The Head and Neck Anatomy of Sea Turtles (Cryptodira: Chelonioidea) and Skull Shape in Testudines

Background Sea turtles (Chelonoidea) are a charismatic group of marine reptiles that occupy a range of important ecological roles. However, the diversity and evolution of their feeding anatomy remain incompletely known. Methodology/Principal Findings Using computed tomography and classical comparative anatomy we describe the cranial anatomy in two sea turtles, the loggerhead (Caretta caretta) and Kemp’s ridley (Lepidochelys kempii), for a better understanding of sea turtle functional anatomy and morphological variation. In both taxa the temporal region of the skull is enclosed by bone and the jaw joint structure and muscle arrangement indicate that palinal jaw movement is possible. The tongue is relatively small, and the hyoid apparatus is not as conspicuous as in some freshwater aquatic turtles. We find several similarities between the muscles of C. caretta and L. kempii, but comparison with other turtles suggests only one of these characters may be derived: connection of the m. adductor mandibulae internus into the Pars intramandibularis via the Zwischensehne. The large fleshy origin of the m. adductor mandibulae externus Pars superficialis from the jugal seems to be a characteristic feature of sea turtles. Conclusions/Significance In C. caretta and L. kempii the ability to suction feed does not seem to be as well developed as that found in some freshwater aquatic turtles. Instead both have skulls suited to forceful biting. This is consistent with the observation that both taxa tend to feed on relatively slow moving but sometimes armoured prey. The broad fleshy origin of the m. adductor mandibulae externus Pars superficialis may be linked to thecheek region being almost fully enclosed in bone but the relationship is complex.

[1]  G. Hays,et al.  THE IMPLICATIONS OF LUNG-REGULATED BUOYANCY CONTROL FOR DIVE DEPTH AND DURATION , 2004 .

[2]  C. K. Dodd,et al.  Synopsis of the Biological Data on the Loggerhead Sea Turtle Caretta Caretta (Linnaeus 1758). , 1989 .

[3]  J. F. Parham,et al.  DEVELOPING A PROTOCOL FOR THE CONVERSION OF RANK-BASED TAXON NAMES TO PHYLOGENETICALLY DEFINED CLADE NAMES, AS EXEMPLIFIED BY TURTLES , 2004 .

[4]  A. Bolten,et al.  Loggerhead sea turtles , 2003 .

[5]  Peter L. Lutz,et al.  The Biology of Sea Turtles , 1998 .

[6]  V. Chernick,et al.  Remodeling , 2006 .

[7]  G. ELLIOT SMITH,et al.  Studies on the Structure and Development of Vertebrates , 1930, Nature.

[8]  E. C. Olson,et al.  The family Diadectidae and its bearing on the classification of reptiles , 1947 .

[9]  Jauns F. Pnnnlur,et al.  The Phylogeny of Cheloniid Sea Turtles Revisited , 2009 .

[10]  P. M. Sander,et al.  Shell bone histology indicates terrestrial palaeoecology of basal turtles , 2007, Proceedings of the Royal Society B: Biological Sciences.

[11]  John,et al.  In Search of the Tree of Life for Turtles , 2008 .

[12]  E. S. Gaffney,et al.  The skeletal morphology of the Cretaceous cryptodiran turtle, Adocus, and the relationships of the Trionychoidea. American Museum novitates ; ; no. 2941. , 1989 .

[13]  Ulrich Witzel,et al.  Finite-element model construction for the virtual synthesis of the skulls in vertebrates: case study of Diplodocus. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[14]  W. Joyce,et al.  The cranial anatomy of the Early Jurassic turtle Kayentachelys aprix , 2007 .

[15]  Jonathan D. R. Houghton,et al.  Endangered species: Pan-Atlantic leatherback turtle movements , 2004, Nature.

[16]  Sir,et al.  The Development of the Vertebrate Skull , 1938, Nature.

[17]  J. Davenport,et al.  A comparison of the swimming of marine and freshwater turtles , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  G. Baur On the morphology of the vertebrate‐skull , 1889 .

