Oropharyngeal cavity floor morphology in Eretmochelys imbricata (Testudines: Cheloniidae) hatchlings and evolutionary implications

Morphological studies of the oropharyngeal cavity of chelonians have become an interesting tool in the understanding of evolutionary processes associated with feeding habits in aquatic animals and the transition from aquatic to terrestrial forms. In this context, the aim of the present study was to describe the oropharyngeal cavity floor morphology of hawksbill sea turtle (Eretmochelys imbricata) hatchlings. Ten dead hatchlings of undefined sex were obtained from nests hatched on the coast of the state of Rio Grande do Norte, Brazil. The heads of each specimen were fixed, dissected, and analyzed at the macroscopic and microscopic levels. The oropharyngeal cavity floor of the hawksbill sea turtle hatchlings is formed by the tongue, pharynx, floor muscles, and hyolingual skeleton, delimited in the rostral and lateral directions by a keratinized beak, called the rhamphotheca, and in the caudal region at the limit between the pharynx and the esophagus. The tongue muscles and the muscles that support the floor of the oral cavity comprise the following: m. hypoglossohyoideus, m. hypoglossoglossus, m. hyoglossus, m. genioglossus, m. constrictor laryngis, m. geniohyoideus pars lateralis, and m. intermandibularis. The oropharyngeal cavity floor mucosa is formed by keratinized stratified squamous epithelium and the lamina propria is formed by loose connective tissue. The floor mucosa is devoid of taste buds. We believe that the basic oropharyngeal cavity floor characteristics in hawksbill sea turtle hatchlings may comprise indications that these animals are plesiomorphic and that semiaquatic and terrestrial turtles may have undergone adaptations to feed out of water.

[1]  O. Horak,et al.  Differences in the anatomy of the lower respiratory tract in selected species of the order Testudines , 2021, Veterinární Medicína.

[2]  H. Jackowiak,et al.  Functional morphology of the tongue in the domestic turkey (Meleagris gallopavo gallopavo var. domesticus) , 2021, Poultry science.

[3]  Meg Barboza,et al.  Gross and Microscopic Anatomy of the Nasal Cavity, Including Olfactory Epithelium, of the Florida Manatee (Trichechus manatus latirostris) , 2020 .

[4]  M. Abumandour,et al.  Structural and Functional Characterization of the Tongue and Digestive Tract of Psammophis sibilans (Squamata, Lamprophiidae): Adaptive Strategies for Foraging and Feeding Behaviors , 2020, Microscopy and Microanalysis.

[5]  I. Watanabe,et al.  Structural and ultrastructural characteristics of the tongue of the Collared Peccary (Pecari tajacu, Linnaeus, 1758) , 2020, Anatomia, histologia, embryologia.

[6]  I. Watanabe,et al.  Morphological and ultrastructural characteristics of the tongue of wild boar , 2020, European journal of histochemistry : EJH.

[7]  R. Sousa-lima,et al.  First Record of Bioacoustic Emission in Embryos and Hatchlings of Hawksbill Sea Turtles (Eretmochelys imbricata) , 2019, Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal.

[8]  M. Abumandour,et al.  Morphological features of the tongue and laryngeal entrance in two predatory birds with similar feeding preferences: common kestrel (Falco tinnunculus) and Hume’s tawny owl (Strix butleri) , 2017, Anatomical Science International.

[9]  M. A. Miglino,et al.  Avaliação da cavidade orofaríngea da tartaruga da Amazônia, Podocnemis expansa (Schweigger, 1812) , 2015 .

[10]  P. Čížek,et al.  Light and scanning electron microscopy of the tongue of the sand lizard (Lacerta agilis). , 2015, Folia morphologica.

[11]  R. Ríosmena-Rodríguez,et al.  Habitat Use and Diet of Juvenile Eastern Pacific Hawksbill Turtles (Eretmochelys imbricata) in the North Pacific Coast of Costa Rica , 2013 .

[12]  I. Watanabe,et al.  Structural and ultrastructural features of the agouti tongue (Dasyprocta aguti Linnaeus, 1766) , 2013, Journal of anatomy.

[13]  A. Weissenbacher,et al.  The Oropharyngeal Morphology in the Semiaquatic Giant Asian Pond Turtle, Heosemys grandis, and Its Evolutionary Implications , 2012, PloS one.

[14]  C. T. Stayton.  Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae , 2011, Journal of Experimental Biology.

[15]  P. Lemell,et al.  Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue , 2011, Journal of morphology.

[16]  W. Meyer,et al.  Functional Morphology of the Tongue in the Domestic Goose (Anser Anser f. Domestica) , 2011, Anatomical record.

[17]  J. Davenport,et al.  Opening and closing mechanisms of the leatherback sea turtle larynx: a crucial role for the tongue , 2010, Journal of Experimental Biology.

[18]  Juliana Normando Pinheiro,et al.  Macroscopia do aparelho digestório do cágado sul-americano Mesoclemmys vanderhaegei (Bour, 1973) , 2010 .

[19]  P. Lemell,et al.  Aquatic feeding in a terrestrial turtle: a functional-morphological study of the feeding apparatus in the Indochinese box turtle Cuora galbinifrons (Testudines, Geoemydidae) , 2010, Zoomorphology.

[20]  H. Plenk,et al.  Microanatomy of the Palatal Mucosa of the Semiaquatic Malayan Box Turtle, Cuora amboinensis, and Functional Implications , 2008, Anatomical record.

[21]  Brazil,et al.  Comparative Scanning Electron Microscopic Study of the Lingual Papillae in Three Species of Bats (Carollia perspicillata, Glossophaga soricina and Desmodus rotundus) , 2007, Microscopy and Microanalysis.

