Balaenopterid whales , 1977, Journal of morphology.

[39]  H. Fong.  Animal Physiology: Adaptation and Environment , 1975, The Yale Journal of Biology and Medicine.

[40]  P. Sund.  Evidence of feeding during migration and of an early birth of the California gray whale (eschrichtius robustus). , 1975, Journal of mammalogy.

[41]  K. Backhouse,et al.  The sperm whale , 1974 .

[42]  B. Parkins,et al.  Functional anatomy of the porpoise larynx. , 1973, The American journal of anatomy.

[43]  S. Ridgway,et al.  Mammals of the sea : biology and medicine , 1973 .

[44]  C. M. Scammon.  The Marine Mammals of the North-Western Coast of North America: Described and Illustrated, Together With an Account of the American Whale-Fishery , 1968 .

[45]  P. Best,et al.  Functional Polyovuly in the Sei Whale Balaenoptera borealis Lesson , 1963, Nature.

[46]  C. Hubbs.  First Records of Two Beaked Whales, Mesoplodon bowdoini and Ziphius cavirostris, from the Pacific Coast of the United States , 1946 .

[47]  H. C. Raven.  SECTION OF BIOLOGY: Some Morphological Adaptations of Cetaceans (Whales and Porpoises) for Life in the Water , 1942 .

[48]  H. L. Kesteven.  Some features in the anatomy and later development of the head of Delphinus delphinus Linné , 1941 .

[49]  S Abd-El-Malek,et al.  A contribution to the study of the movements of the tongue in animals, with special reference to the cat. , 1938, Journal of anatomy.

[50]  A. Howell.  Myology of the narwhal (Monodon monoceros) , 1930 .

[51]  F. Sonntag.  The Comparative Anatomy of the Tongues of the Mammalia.—VII. Cetaeea, Sirenia, and Ungulata. , 1922 .

[52]  W. H. Flower.  An Introduction to the Osteology of the Mammalia , 1870, Nature.

[53]  Peter G. H. Evans,et al.  Marine Mammals , 2001, Springer US.

[54]  T. Halliday.  The senses and communication , 1998 .

[55]  S. L. Sanderson.  Convergent and Alternative Designs for Vertebrate Suspension Feeding , 1993 .

[56]  W. Kier,et al.  Trunks, Tongues, and Tentacles: Moving with Skeletons of Muscle , 1989 .

[57]  G. Behrmann.  The peripheral nerve ends in the tongue of the harbour porpoise Phocoena phocoena (Linne, 1758) , 1988 .

[58]  D. Murie,et al.  19 – Foraging of the Gray Whale along the West Coast of Vancouver Island, British Columbia , 1984 .

[59]  M. Nerini,et al.  18 – A Review of Gray Whale Feeding Ecology , 1984 .

[60]  S. Ridgway,et al.  Functional and Descriptive Anatomy of the Bottlenosed Dolphin Nasolaryngeal System with Special Reference to the Musculature Associated with Sound Production , 1980 .

[61]  A. Cave.  The rhinoceros lingual intrinsic musculature , 1980 .

[62]  Howard E. Evans,et al.  Miller's anatomy of the dog , 1979 .

[63]  E. J. Slijper.  Die cetaceen, vergleichend-anatomisch und systematisch , 1973 .

[64]  H. Mills,et al.  Morphology and ecology of marine mammals;: Seals, dolphins, porpoises , 1973 .

[65]  J. K. Summitt.  SENSES AND COMMUNICATION: DISCUSSION , 1971 .

[66]  François Moris.  ETUDE ANATOMIQUE DE LA RÉGION CÉPHALIQUE DU MARSOUIN, PHOCAENA PHOCAENA L. (CÉTACÉ ODONTOCÈTE) , 1969 .

[67]  S. E. Kleĭnenberg.  Beluga (Delphinapterus leucas) : investigation of the species , 1969 .

[68]  F. S. Essapian.  Some observations on body flexibility of bottle-nosed dolphins, Tursiops truncatus in captivity , 1965 .

[69]  根本 敬久.  Food of baleen whales with reference to whale movements , 1963 .

[70]  F. Fraser,et al.  Handbook of R.H. Burne's Cetacean dissections / , 1952 .

[71]  A. Howell.  Contribution to the anatomy of the Chinese finless porpoise, Neomeris phocaenoides , 1927 .

[72]  M. D. Smith,et al.  The external characters, skeletal muscles and peripheral nerves of Kogia breviceps (Blainville). Bulletin of the AMNH ; v. 38, article 2. , 1918 .

[73]  J. D. Kernan,et al.  Memoranda upon the anatomy of the respiratory tract, foregut, and thoracic viscera of a foetal Kogia breviceps. Bulletin of the AMNH ; v. 38, article 8. , 1918 .

[74]  W. Kükenthal.  Vergleichend-anatomische und entwickelungsgeschichtliche Untersuchungen an Walthieren , 1889 .

[75]  M. Watson,et al.  XI.—The Anatomy of the Northern Beluga (Beluga catodon, Gray; Delphinapterus leucas, Pallas) compared with that of other Whales , 1880, Transactions of the Royal Society of Edinburgh.

[76]  W. Dall,et al.  The marine mammals of the north-western coast of North America described and illustrated , 1874 .