[19]  Johannes Müller Early loss and multiple return of the lower temporal arcade in diapsid reptiles , 2003, Naturwissenschaften.

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

[21]  R. Hill,et al.  Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. , 2005, Systematic biology.

[22]  A. Carr,et al.  Handbook of Turtles , 1952 .

[23]  N. Arai,et al.  Differences in the Skull Morphology between Juvenile and Adult Green Turtles: Implications for the Ontogenetic Diet Shift , 2010 .

[24]  J. Thomason,et al.  Functional Morphology in Vertebrate Paleontology , 1998 .

[25]  A. Meyer,et al.  The evolutionary position of turtles revised , 2001, Naturwissenschaften.

[26]  R. C. Fox,et al.  Osteology and relationships of Captorhinus aguti (Cope) (Reptilia: Captorhinomorpha) , 1966 .

[27]  I. Werneburg Jaw musculature during the dawn of turtle evolution , 2013, Organisms Diversity & Evolution.

[28]  T. Frazzetta Adaptive problems and possibilities in the temporal fenestration of tetrapod skulls , 1968, Journal of morphology.

[29]  S. Renous,et al.  Evolution of Locomotion in Aquatic Turtles , 2007 .

[30]  P. O’Higgins,et al.  Hard tissue anatomy of the cranial joints in Sphenodon (Rhynchocephalia): sutures, kinesis, and skull mechanics , 2011 .

[31]  C. Holliday,et al.  Ontogeny of the Alligator Cartilago Transiliens and Its Significance for Sauropsid Jaw Muscle Evolution , 2011, PloS one.

[32]  J. Wyneken The anatomy of sea turtles , 2001 .

[33]  S. Løvtrup On the Classification of the Taxon Tetrapoda , 1985 .

[34]  Michel Laurin,et al.  A reevaluation of early amniote phylogeny , 1995 .

[35]  C. Limpus,et al.  Evidence for transoceanic migrations by loggerhead sea turtles in the southern Pacific Ocean , 2009, Proceedings of the Royal Society B: Biological Sciences.

[36]  P. Pritchard,et al.  Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment. , 2004, Systematic biology.

[37]  J. Raga,et al.  Feeding ecology of the loggerhead turtle Caretta caretta in the western Mediterranean , 2006 .

[38]  K. Bjorndal,et al.  Selective feeding in the hawksbill turtle, an important predator in coral reef ecosystems , 2002 .

[39]  I. Werneburg,et al.  Timing of organogenesis support basal position of turtles in the amniote tree of life , 2009, BMC Evolutionary Biology.

[40]  K. Bjorndal,et al.  Roles of Sea Turtles in Marine Ecosystems: Reconstructing the Past , 2002 .

[41]  Michael S. Y. Lee Pareiasaur phylogeny and the origin of turtles , 1997 .

[42]  George V. Lauder,et al.  Chapter 12. Aquatic Feeding in Lower Vertebrates , 1985 .

[43]  O. Rieppel,et al.  THE ORIGIN AND EARLY EVOLUTION OF TURTLES , 1999 .

[44]  I. Werneburg The cranial musculature of turtles , 2011 .

[45]  A. A. Bellairs,et al.  The chondrocranium and the development of the skull in recent reptiles , 1981 .

[46]  P. Dutton,et al.  Marine turtle mitogenome phylogenetics and evolution. , 2012, Molecular phylogenetics and evolution.

[47]  U. Fritz,et al.  Checklist of Chelonians of the World , 2007, Vertebrate Zoology.

[48]  H. Shaffer,et al.  Tests of turtle phylogeny: molecular, morphological, and paleontological approaches. , 1997, Systematic biology.

[49]  E. S. Gaffney The side-necked turtle family Chelidae : a theory of relationships using shared derived characters. American Museum novitates ; no. 2620 , 1977 .

[50]  O. Rieppel,et al.  Reptile phylogeny and the interrelationships of turtles , 1997 .