[22]  W. Joyce.  Phylogenetic Relationships of Mesozoic Turtles , 2007 .

[23]  D. Schraufnagel,et al.  Scanning Electron Microscopic Structure of the Lingual Papillae of the Common Opossum (Didelphis marsupialis) , 2005, Microscopy and Microanalysis.

[24]  Roberto Sacchi,et al.  Larynx morphology and sound production in three species of Testudinidae , 2004, Journal of morphology.

[25]  S. Iwasaki.  Evolution of the structure and function of the vertebrate tongue , 2002, Journal of anatomy.

[26]  P. Aerts,et al.  Intrinsic Mechanics and Control of Fast Cranio-Cervical Movements in Aquatic Feeding Turtles1 , 2001 .

[27]  K. Zuwala,et al.  Morphological differentiation of taste organs in the ontogeny of Salamandra salamandra , 2001, Anatomy and Embryology.

[28]  P. Lemell,et al.  Light and transmission electron microscopy of the dorsal lingual epithelium of Pelusios castaneus (Pleurodira, Chelidae) with special respect to its feeding mechanics. , 2001, Tissue & cell.

[29]  E. Brainerd,et al.  Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. , 1998, The Journal of experimental zoology.

[30]  H. Hilgers,et al.  Fine structure of the dorsal lingual epithelium of Trachemys scripta elegans (Chelonia: Emydidae) , 1998, The Anatomical record.

[31]  S. Iwasaki,et al.  Fine structure of the dorsal lingual epithelium of the juvenile hawksbill turtle, Eretmochelys imbricata bissa , 1996, The Anatomical record.

[32]  S. Iwasaki,et al.  An ultrastructural study of the dorsal lingual epithelium of the rat snake, Elaphe quadrivirgata. , 1994, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[33]  J. Avise,et al.  A molecular phylogeny for marine turtles: trait mapping, rate assessment, and conservation relevance. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Iwasaki,et al.  Fine structure of the dorsal epithelium of the tongue of the Japanese terrapin, Clemmys japonica (Cheloia, Emydinae). , 1992, Archives of histology and cytology.

[35]  S. Iwasaki,et al.  Fine structure of the dorsal lingual epithelium of the Japanese lizard, Takydromus tachydromoides. , 1992, Kaibogaku zasshi. Journal of anatomy.

[36]  S. Iwasaki.  Fine structure of the dorsal lingual epithelium of the little tern, Sterna albifrons pallas (Aves, Lari) , 1992, Journal of morphology.

[37]  G. Lauder,et al.  KINEMATICS OF AQUATIC PREY CAPTURE IN THE SNAPPING TURTLE CHELYDRA SERPENTINA , 1992 .

[38]  S. Iwasaki.  Fine structure of the dorsal epithelium of the tongue of the freshwater turtle, Geoclemys reevesii (Chelonia, Emydinae) , 1992 .

[39]  S. Iwasaki,et al.  Fine structure of the dorsal epithelium of the mongoose tongue. , 1990, Journal of anatomy.

[40]  R. M. Winokur,et al.  The buccopharyngeal mucosa of the turtles (Testudines) , 1988, Journal of morphology.

[41]  K. Schwenk.  Occurrence, Distribution and Functional Significance of Taste Buds in Lizards , 1985 .

[42]  M. Dierich,et al.  HISTOCHEMICAL STUDIES , 1967, Beitrage zur Neurochirurgie.

[43]  P. Lemell,et al.  Feeding in Turtles: Understanding Terrestrial and Aquatic Feeding in a Diverse but Monophyletic Group , 2019, Feeding in Vertebrates.

[44]  J. Mortimer,et al.  Diet Composition of Hawksbill Turtles (Eretmochelys imbricata) in the Republic of Seychelles , 2014 .

[45]  N. Natchev,et al.  Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae) , 2011 .

[46]  I. Werneburg.  Evolution and development of turtles : organogenesis and cranial musculature , 2010 .

[47]  P. Soille.  Opening and Closing , 2004 .

[48]  S. Iwasaki,et al.  Histochemical and ultrastructural features of the lingual epithelium of the rat snake (Elaphe climacophora). , 2003, Zoology.

[49]  O. Behmer,et al.  Manual de técnicas para histologia: normal e patológica , 2003 .

[50]  E. Brainerd,et al.  Buccal oscillation and lung ventilation in a semi-aquatic turtle, Platysternon megacephalum. , 2001, Zoology.

[51]  Kurt Schwenk,et al.  Feeding : form, function, and evolution in tetrapod vertebrates , 2000 .

[52]  K. Eckert,et al.  Research and Management Techniques for the Conservation of Sea Turtles , 1999 .

[53]  H. Hilgers,et al.  FEEDING MECHANISM OF TESTUDO HERMANNI BOETTGERI (CHELONIA, CRYPTODIRA) , 1999 .

[54]  P. Lemell,et al.  Feeding Patterns of Pelusios Castaneus (Chelonia: Pleurodira) , 1996 .

[55]  S. Iwasaki.  Fine structure of the dorsal lingual epithelium of the lizard, Gekko japonicus (Lacertilia, Gekkonidae). , 1990, The American journal of anatomy.

[56]  S. Yagishita,et al.  An Ultrastructural Study , 1979 .

[57]  A. Jasiński.  Light and scanning microscopy of the tongue and its gustatory organs in the common toad, Bufo bufo (L.). , 1979, Zeitschrift fur mikroskopisch-anatomische Forschung.

[58]  Nalavade Mn,et al.  Histochemical studies on the mucins of the vertebrate tongues. VIII. Histochemical analysis of mucosubstances in the tongue of the turtle. , 1976 .