Novel data on aetosaur (Archosauria, Pseudosuchia) osteoderm microanatomy and histology: palaeobiological implications

One of the most striking features of aetosaurs is the possession of an extensive bony armour composed of dorsal, ventral and appendicular osteoderms. With the purpose of establishing the main histological changes during ontogeny and the degree of histological variation within the armour, we analysed the bone histology of dorsal (paramedian and lateral), ventral and appendicular osteoderms from different taxa from the Late Triassic of South America, including Aetosauroides scagliai, Aetobarbakinoides brasiliensis and Neoaetosauroides engaeus. Histological data support an intramembranous origin for osteoderms. Nevertheless, evidence for metaplastic ossification (i.e. structural fibres) at advanced ontogenetic stages, in at least some elements, is also present. A variant type of parallel fibred bone, which we have named ‘crossed parallel fibred bone’, is characterized for aetosaurs. In this pseudosuchian group, osteoderms exhibit very important microstructural changes during ontogeny, which can be useful for determining ontogenetic stages from isolated elements. Histological data suggest a relatively early onset of sexual maturity among aetosaurs. Microanatomical analysis from different taxa reveal that having high values of compactness is the plesiomorphic condition for Aetosauria. The notably increased compactness of the osteoderms does not appear to be related to size, ontogeny, sex or reproductive status of the individuals. Although a high degree of compactness of osteoderms and other bones has been considered as evidence for an aquatic lifestyle in vertebrates, such an inference contradicts the current concept of a fully terrestrial lifestyle in aetosaurs.

[1]  S. Nesbitt,et al.  The osteoderm microstructure in doswelliids and proterochampsids and its implications for palaeobiology of stem archosaurs , 2017 .

[2]  F. Clarac,et al.  Comparative data on the differentiation and growth of bone ornamentation in gnathostomes (Chordata: Vertebrata) , 2016, Journal of morphology.

[3]  I. Cerda,et al.  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 , 2016, The Science of Nature.

[4]  I. Cerda,et al.  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 , 2016, The Science of Nature.

[5]  W. Parker Revised phylogenetic analysis of the Aetosauria (Archosauria: Pseudosuchia); assessing the effects of incongruent morphological character sets , 2016, PeerJ.

[6]  R. Schoch,et al.  Cranial anatomy of the aetosaur Paratypothorax andressorum Long & Ballew, 1985, from the Upper Triassic of Germany and its bearing on aetosaur phylogeny , 2016 .

[7]  M. Vickaryous,et al.  Armored geckos: A histological investigation of osteoderm development in Tarentola (Phyllodactylidae) and Gekko (Gekkonidae) with comments on their regeneration and inferred function , 2015, Journal of morphology.

[8]  M. Vickaryous,et al.  Armored geckos: A histological investigation of osteoderm development in Tarentola (Phyllodactylidae) and Gekko (Gekkonidae) with comments on their regeneration and inferred function , 2015, Journal of morphology.

[9]  Z. Gasparini,et al.  HISTOLOGY OF DERMAL OSSIFICATIONS IN AN ANKYLOSAURIAN DINOSAUR FROM THE LATE CRETACEOUS OF ANTARCTICA , 2015 .

[10]  A. Heckert,et al.  Intraspecific Variation in Aetosauroides scagliai Casamiquela (Archosauria: Aetosauria) from the Upper Triassic of Argentina and Brazil: An Example of Sexual Dimorphism? , 2015 .

[11]  T. Scheyer,et al.  Osteoderm histology of Proterochampsia and Doswelliidae (Reptilia: Archosauriformes) and their evolutionary and paleobiological implications , 2015, Journal of morphology.

[12]  J. Powell,et al.  Morphology, Microanatomy, and Histology of Titanosaur (Dinosauria, Sauropoda) Osteoderms from the Upper Cretaceous of Patagonia , 2015 .

[13]  R. Webb,et al.  A New Aetosaur (Archosauria, Suchia) from the Upper Triassic Pekin Formation, Deep River Basin, North Carolina, U.S.A., and Its Implications for Early Aetosaur Evolution , 2015 .

[14]  A. Houssaye Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation , 2014 .

[15]  D. Vasconcellos,et al.  Osteoderm accretion as proxy for whole body growth in the American alligator (1161.3) , 2014 .

[16]  J. Desojo,et al.  A new aetosaur from the Upper Triassic of the Santa Maria Formation, southern Brazil. , 2014, Zootaxa.

[17]  T. Scheyer,et al.  Bone Histology of Phytosaur, Aetosaur, and Other Archosauriform Osteoderms (Eureptilia, Archosauromorpha) , 2014, Anatomical record.

[18]  C. Schultz,et al.  Osteoderm microstructure of "rauisuchian" archosaurs from South America , 2013 .

