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Shell bone histology of the long-necked chelid Yaminuechelys (Testudines: Pleurodira) from the late Cretaceous—early Palaeocene of Patagonia with comments on the histogenesis of bone ornamentation

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Abstract

Yaminuechelys is a long-necked chelid turtle whose remains have been recovered from outcrops of the Santonian-Maastrichtian and Danian of South America. With the purpose of providing data about shell sculpturing origin and palaeoecology, the bone histology of several shell elements (including neural, costal, peripheral and plastral plates) of Yaminuechelys is described herein. Histological analysis reveals that Yaminuechelys shares with Chelidae the presence of interwoven structural fibre bundles in the external cortex, and parallel-fibred bone of the internal cortex. The presence of resorption lines in several samples indicates that the particular ornamentation of the external surfaces originated, at least in part, by focalized resorption and new bone deposition. This mechanism for ornamentation origin and maintenance is here described for the first time in a turtle. Compactness of the shell bones is consistent with an aquatic habitat, which supports previous hypothesis based on palaeoenvironmental and morphological data.

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Abbreviations

MPEF-PV:

Paleovertebrate collection of the Museo Paleontológico “Egidio Feruglio”, Trelew, Chubut, Argentina

MAU-Ph:

Paleohistological collection of the Museo Municipal “Argentino Urquiza”, Rincón de los Sauces, Neuquén, Argentina

N:

Narambuena collection

CO:

Cerro Overo collection

PR:

Puesto La Rinconada collection

LI:

La Invernada collection

References

  • Bona P, de la Fuente MS (2005) Phylogenetic and paleobiogeographic implications of Yaminuechelys maior (Staesche, 1929) new comb., a large long-necked chelid turtle from the early Paleocene of Patagonia, Argentina. J Vertebr Paleont 25:569–582

    Article  Google Scholar 

  • Bona P, Cladera G, de la Fuente MS (1998) Las tortugas pleurodiras de la Formación Salamanca (Paleoceno inferior) en el área de Cerro Hansen, Provincia de Chubut, Argentina. X Congr Latinoamer Geología VI Congr Naci Geol Económica, Actas 1:268–273

    Google Scholar 

  • Boulenger C (1889) Catalogue of the Chelonians, Rhynchocephalians and Crocodiles in the British Museum (Natural History). Trustees British Museum (Natural History). pp 311

  • Cadena AE, Ksepka DT, Norell MA (2013) New material of Mongolemys elegans Khosatzky and Mlynarski, 1971 (Testudines: Lindholmemydidae), from the Late Cretaceous of Mongolia with comments on bone histology and phylogeny. Am Mus Nov 3766:1–27

    Article  Google Scholar 

  • Cerda IA, Desojo JB (2011) Dermal armour histology of aetosaurs (Archosauria: Pseudosuchia), from the Upper Triassic of Argentina and Brazil. Lethaia 44:417–428

    Article  Google Scholar 

  • Cerda IA, Sterli J, Scheyer T (2015) Bone shell microstructure of the Condorchelys antiqua Sterli 2008, a stem turtle from the Jurassic of Patagonia. C R Palevol 821:1–14. doi:10.1016/j.crpv.2015.01.004

    Google Scholar 

  • Chinsamy A, Raath MA (1992) Preparation of fossil bone for histological examination. Palaeontol Afr 29:39–44

    Google Scholar 

  • de Buffrénil V (1982) Morphogenesis of bone ornamentation in extant and extinct crocodilians. Zoomorphology 99:155–166

    Article  Google Scholar 

  • de Buffrénil V, Farlow JO, de Ricqlès A (1986) Growth and function of Stegosaurus plates: evidence from bone histology. Paleobiology 12:459–473

    Google Scholar 

  • de Buffrénil V, Clarac F, Fau M, Martin S, Martin B, Pellé E, Laurin M (2014) Differentiation and growth of bone ornamentation in vertebrates: a comparative histological study among the Crocodylomorpha. J Morphol 276:425–445

    Article  PubMed  Google Scholar 

  • de la Fuente MS (1999) A review of the Pleistocene reptiles of Argentina: taxonomic and palaeoenvironmental considerations. Quat South Am Antar Penin 12:111–138

    Google Scholar 

  • de la Fuente MS, Lapparent de Broin F, Manera de Bianco T (2001) The oldest and first nearly complete skeleton of a chelid, of the Hydromedusa sub-group (Chelidae, Pleurodira), from the Upper Cretaceous of Patagonia. Bull Soc Géol France 172:237–244

    Article  Google Scholar 

  • de la Fuente MS, Salgado L, Albino A, Báez AM, Bonaparte JF, Calvo JO, Chiappe LM, Codorniú LS, Coria RA, Gasparini Z, González Riga BJ, Novas FE, Pol D (2007) Tetrápodos continentales del Cretácico de la Argentina: una síntesis actualizada. Asoc Paleontol Arg Publ Esp 11:137–153