[51]  P. O’Higgins,et al.  Functional Relationship between Skull Form and Feeding Mechanics in Sphenodon, and Implications for Diapsid Skull Development , 2011, PloS one.

[52]  O. Rieppel The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina , 1990 .

[53]  E. S. Gaffney,et al.  The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the AMNH ; no. 194 , 1990 .

[54]  C. Gans,et al.  Biology of the Reptilia. Volume 3: Morphology C , 1970 .

[55]  E. S. Gaffney,et al.  Evolution of the Side-Necked Turtles: The Family Podocnemididae , 2011 .

[56]  R. Zangerl Two toxochelyid sea turtles from the Landenian sands of Erquelinnes (Hainaut), of Belgium , 1971 .

[57]  W. K. Gregory Pareiasaurs versus placodonts as near ancestors to the turtles. Bulletin of the AMNH ; v. 86, article 6 , 1946 .

[58]  O. Rieppel,et al.  An ancestral turtle from the Late Triassic of southwestern China , 2008, Nature.

[59]  Tage Lakjer,et al.  Studien über die Trigeminus-versorgte Kaumuskulatur der Sauropsiden , 1926 .

[60]  C. Shoop,et al.  Increasing turtle strandings in the southeast United States: A complicating factor , 1982 .

[61]  The Skeletal Morphology of the Cretaceous Cryptodiran Turtle , Adocus , and the Relationships of the Trionychoidea PETER A . MEYLAN , 2022 .

[62]  P. Johnston Cranial muscles of the anurans leiopelma hochstetteri and ascaphus truei and the homologies of the mandibular adductors in lissamphibia and other gnathostomes , 2011, Journal of morphology.

[63]  S. Williston THE TEMPORAL ARCHES OF THE REPTILIA , 1904 .

[64]  P. Pritchard Piscivory in turtles, and evolution of the long-necked Chelidae , 1984 .

[65]  P. Aerts,et al.  Cervical Anatomy and Function in Turtles , 2007 .

[66]  R. Hirayama Oldest known sea turtle , 1998, Nature.

[67]  M. Edgar,et al.  Clinical Oral Science , 1998 .

[68]  Steve A. Johnson,et al.  Effects of Organized Turtle Watches on Loggerhead (Caretta caretta) Nesting Behavior and Hatchling Production in Florida , 1996 .

[69]  G. Amato,et al.  Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. , 2008, Molecular phylogenetics and evolution.

[70]  N. Hunt Muscle function and the control of facial form , 1998 .

[71]  A. Kluge,et al.  Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology. , 1993, Molecular biology and evolution.

[72]  J. Wyneken The External Morphology, Musculoskeletal System, and Neuro‚ÄìAnatomy of Sea Turtles , 2002 .

[73]  G. Bever,et al.  An Archosaur-Like Laterosphenoid in Early Turtles (Reptilia: Pantestudines) , 2009 .

[74]  F. D. Broin The oldest pre-Podocnemidid turtle (Chelonii, Pleurodira), from the early Cretaceous, Ceará state, Brasil, and its environment , 2000 .

[75]  K. Bjorndal,et al.  SEA TURTLES AS BIOLOGICAL TRANSPORTERS OF NUTRIENTS AND ENERGY FROM MARINE TO TERRESTRIAL ECOSYSTEMS , 2000 .

[76]  S. Morreale,et al.  Diet of juvenile Kemp's ridley and loggerhead sea turtles from Long Islands, New York , 1993 .

[77]  H. Preuschoft,et al.  Biomechanical investigations on the skulls of reptiles and mammals , 2002 .

[78]  W. K. Gregory,et al.  The Temporal Fossae of Vertebrates in Relation to the Jaw Muscles , 1915 .

[79]  W. Joyce,et al.  Transitional fossils and the origin of turtles , 2010, Biology Letters.

[80]  J. Sterli,et al.  Anatomy of Condorchelys antiqua Sterli, 2008, and the Origin of the Modern Jaw Closure Mechanism in Turtles , 2010 .