[19]  T. Sulej,et al.  Aetosauria: a clade of armoured pseudosuchians from the Upper Triassic continental beds , 2013 .

[20]  I. Cerda,et al.  Growth curve of Aetosauroides scagliai Casamiquela 1960 (Pseudosuchia: Aetosauria) inferred from osteoderm histology , 2013 .

[21]  V. Buffrénil,et al.  Microstructure and Mineralization of Vertebrate Skeletal Tissues , 2013 .

[22]  Stewart L. Macdonald,et al.  Gross morphology and microstructure of type locality ossicles of Psephophorus polygonus Meyer, 1847 (Testudines, Dermochelyidae) , 2013, Geological Magazine.

[23]  A. Houssaye,et al.  Palaeoecological and morphofunctional interpretation of bone mass increase: an example in Late Cretaceous shallow marine squamates , 2013, Biological reviews of the Cambridge Philosophical Society.

[24]  M. Buchwitz,et al.  Osteoderm microstructure indicates the presence of a crocodylian-like trunk bracing system in a group of armoured basal tetrapods , 2012 .

[25]  V. Morra,et al.  40Ar–39Ar ages and isotope geochemistry of Cretaceous basalts in northern Madagascar: refining eruption ages, extent of crustal contamination and parental magmas in a flood basalt province , 2012, Geological Magazine.

[26]  D. Wolf,et al.  Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): Implications for systematics, osteoderm growth, and biomechanical adaptation , 2012, Journal of morphology.

[27]  Edio-Ernst Kischlat,et al.  A new aetosaur genus (Archosauria: Pseudosuchia) from the early Late Triassic of southern Brazil , 2012 .

[28]  S. Hayashi,et al.  Ontogenetic histology of Stegosaurus plates and spikes , 2012 .

[29]  I. Cerda,et al.  Dermal armour histology of aetosaurs (Archosauria: Pseudosuchia), from the Upper Triassic of Argentina and Brazil , 2011 .

[30]  T. Scheyer,et al.  Palaeohistology and external microanatomy of rauisuchian osteoderms (Archosauria: Pseudosuchia) , 2011 .

[31]  S. Nesbitt The Early Evolution of Archosaurs: Relationships and the Origin of Major Clades , 2011 .

[32]  M. Ezcurra,et al.  A Reappraisal of the Taxonomic Status of Aetosauroides (Archosauria, Aetosauria) Specimens from the Late Triassic of South America and Their Proposed Synonymy with Stagonolepis , 2011 .

[33]  J. Powell,et al.  Dermal Armor Histology of Saltasaurus loricatus, an Upper Cretaceous Sauropod Dinosaur from Northwest Argentina , 2010 .

[34]  J. Martz,et al.  Using Positional Homology in Aetosaur (Archosauria: Pseudosuchia) Osteoderms to Evaluate the Taxonomic Status of Lucasuchus hunti , 2010 .

[35]  S. Lucas,et al.  Articulated Skeletons of the Aetosaur Typothorax coccinarum Cope (Archosauria: Stagonolepididae) from the Upper Triassic Bull Canyon Formation (Revueltian: Early-Mid Norian), Eastern New Mexico, USA , 2010 .

[36]  F. Witzmann,et al.  The bone histology of osteoderms in temnospondyl amphibians and in the chroniosuchian Bystrowiella , 2010 .

[37]  A. Houssaye,et al.  "Pachyostosis" in aquatic amniotes: a review. , 2009, Integrative zoology.

[38]  T. Scheyer,et al.  Skeletochronology and isotopic analysis of a captive individual of Alligator mississippiensis Daudin, 1802 , 2009 .

[39]  T. Scheyer,et al.  Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa , 2009, Journal of evolutionary biology.

[40]  F. Witzmann Comparative histology of sculptured dermal bones in basal tetrapods, and the implications for the soft tissue dermis , 2009 .

[41]  R. Irmis,et al.  A New Desmatosuchine Aetosaur (Archosauria: Suchia) from the Upper Triassic Tecovas Formation (Dockum Group) of Texas , 2008 .

[42]  B. Hall,et al.  Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms , 2008, Journal of morphology.

[43]  T. Joanen,et al.  Herpetologists ' League Growth Rates of American Alligators in Louisiana , 2008 .

[44]  R. Schoch Osteology of the small archosaur Aetosaurus from the Upper Triassic of Germany , 2007 .

[45]  A. Báez,et al.  CRANIAL MORPHOLOGY OF THE LATE TRIASSIC SOUTH AMERICAN ARCHOSAUR NEOAETOSAUROIDES ENGAEUS: EVIDENCE FOR AETOSAURIAN DIVERSITY , 2007 .

