Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa

Journal of Evolutionary Biology

Volumn 22, Issue 6, 2009, Pages 1153-1162

  Scheyer, T M ^a   Sander, P M ^b  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Anthodon; Bone histology; Bone profiler; Bradysaurus; Dermal armour; Pareiasauria; Pareiasaurus

Indexed keywords

BONE; EXTINCTION; FOSSIL RECORD; HISTOLOGY; MICROSTRUCTURE; PERMIAN; REPTILE; SKELETAL REMAINS;

ADAPTATION; ANIMAL; ARTICLE; BONE; FOSSIL; HISTOLOGY; PHYSIOLOGY; TURTLE;

ADAPTATION, BIOLOGICAL; ANIMALS; BONE AND BONES; FOSSILS; TURTLES;

AFRICA; SOUTH AFRICA; SOUTHERN AFRICA; SUB-SAHARAN AFRICA;

ANIMALIA; PARAREPTILIA; PAREIASAURIA; TESTUDINES;

EID: 66149104758     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01732.x     Document Type: Article

References (63)

1. Boonstra, L.D. 1934. Pareiasaurian studies, part X. The dermal armour. Ann. S. Afr. Mus. 31 : 39 48.
2. deBraga, M. Rieppel, O. 1997. Reptile phylogeny and the interrelationships of turtles. Zool. J. Linn. Soc. 120 : 281 354. (Pubitemid 127095171)
3. Buffrénil, V. de. Mazin, J.-M. 1992. Contribution de l'histologie osseuse à l'interprétation paléobiologique du genre Placodus Agassiz, 1833 (Reptilia, Placodontia). Revue Paléobiol. 11 : 397 407.
4. Buffrénil, V. de., Farlow, J.O. Ricqlès, A.de. 1986. Growth and function of Stegosaurus plates: evidence from bone histology. Paleobiology 12 : 459 473. (Pubitemid 17263866)
5. Canoville, A. Laurin, M. 2008. Microanatomical diversity of the humerus and lifestyle in lissamphibians. Acta Zool. 90 : 110 122.
6. Castanet, J., Curry Rogers, K., Cubo, J. Boisard, J.-J. 2000. Periosteal bone growth rates in extant ratites (ostrich and emu). Implications for assessing growth in dinosaurs. C. R. Acad. Sci. 323 : 543 550. (Pubitemid 30458613)
7. Currey, J.D. Alexander, R.M. 1985. The thickness of the walls of tubular bones. J. Zool. Lond. 206 : 453 468.
8. Findlay, G.H. 1970. Skin structure of small pareiasaurs. Palaeontol. Afr. 13 : 15 23.
9. Gaffney, E.S. 1990. The comparative osteology of the Triassic turtle Proganochelys. Bull. Am. Mus. Nat. Hist. 194 : 1 263.
10. Germain, D. Laurin, M. 2005. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool. Scr. 34 : 335 350. (Pubitemid 40886727)
11. Girondot, M. Laurin, M. 2003. Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J. Vertebr. Paleontol. 23 : 458 461. (Pubitemid 36941802)
12. Gregory, W.K. 1946. Pareiasaurs versus placodonts as near ancestors to the turtles. Bull. Am. Mus. Nat. Hist. 86 : 275 326.
13. Haughton, S.H. Boonstra, L.D. 1929. Pareiasaurian studies. Part I. An attempt at a classification of the Pareiasauria based on skull features. Ann. S. Afr. Mus. 28 : 79 87.
14. Hill, R.V. 2005. Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. Syst. Biol. 54 : 530 547. (Pubitemid 41356468)
15. Huene, F. von. 1944. Pareiasaurierreste aus dem Ruhuhu-Gebiet. Palaeontol. Z. 23 : 386 410.
16. Hua, S. Buffrénil, V. de. 1996. Bone histology as a clue in the interpretation of functional adaptations in the Thalattosuchia (Reptilia, Crocodylia). J. Vertebr. Paleontol. 16 : 703 717. (Pubitemid 126311901)
17. Horner, J.R., Ricqlés, A. de Padian, K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25 : 295 304. (Pubitemid 30049119)
18. Huene, F. von. 1956. Paläontologie und Phylogenie der Niederen Tetrapoden. Gustav Fisher Verlag, Jena.
19. Iwabe, N., Hara, Y., Kumazawa, Y., Shibamoto, K., Saito, Y., Miyata, T. Katoh, K. 2004. Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol. Biol. Evol. 22 : 810 813. (Pubitemid 40471395)
20. Jalil, N.-E. Janvier, P. 2005. Les pareiasaures (Amniota, Parareptilia) du Permien supérieur du Bassin d'Argana, Maroc. Geodiversitas 27 : 35 132. (Pubitemid 40579016)
21. Jiang, Z.J., Castoe, T.A., Austin, C.C., Burbrinh, F.T., Herron, M.D., McGuire, J.A., Parkinson, C.L. Pollock, D.D. 2007. Comparative mitochondrial genomics of snakes: extraordinary rate dynamics and functionality of the duplicate control region. BMC Evol. Biol. 7 : 123 (doi :). (Pubitemid 47301725)