[81]  C. McHenry,et al.  Biomechanics of the rostrum in crocodilians: a comparative analysis using finite-element modeling. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[82]  E. C. Case A Possible Explanation of Fenestration in the Primitive Reptilian Skull, with Notes on Temporal Region of the Genus Dimetrodon , 1924 .

[83]  J. GRAHAM KERR,et al.  The Osteology of the Reptiles , 1926, Nature.

[84]  D. Henderson THE EYES HAVE IT: THE SIZES, SHAPES, AND ORIENTATIONS OF THEROPOD ORBITS AS INDICATORS OF SKULL STRENGTH AND BITE FORCE , 2003 .

[85]  E. Goodrich On the Classification of the Reptilia , 1916 .

[86]  O. P. Hay The fossil turtles of North America , 2010 .

[87]  Andreas T. Matzke Osteology of the skull of Toxochelys(Testudines, Chelonioidea) , 2009 .

[88]  Michael S. Y. Lee Molecules, morphology, and the monophyly of diapsid reptiles , 2001 .

[89]  D. Bramble,et al.  Chapter 13. Feeding Mechanisms of Lower Tetrapods , 1985 .

[90]  Herbert R. Barghusen The adductor jaw musculature of Dimetrodon (Reptilia, Pelycosauria) , 1973 .

[91]  G. Zug,et al.  Age and growth of loggerhead sea turtles (Caretta caretta) of coastal Georgia : An assessment of skeletochronological age-estimates , 1997 .

[92]  K. Lohmann,et al.  The Biology of Sea Turtles, Volume III , 2002 .

[93]  I. Werneburg Temporal bone arrangements in turtles: an overview. , 2012, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[94]  R. Aguilar,et al.  Sea Turtles: A Complete Guide to Their Biology, Behavior, and Conservation , 2009 .

[95]  Susan E. Evans,et al.  Predicting muscle activation patterns from motion and anatomy: modelling the skull of Sphenodon (Diapsida: Rhynchocephalia) , 2010, Journal of The Royal Society Interface.

[96]  C. Gans,et al.  Biology of the Reptilia Volume : 11, Morphology F , 1981 .

[97]  M. Hasegawa,et al.  Phylogenetic position of turtles among amniotes: evidence from mitochondrial and nuclear genes. , 2000, Gene.

[98]  Katsufumi Sato,et al.  The ontogenetic scaling of bite force and head size in loggerhead sea turtles (Caretta caretta): implications for durophagy in neritic, benthic habitats , 2012, Journal of Experimental Biology.

[99]  P. O’Higgins,et al.  The head and neck muscles associated with feeding in Sphenodon (Reptilia: Lepidosauria: Rhynchocephalia) , 2009 .

[100]  R. McKinney,et al.  PCBs and other chlorinated organic contaminants in tissues of Juvenile Kemp's Ridley Turtles (Lepidochelys kempi) , 1994 .

[101]  P. Dutton,et al.  Molecular phylogeny for marine turtles based on sequences of the ND4-leucine tRNA and control regions of mitochondrial DNA. , 1996, Molecular phylogenetics and evolution.

[102]  O. Rieppel,et al.  Turtles as diapsid reptiles , 1996, Nature.

[103]  M. Salmon,et al.  Predation on loggerhead turtle hatchlings after entering the sea , 1992 .

[104]  R. Martin,et al.  Toward a unifying theory of bone remodeling. , 2000, Bone.

[105]  Philip G Cox,et al.  Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. , 2011, Journal of biomechanics.

[106]  S. Williston The Osteology of Some American Permian Vertebrates , 1914, The Journal of Geology.

[107]  R. Zangerl The vertebrate fauna of the Selma Formation of Alabama. Part III. The turtles of the family Protostegidae. Part IV. The turtles of the family Toxochelyidae. , 1953 .

[108]  B. King,et al.  MicroRNAs support a turtle + lizard clade , 2012, Biology Letters.

