Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation X-ray microtomography

LITERATURE CITED

• Abramoff , M. D. , Magelhaes , P. J. and Ram , S. J. 2004 . Image Processing with Image. J . Biophotonics International , 11 : 36 – 42 .
   Google Scholar
• Agenbroad , L. D. 2001 . “ Channel Islands (USA) pygmy mammoths (Mammuthus exilis) compared and contrasted with M. columbi, their continental ancestral stock ” . In The World of Elephants: Proceedings of the 1st International Congress , Edited by: Cavaretta , G. , Gioia , P. M. , Muss , M. and Palombo , M. R. 473 – 475 . Rome , , Italy : Consiglio Nazionale delle Ricerche . , Rome, Italy, 16–20 October 2001.
   Google Scholar
• Amprino , R. 1947 . La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement . Archives de Biologie , 58 : 315 – 330 .
   Google Scholar
• Benedict , F. G. and Lee , R. C. 1936 . Studies on the body temperatures of elephants . Proceedings of the National Academy of Sciences of the United States of America , 22 : 405 – 408 .
   PubMedGoogle Scholar
• Boin , M. and Haibel , A. 2006 . Compensation of ring artifacts in synchrotron tomographic images . Optics Express , 14 : 12071 – 12075 .
   PubMed Web of Science ®Google Scholar
• Brouwer , E. 1952 . Over beenstructure en voedingbij mens en dier . Voeding , 13 : 55 – 65 .
   Google Scholar
• Blumenbach , J. H. 1797 . Handbuch der Naturgeschicte, , 5th edition Edited by: Dieterich , J. H. 714 Göttingen , , Germany
   Google Scholar
• Botha , J. and Chinsamy , A. 2000 . Growth patterns deduced from the bone histology of the cynodonts Diademodon and Cynognathus . Journal of Vertebrate Paleontology , 20 : 705 – 711 .
   Web of Science ®Google Scholar
• Buss , I. O. and Wallner , A. 1965 . Body temperature of the African elephant . Journal of Mammalogy , 46 : 104 – 107 .
   Google Scholar
• Caloi , L. , Kotsakis , T. , Palombo , M. R. and Petronio , C. 1996 . “ The Pleistocene dwarf elephants of Mediterranean islands ” . In The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives , Edited by: Shoshani , J. and Tassy , P. 234 – 239 . Oxford , , U.K : Oxford University Press .
   Google Scholar
• Castanet , J. , Curry-Rogers , K. , Cubo , J. and Boisard , J. J. 2000 . Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs . Comptes Rendus de l’Academie des Sciences. Serie III, Sciences de la Vie (Paris) , 323 : 543 – 550 .
   PubMed Web of Science ®Google Scholar
• Castanet , J. , Francillon-Vieillot , F. , Meunier , F. J. and De Ricqlès , A. 1993 . “ Bone and individual aging ” . In Bone, Volume 7. Bone Growth. B , Edited by: Hall , B. K. 245 – 283 . Boca Raton , Florida : CRC Press .
   Google Scholar
• Chinsamy , A. and Hurum , J. H. 2006 . Bone microstructure and growth patterns of early mammals . Acta Palaeontologica Polonica , 51 : 325 – 338 .
   Web of Science ®Google Scholar
• Cook , S. F. , Brooks , S. T. and Ezra-Cohn , H. E. 1962 . Histological studies on fossil bone . Journal of Paleontology , 36 : 81 – 85 .
   Web of Science ®Google Scholar
• Cormack , D. 2001 . Essential Histology , 345 Philadelphia , Pennsylvania : Lippincott, Williams and Wilkins .
   Google Scholar
• Cubo , G. , Legendre , P. , de Ricqlès , A. , Montes , L. , de Margerie , E. , Castanet , J. and Desdevises , Y. 2008 . Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes . Evolution and Development , 10 : 217 – 227 .
   PubMed Web of Science ®Google Scholar
• Currey , J. D. 1960 . Differences in the blood-supply of bone of different histological types . Quarterly Journal of Microscopical Science , 101 : 51 – 370 .
   Google Scholar
• Currey , J. D. 2002 . Bones: Structure and Mechanics , 436 Princeton , New Jersey : Princeton University Press .