    Google Scholar 

  • de la Fuente MS, Barbieri R, Chafrat P (2010) Una tortuga Chelidae (Testudines: Pleurodira) de cuello largo en el Grupo Neuquén, Río Negro, Argentina. Significado cronológico y paleobiogeográfico. Andean Geol 37:399–413

    Google Scholar 

  • de la Fuente MS, Sterli J, Maniel IJ (2014) Origin, Evolution and Biogeographic History of South American Turtles. Springer Earth System Sciences, Heidelberg

    Book  Google Scholar 

  • de la Fuente MS, Maniel IJ, Jannello JM, Filippi LS, Cerda I (2015) Long-necked chelid turtles from the Campanian of northwestern Patagonia with comments on K/P survivorship of the genus Yaminuechelys. C R Palevol 14:563–576

    Article  Google Scholar 

  • Filippi LS, Garrido AC (2012) Nuevo registro del género Dinilysia (Squamata, Serpentes) para la Formación Anacleto (Campaniano Inferior-Medio), Rincón de Los Sauces, Neuquén, Argentina. Ameghiniana 49:132–136

    Article  Google Scholar 

  • Filippi LS, García RA, Garrido AC (2011) A new titanosaur sauropod dinosaur from the Upper Cretaceous of North Patagonia, Argentina. Acta Palaeontol Pol 56:505–520

    Article  Google Scholar 

  • Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY, Zylberberg L, de Ricqlès A (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG (ed) Skeletal biomineralization: patterns, processes and evolutionary trends. Van Nostrand Reinhold, New York, pp 471–548

    Google Scholar 

  • Frazer J (1986) Epizoic barnacles on pleurodiran turtles: is the relation rare? Proc Biol Soc Washington 99:472–477

    Google Scholar 

  • Gaffney ES (1977) The side-necked turtle family Chelidae: a theory of relationship using shared derived characters. Amer Mus Nov 2681:1–23

    Google Scholar 

  • Georges A, Birrell J, Saint KM, McCord W, Donnellan SC (1998) A phylogeny for side-necked turtle (Chelonia: Pleurodira) based on mitochondrial and nuclear gene sequence variation. Biol J Linn Soc 67:213–246

    Article  Google Scholar 

  • Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleont 23:458–461

    Article  Google Scholar 

  • Guillon JM, Guéry L, Hulin V, Girondot M (2012) A large phylogeny of turtles (Testudines) using molecular data. Contrib Zool 81:147–158

    Google Scholar 

  • Hayashi S, Carpenter K, Suzuki D (2009) Different growth patterns between the skeleton and osteoderms of Stegosaurus (Ornithischia: Thyreophora). J Vertebr Paleont 29:123–131

    Article  Google Scholar 

  • Hill RV (2006) Comparative anatomy and histology of xenarthran osteoderms. J Morphol 267:1441–1460

    Article  PubMed  Google Scholar 

  • Hua S, de Buffrénil V (1996) Bone histology as a clue in the interpretation of functional adaptations in the thalattosuchia (Reptilia, Crocodylia). J Vertebr Paleont 16:703–717

    Article  Google Scholar 

  • Jannello JM, Cerda IA, de la Fuente MS (2014) Estudio histológico comparativo del caparazón óseo de quelidos de cuello largo (Testudines: Pleurodira) del Paléogeno de Patagonia: Datos preliminares. Ameghiniana 51:14

    Google Scholar 

  • Joyce WG, Gauthier JA (2004) Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proc R Soc London B 271:1–5

    Article  Google Scholar 

  • Main RP, de Ricqlès A, Horner J, Padian K (2005) The evolution and function of thyreophoran dinosaur scutes: implications for plate function in stegosaurs. Paleobiology 31:291–314

    Article  Google Scholar 

  • Maniel IJ, de la Fuente MS, Sterli J (2012) New material of Hydromedusa casamayorensis from the Middle Eocene of Patagonia and its phylogenetic implications. Symposium on turtle evolution, Tübingen, Germany. Programe and Abstract 29

  • Pérez-Garcia A, Scheyer TM, Murelaga X (2012) New interpretations of Dortoka vasconica Lapparent de Broin and Murelaga, a freshwater turtle with an unusual caparace. Cret Res 36:151–161

    Article  Google Scholar 

  • Pérez-García A, Scheyer TM, Murelaga X (2013) The turtles from the uppermost Jurassic and Early Cretaceous of Galve (Iberian Range, Spain): anatomical, systematic, biostratigraphic and palaeobiogeographical implications. Cret Res 44:64–82