[109]  D. Bramble,et al.  Functional vertebrate morphology , 1985 .

[110]  M. Nishida,et al.  Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. , 1999, Molecular biology and evolution.

[111]  J. Sterli A new, nearly complete stem turtle from the Jurassic of South America with implications for turtle evolution , 2008, Biology Letters.

[112]  C. Cox THE PROBLEMATIC PERMIAN REPTILE EUNOTOSAURUS , 1969 .

[113]  M L Moss,et al.  A functional approach to craniology. , 1960, American journal of physical anthropology.

[114]  C. Limpus,et al.  The stomach contents of post-hatchling green and loggerhead sea turtles in the southwest Pacific: an insight into habitat association , 2008 .

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

[116]  W. J. Moore Masticatory function and skull growth , 2010 .

[117]  Robert C Thomson,et al.  Sparse supermatrices for phylogenetic inference: taxonomy, alignment, rogue taxa, and the phylogeny of living turtles. , 2010, Systematic biology.

[118]  J. Schmid,et al.  Sex ratio of immature Kemp's ridley turtles (Lepidochelys kempi) from Gullivan Bay, Ten Thousand Islands, south-west Florida , 2005, Journal of the Marine Biological Association of the United Kingdom.

[119]  R. Zangerl Patterns of Phylogenetic Differentiation in the Toxochelyid and Cheloniid Sea Turtles , 1980 .

[120]  E. S. Gaffney,et al.  Comparative cranial morphology of Recent and fossil turtles. Bulletin of the AMNH ; v. 164, article 2 , 1979 .

[121]  Leverett Allen Adams,et al.  A MEMOIR ON THE PHYLOGENY OF THE JAW MUSCLES IN RECENT AND FOSSIL VERTEBRATES , 1918 .

[122]  D. Shaver Feeding ecology of wild and head-started Kemp's ridley sea turtles in South Texas Waters , 1991 .

[123]  Nicholas G. Crawford,et al.  More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs , 2012, Biology Letters.

[124]  P. Aerts,et al.  Kinematics and functional morphology of aquatic feeding in Australian snake‐necked turtles (Pleurodira; Chelodina) , 1997, Journal of morphology.

[125]  C. Ray A sesamoid bone in the jaw musculature of Gopherus polyphemus (Reptilia: Testudiniae). , 1959, Anatomischer Anzeiger.

[126]  N. Kamezaki,et al.  Geographic Variation in Skull Morphology of the Green Turtle, Chelonia mydas, with a Taxonomic Discussion , 1995 .

[127]  S. Applegate The vertebrate fauna of the Selma Formation of Alabama. , 1970 .

[128]  E. C. Olson JAW MECHANISMS: RHIPIDISTIANS, AMPHIBIANS, REPTILES , 1961 .

[129]  E. Williams Variation and selection in the cervical central articulations of living turtles. Bulletin of the AMNH ; v. 94, article 9 , 1950 .

[130]  C. K. Dodd,et al.  Fossil sea turtles from the early Pliocene Bone Valley Formation, central Florida , 1992 .

[131]  J. F. Parham,et al.  New Sea Turtle from the Miocene of Peru and the Iterative Evolution of Feeding Ecomorphologies since the Cretaceous , 2010 .

[132]  R. Hirayama Phylogenetic systematics of chelonioid sea turtles , 1994 .

[133]  MlsclIm,et al.  An Illustrated Glossary of Turtle Skull Nomenclature , 2022 .

[134]  Marc E. H. Jones Skull shape and feeding strategy in Sphenodon and other Rhynchocephalia (Diapsida: Lepidosauria) , 2008, Journal of morphology.

[135]  V. Bels,et al.  Biology of Turtles: From Structures to Strategies of Life , 2007 .

[136]  Nina S Sverdlova,et al.  Principles of determination and verification of muscle forces in the human musculoskeletal system: Muscle forces to minimise bending stress. , 2010, Journal of biomechanics.