22. Joyce, W.G. Gauthier, J.A. 2004. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proc. R. Soc. Lond. B 271 : 1 5. (Pubitemid 38096088)
23. Klein, N., Scheyer, T.M. Tütken, T. 2009. Long bone and osteoderm bone histological skeletochronology and isotope data of an individual specimen of Alligator mississippiensis (Crocodylia: Alligatoridae). Fossil Rec., in press.
24. Kozur, H.W. Bachmann, G.H. 2008. Updated correlation of the Germanic Triassic with the Tethyan scale and assigned numeric ages. In : Upper Triassic Subdivisions, Zonations and Events: Meeting of the late IGCP 467 and STS: Abstracts and Excursion-Guide. Berichte der Geologischen Bundesanstalt, Vol. 76, 28 September-2 October 2008, Bad Goisern (L. Krystyn G.W. Mandl, eds pp. 53 58. Geologische Bundesanstalt, Wien.
25. Kriloff, A., Germain, D., Canoville, A., Vincent, P., Sache, M. Laurin, M. 2008. Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. J. Evol. Biol. 21 : 807 826.
26. Laurin, M. Reisz, R.R. 1995. A reevaluation of early amniote phylogeny. Zool. J. Linn. Soc. 113 : 165 223.
27. Laurin, M., Girondot, M. Loth, M.-M. 2004. The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30 : 589 613. (Pubitemid 39455013)
28. Lee, M.S.Y. 1993. The origin of the turtle body plan: bridging a famous morphological gap. Science 261 : 1716 1720. (Pubitemid 23982899)
29. Lee, M.S.Y. 1995. Historical burden in systematics and interrelationships of "parareptiles". Biol. Rev. 70 : 459 547.
30. Lee, M.S.Y. 1996. Correlated progression and the origin of turtles. Nature 379 : 812 815. (Pubitemid 26067719)
31. Lee, M.S.Y. 1997a. Pareiasaur phylogeny and the origin of turtles. Zool. J. Linn. Soc. 120 : 197 280. (Pubitemid 127170685)
32. Lee, M.S.Y. 1997b. Reptile relationships turn turtle. Nature 389 : 245 246. (Pubitemid 27406630)
33. Levrat-Calviac, V. Zylberberg, L. 1986. The structure of the osteoderms in the gekko: Tarentola mauritanica. Am. J. Anat. 176 : 437 446. (Pubitemid 16045791)
34. Li, C., Wu, X.-C., Rieppel, O., Wang, L.-T. Zhao, L.-J. 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456 : 497 501. (Pubitemid 352759012)
35. Main, R.P., Ricqlès, A. de., Horner, J.R. Padian, K. 2005. The evolution and function of thyreophoran dinosaur scutes: implications for plate function in stegosaurs. Paleobiology 31 : 291 314. (Pubitemid 40906535)
36. McCrea, R.T., Lockley, M.G. Meyer, C.A. 2001. Global distribution of purported ankylosaur track occurrences. In : The Armored Dinosaurs (K. Carpenter, ed. pp. 413 454. Indiana University Press, Bloomington.
37. Müller, J. 2003. Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 90 : 473 476. (Pubitemid 37363558)
38. Owen, R. 1876. Descriptive and Illustrated Catalogue of the Fossil Reptilia of South Africa in the Collection of the British Museum. Order of the Trustees, London.
39. Piveteau J. (ed 1955. Traité de Paléontologie. Tome V - Amphibiens, Reptiles, Oiseaux. Masson et Cie, Paris.
40. Reisz, R.R. Head, J.J. 2008. Turtle origins out to sea. Nature 456 : 450 451.
41. Reisz, R.R. Laurin, M. 1991. Owenetta and the origin of turtles. Nature 349 : 324 326. (Pubitemid 21912073)
42. Rest, J.S.R., Ast, J.C., Austin, C.C., Waddell, P.J., Tibbetts, E.A., Hay, J.M. Mindell, D.P. 2003. Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol. Phylogenet. Evol. 29 : 289 297. (Pubitemid 38370217)
43. Rhodin, A.G.J. 1985. Comparative chondro-osseous development and growth of marine turtles. Copeia 1985 : 752 771.
44. Ricqlès, A. de. 1978a. Recherches paléohistologiques sur les os longs des tétrapodes. VII. - Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des tétrapodes. Troisième partie. IV. Les problèmes du déterminisme des types de tissus osseux. Ann. Paléontol. 64 : 153 184.