    Article  Google Scholar 

  • Scheyer TM (2007) Skeletal histology of the dermal armor of Placodontia: the occurrence of postcranial fibro-cartilaginous bone and its developmental implications. J Anat 211:737–753

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheyer TM (2008) Aging the oldest turtles: the placodont affinities of Priscochelys hegnabrunnensis. Naturwissenschaften 95:803–810

    Article  CAS  PubMed  Google Scholar 

  • Scheyer TM (2009) Conserved bone microstructure in the shells of long-necked and short-necked chelid turtles (Testudinata, Pleurodira). Fossil Rec 12:47–57

    Article  Google Scholar 

  • Scheyer TM, Sanchez-Villagra MR (2007) Carapace bone histology in the giant pleurodiran turtle Stupendemys geographicus: phylogeny and function. Acta Pal Pol 52:137–154

    Google Scholar 

  • Scheyer TM, Sander PM (2004) Histology of ankylosaur osteoderms: implications for systematics and function. J Vertebr Paleont 24:874–893

    Article  Google Scholar 

  • Scheyer TM, Sander PM (2007) Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proc Royal Soc B 274:1885–1893

    Article  Google Scholar 

  • Scheyer TM, Sander PM (2009) Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaurs taxa from the Permian of South Africa. J Evol Biol 22:1153–1162

    Article  CAS  PubMed  Google Scholar 

  • Scheyer TM, Sander PM, Joyce WG, Bohme W, Witzel U (2007) Unique plywood structure in the shell of fossil and recent soft shelled turtles (Trionychidae) revealed by soft tissue and bone histology: a key adaptation? Org Divers Evol 7:136–144

    Article  Google Scholar 

  • Scheyer TM, Danilov IG, Sukhanov VB, Syromyatnikova EV (2014a) The shell bone histology of fossil and extant marine turtles revisited. Biol J Linnean Soc 112:701–718

    Article  Google Scholar 

  • Scheyer TM, Pérez-García A, Murelaga X (2014b) Shell bone histology of solemydid turtles (stem Testudines): palaeoecological implications. Org Divers Evol 15:199–212

    Article  Google Scholar 

  • Seddon JM, Georges A, Baverstock PR, McCord W (1997) Phylogenetic relationship of chelid turtles (Pleurodira: Chelidae) based on mitochondrial 12S rRNA sequence variation. Mol Phyl Evol 7:55–61

    Article  CAS  Google Scholar 

  • Staesche K (1929) Schildkrötenreste aus der oberen Kreide Patagoniens. Palaeontographica A 72:103–112

    Google Scholar 

  • Sterli J, Pol D, Laurin M (2013) Incorporating phylogenetic uncertainty on phylogeny-based palaeontological dating and the timing of turtle diversification. Cladistics 29:233–246

    Article  Google Scholar 

  • Vlachos E, Cerda IA, Tsoukala E (2015) The morphology and bone histology of the first soft–shelled turtle from the Pliocene of Greece. Sci Nat. doi:10.1007/s00114-015-1295-2

    Google Scholar 

  • Witzmann F (2009) Comparative histology of sculptured dermal bones in basal tetrapods, and the implications for the soft tissue dermis. Palaeodiv 2:233–270

    Google Scholar 

  • Witzmann F, Soler-Gijon R (2008) The bone histology of osteoderms in temnospondyl amphibians and in the chroniosuchian Bystrowiella. Acta Zool (Stockholm) 89:1–19

    Google Scholar 

  • Zangerl R (1953) The vertebrate fauna of the Selma Formation of Alabama. Part IV. The turtles of the family Toxochelyidae. Field Geol Mem 3:137–277

    Google Scholar 

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Acknowledgments

The authors thank M. Caffa (Museo Egidio Feruglio) for the skilful preparation of the histological sections, Leonardo Filippi (Museo Argentino Urquiza) and Juliana Sterli (Museo Egidio Feruglio) for finding the fossils studied here, and John Whitlock for valuable remarks on the English of the manuscript. The authors would also like to thank Editor, Sven Thatje and three anonymous reviewers for their helpful suggestions for the improvement of this manuscript. This paper was partially supported by Proyecto de Investigación Científica y Tecnológica 2013–0095 (Marcelo de la Fuente) and Proyecto de Investigación Científica y Tecnológica 2010–0646 (Juliana Sterli) granted by the Agencia Nacional de Promoción Científica y Tecnológica.

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Correspondence to Juan Marcos Jannello.

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Communicated by: Sven Thatje

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Jannello, J.M., Cerda, I.A. & de la Fuente, M.S. Shell bone histology of the long-necked chelid Yaminuechelys (Testudines: Pleurodira) from the late Cretaceous—early Palaeocene of Patagonia with comments on the histogenesis of bone ornamentation. Sci Nat 103, 26 (2016). https://doi.org/10.1007/s00114-016-1346-3

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