[137]  R. Carroll PROBLEMS OF THE ORIGIN OF REPTILES , 1969 .

[138]  Dent. G. H. Schumacher KRITISCHE STELLUNGNAHME ZU DER ARBEIT VON POGLAYEN‐NEUWALL “UNTERSUCHUNGEN DER KIEFERMUSKULATUR UND DEREN INNERVATION BEI SCHILDKRÖTEN” , 1956 .

[139]  H. R. Bustard Sea turtles: natural history and conservation , 1972 .

[140]  M. Taylor How tetrapods feed in water: a functional analysis by paradigm , 1987 .

[141]  G. Domokos,et al.  Shell geometry and habitat determination in extinct and extant turtles (Reptilia: Testudinata) , 2011, Paleobiology.

[142]  S. Williston The Phylogeny and Classification of Reptiles , 1917, The Journal of Geology.

[143]  P. Lemell,et al.  Morphology and function of the feeding apparatus of Pelusios castaneus (Chelonia; Pleurodira) , 2000, Journal of morphology.

[144]  B. Metscher MicroCT for developmental biology: A versatile tool for high‐contrast 3D imaging at histological resolutions , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[145]  H. Vallois Les transformations de la musculature de l'épisome chez les vertébrés , 1922 .

[146]  Yuichiro Hara,et al.  Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. , 2005, Molecular biology and evolution.

[147]  P. Snelderwaard,et al.  The feeding apparatus of Chelus fimbriatus (Pleurodira; Chelidae) – adaptation perfected? , 2010 .

[148]  D. Krause Jaw movement, dental function, and diet in the Paleocene multituberculate Ptilodus , 1982, Paleobiology.

[149]  I. Poglayen-Neuwall UNTERSUCHUNGEN DER KIEFERMUSKULATUR UND DEREN INNERVATION BEI SCHILDKRÖTEN , 1953 .

[150]  A. Bolten Variation in Sea Turtle Life History Patterns: Neritic vs. Oceanic Developmental Stages , 2002 .

[151]  M. Wicksten,et al.  Feeding ecology of the loggerhead sea turtle Caretta caretta in the Northwestern Gulf of Mexico , 1993 .

[153]  R. Zangerl,et al.  THE METHODS OF COMPARATIVE ANATOMY AND ITS CONTRIBUTION TO THE STUDY OF EVOLUTION , 1948, Evolution; international journal of organic evolution.

[154]  J. Hendrickson The Ecological Strategies of Sea Turtles , 1980 .

[155]  J. Frazier Misidentifications of Sea Turtles in the East Pacific: Caretta caretta and Lepidochelys olivacea , 1985 .

[156]  R. Broom On the Structure of the Reptilian Tarsus , 2009 .

[157]  A. Carr Handbook of Turtles: The Turtles of the United States, Canada, and Baja California , 1952 .

[158]  Arnold G. Kluge,et al.  AMNIOTE PHYLOGENY AND THE IMPORTANCE OF FOSSILS , 1988, Cladistics : the international journal of the Willi Hennig Society.

[159]  A. Herrel,et al.  Evolution of bite performance in turtles , 2002 .

[160]  J. Robins The biology of sea turtles. Volume II: Edited by Peter L. Lutz, John A. Musick and Jeanette Wyneken, CRC Press, Boca Raton, 2003, ISBN 0-8493-1123-3; 440 pp., USD 99.95 , 2003 .

[161]  J. Avise,et al.  Population Structure of Loggerhead Turtles (Caretta caretta) in the Northwestern Atlantic Ocean and Mediterranean Sea , 1993 .

[162]  W. Joyce,et al.  Palaeoecology of Triassic stem turtles sheds new light on turtle origins , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[163]  W. Joyce,et al.  Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage , 2012, Biology Letters.

[164]  P. O’Higgins,et al.  Shearing Mechanics and the Influence of a Flexible Symphysis During Oral Food Processing in Sphenodon (Lepidosauria: Rhynchocephalia) , 2012, Anatomical record.