[46]  B. Small,et al.  TECOVASUCHUS CHATTERJEEI, A NEW AETOSAUR (ARCHOSAURIA: STAGONOLEPIDIDAE) FROM THE TECOVAS FORMATION (CARNIAN, UPPER TRIASSIC) OF TEXAS , 2006 .

[47]  S. Lucas,et al.  New data on the anatomy and relationships of the Paleocene crocodylian Akanthosuchus langstoni , 2006 .

[48]  A. Chinsamy-Turan The Microstructure of Dinosaur Bone: Deciphering Biology with Fine-Scale Techniques , 2005 .

[49]  J. Desojo,et al.  El esqueleto postcraneano de Neoaetosauroides (Archosauria: Aetosauria) del Triásico Superior del centro-oeste de Argentina , 2005 .

[50]  P. M. Sander,et al.  HISTOLOGY OF ANKYLOSAUR OSTEODERMS: IMPLICATIONS FOR SYSTEMATICS AND FUNCTION , 2004 .

[51]  V. Buffrénil Morphogenesis of bone ornamentation in extant and extinct crocodilians , 1982, Zoomorphology.

[52]  V. Buffrénil,et al.  VERMIFORM BONES AND THE EVOLUTION OF GIGANTISM IN MEGALANIA—HOW A REPTILIAN FOX BECAME A LION , 2003 .

[53]  J. Currey The many adaptations of bone. , 2003, Journal of biomechanics.

[54]  M. Girondot,et al.  BONE PROFILER: A TOOL TO QUANTIFY, MODEL, AND STATISTICALLY COMPARE BONE-SECTION COMPACTNESS PROFILES , 2003 .

[55]  S. Lucas,et al.  SOUTH AMERICAN OCCURRENCES OF THE ADAMANIAN (LATE TRIASSIC:LATEST CARNIAN) INDEX TAXON STAGONOLEPIS (ARCHOSAURIA: AETOSAURIA) AND THEIR BIOCHRONOLOGICAL SIGNIFICANCE , 2002 .

[56]  Rafael A. García,et al.  Baezia vulcania sp. n., an endogeous weevil from La Palma I. (Canary Is.) (Coleoptera: Curculionidae: Molytinae) , 2002 .

[57]  M. A. Taylor Functional significance of bone ballastin in the evolution of buoyancy control strategies by aquatic tetrapods , 2000 .

[58]  S. Lucas,et al.  A new aetosaur (Reptilia: Archosauria) from the Upper Triassic of Texas and the phylogeny of aetosaurs , 1999 .

[59]  C. Brochu,et al.  How the ‘terror crocodile’ grew so big , 1999, Nature.

[60]  Frankie D. Jackson,et al.  Sauropod dinosaur embryos from the Late Cretaceous of Patagonia , 1998, Nature.

[61]  P. Wilkinson,et al.  Growth rates of American alligators in coastal South Carolina , 1997 .

[62]  A. Tucker Validation of skeletochronology to determine age of freshwater crocodiles (Crocodylus johnstoni) , 1997 .

[63]  V. Buffrénil,et al.  Bone histology as a clue in the interpretation of functional adaptations in the Thalattosuchia (Reptilia, Crocodylia) , 1996 .

[64]  Anusuya Chinsamy,et al.  Preparation of fossil bone for histological examination , 1992 .

[65]  B. Hall Bone matrix and bone specific products , 1991 .

[66]  M. Báez,et al.  Adaptation and evolution in Gallotia lizards from the Canary Islands: age, growth, maturity and longevity , 1991 .

[67]  D. Newman,et al.  Skeletochronological data on the growth, age, and population structure of the tuatara, Sphenodon punctatus, on Stephens and Lady Alice islands, New Zealand , 1988 .

[68]  L. Zylberberg,et al.  The structure of the osteoderms in the Gekko: Tarentola mauritanica. , 1986, The American journal of anatomy.

[69]  J. Hutton Age determination of living nile crocodiles from the cortical stratification of bone , 1986 .

[70]  J. Castanet,et al.  New data on the structure and the growth of the osteoderms in the reptile Anguis fragilis L. (Anguidae, Squamata) , 1985, Journal of morphology.

[71]  M. Moss Comparative histology of dermal sclerifications in reptiles. , 1969, Acta anatomica.

[72]  R. Casamiquela Materiales adicionales y reinterpretación de Aetosauroides Scaglial. (De Ischigualasto, San Juan) , 1967 .

[73]  A. D. Walker Triassic reptiles from the elgin area: Stagonolepis, Dasygnathus and their allies , 1961, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[74]  R. Casamiquela SOBRE DOS NUEVOS ESTAGONOLEPOIDEOS ARGENTINOS , 1960 .