45. Ricqlès, A. de. 1978b. Recherches paléohistologiques sur les os longs des tétrapodes. VII. - Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des tétrapodes. Troisième partie. Évolution: considérations phylogénétiques. Ann. Paléontol. 64 : 85 111.
46. Ricqlès, A. de Buffrénil, V. de. 2001. Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In : Secondary Adaptations of Tetrapods to Life in Water (J.-M. Mazin V. de Buffrénil, eds pp. 289 310. Verlag Dr. Friedrich Pfeil, München.
47. Ricqlès, A. de., Pereda Suberbiola, X., Gasparini, Z. Olivero, E. 2001. Histology of dermal ossifications in an ankylosaurian dinosaur from the Late Cretaceous of Antarctica. Asociación Paleontológica Argentina. Publicación Especial 7 : 171 174.
48. Rieppel, O. 2008. The relationships of turtles within amniotes. In : Biology of Turtles (J. Wyneken, M.H. Godfrey V. Bels, eds pp. 345 353. CRC Press, Boca Raton.
49. Rieppel, O. Reisz, R.R. 1999. The origin and early evolution of turtles. Annu. Rev. Ecol. Syst. 30 : 1 22. (Pubitemid 30065619)
50. Scheyer, T.M. 2007a. Comparative bone histology of the turtle shell (carapace and plastron): implications for turtle systematics, functional morphology, and turtle origins. Mathematisch-Naturwissenschaftliche Fakultät. PhD Thesis, University of Bonn, Bonn. pp. 343 [URN: http://nbn-resolving.de/urn:nbn:de:hbz:5N-12299 ; URL: http://hss.ulb.uni-bonn. de/diss-online/math-nat-fak/2007/scheyer-torsten ].
51. Scheyer, T.M. 2007b. Skeletal histology of the dermal armor of Placodontia: the occurrence of 'postcranial fibro-cartilaginous bone' and its developmental implications. J. Anat. 211 : 737 753. (Pubitemid 350182602)
52. Scheyer, T.M. Sánchez-Villagra, M.R. 2007. Carapace bone histology in the giant pleurodiran turtle Stupendemys geographicus: phylogeny and function. Acta Palaeontol. Pol. 52 : 137 154. (Pubitemid 46510676)
53. Scheyer, T.M. Sander, P.M. 2004. Histology of ankylosaur osteoderms: implications for systematics and function. J. Vertebr. Paleontol. 24 : 874 893. (Pubitemid 40032834)
54. Scheyer, T.M. Sander, P.M. 2007. Terrestrial palaeoecology for basal turtles indicated by shell bone histology. Proc. R. Soc. Lond. B 274 : 1885 1893.
55. Scheyer, T.M., Sander, P.M., Joyce, W.G., Böhme, W. Witzel, U. 2007. A plywood structure in the shell of fossil and living soft-shelled turtles (Trionychidae) and its evolutionary implications. Org. Divers. Evol. 7 : 136 144. (Pubitemid 47031720)
56. Sidor, C.A., Blackburn, D.C. Gado, B. 2003. The vertebrate fauna of the Upper Permian of Niger - II, Preliminary description of a new pareiasaur. Palaeontol. Afr. 39 : 45 52. (Pubitemid 38688628)
57. Snover, M.L. Rhodin, A.G.J. 2008. Comparative ontogenetic and phylogenetic aspects of chelonian chondro-osseous growth and skeletochronology. In : Biology of Turtles (J. Wyneken, M.H. Godfrey V. Bels, eds pp. 17 43. CRC Press, Boca Raton.
58. Spencer, P.S. Lee, M.S.Y. 2000. A juvenile Elginia and early growth in pareiasaurs. J. Paleontol. 74 : 1191 1195. (Pubitemid 32145311)
59. Vickaryous, M.K. Hall, B.K. 2008. Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. J. Morphol. 269 : 398 422.
60. Vickaryous, M.K., Maryańska, T. Weishampel, D.B. 2004. Ankylosauria. In : The Dinosauria, 2nd edn (D.B. Weishampel, P. Dodson H. Osmólska, eds pp. 363 392. University of California Press, Berkeley.
61. Wang, X., Bachmann, G.H., Hagdorn, H., Sander, P.M., Cuny, G., Chen, X., Wang, C., Chen, L., Cheng, L., Meng, F. Xu, G. 2008. The Late Triassic black shales of the Guanling area, Guizhou Province, south-west China: a unique marine reptile and pelagic crinoid fossil lagerstätte. Palaeontology 51 : 27 61.
62. Watson, D.M.S. 1914. On the skull of a pariasaurian reptile, and on the relationships of that type. Proc. Zool. Soc. Lond. 1 : 155 180.
63. Zylberberg, L. Castanet, J. 1985. New data on the structure and the growth of the osteoderms in the reptile Anguis fragilis L. (Anguidae, Squamata). J. Morphol. 186 : 327 342. (Pubitemid 16208322)