   Google Scholar
• Curtin , A. J. , le , P. , Mouton , F. N. and Chinsamy , A. 2005 . Bone growth patterns in two cordylid lizards, Cordylus cataphractus and Pseudocordylus capensis . African Zoology , 40 : 1 – 7 .
   Web of Science ®Google Scholar
• Curtin , A. J. , Zug , G. R. and Spotila , J. R. 2009 . Longevity and growth strategies of the desert tortoise (Gopherus agassizii) in two American deserts . Journal of Arid Environments , 73 : 463 – 471 .
   Web of Science ®Google Scholar
• De Margerie , E. , Cubo , J. and Castanet , J. 2002 . Bone typology and growth rate: testing and quantifying “Amprino's rule” in the mallard (Anas platyrhyncos) . Comptes Rendus Biologies , 325 : 221 – 230 .
   PubMed Web of Science ®Google Scholar
• De Margerie , E. , Robin , J.-P. , Verrier , D. , Cubo , J. , Groscolas , R. and Castanet , J. 2004 . Assessing a relationship between bone microstructure and growth rate: a fluorescent labeling study in the king penguin chick (Aptenodytes patagonicus) . Journal of Experimental Biology , 207 : 869 – 879 .
   PubMed Web of Science ®Google Scholar
• De Ricqlès , A. 1973 . Recherches paléohistologiques sur les os longs de tétrapodes. Ph.D. dissertation , 138 Paris , , France : Université Paris VII .
   Google Scholar
• De Ricqlès , A. , Meunier , F. J. , Castanet , J. and Francillon-Vieillot , H. 1991 . “ Comparative microstructure of bone ” . In Bone , Edited by: Hall , B. K. Vol. 3 , 1 – 78 . Boca Raton , Florida : CRC Press . . Bone Matrix and Bone Specific Products.
   Google Scholar
• Enlow , D. H. 1963 . Principles of Bone Remodeling an Account of Post-natal Growth and Remodeling Processes in Long Bones and the Mandible , 131 Springfield , Illinois : Charles C Thomas .
   Google Scholar
• Enlow , D. H. and Brown , S. O. 1956 . A comparative histology study of fossil and recent bone tissue. Part I . Texas Journal of Science , 8 : 405 – 443 .
   Google Scholar
• Enlow , D. H. and Brown , S. O. 1957 . A comparative histology study of fossil and recent bone tissue. Part II . Texas Journal of Science , 9 : 186 – 214 .
   Google Scholar
• Enlow , D. H. and Brown , S. O. 1958 . A comparative histology study of fossil and recent bone tissue. Part III . Texas Journal of Science , 10 : 187 – 230 .
   Google Scholar
• Erickson , G. 2005 . Assessing dinosaur growth patterns: a microscopic revolution . Trends in Ecology and Evolution , 20 : 677 – 684 .
   PubMed Web of Science ®Google Scholar
• Ezra , H. C. and Cook , S. F. 1959 . Histology of mammoth bone . Science , 129 : 465 – 466 .
   PubMed Web of Science ®Google Scholar
• Falconer , H. 1857 . On the species of mastodon and elephant occurring in the fossil state in Great Britain . Quarterly Journal of the Geological Society of London , 13 : 307 – 360 .
   Google Scholar
• Francillon-Vieillot , H. , de Buffrénil , V. , Castanet , J. , Géraudie , J. , Meunier , F. J. , Sire , J. Y. , Zylberberg , L. and de Ricqlès , A. 1990 . “ Microstructure and mineralization of vertebrate skeletal tissues; pp ” . In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends , Edited by: Carter , J. G. Vol. 1 , 471 – 530 . New York , New York : Van Nostrand Reinhold .
   Google Scholar
• Freeman , W. H. and Bracegirdle , B. 1976 . An Advanced Atlas of Histology , 159 London , , U.K : Heinemann Educational Books .
   Google Scholar
• Halstead , L. B. 1974 . Vertebrate Hard Tissues , London , , U.K. : Wykeham .
   Google Scholar
• Horner , J. R. and Padian , K. 2004 . Age and growth dynamics of Tyrannosaurus rex . Proceedings of the Royal Society of London B , 271 : 1875 – 1880 .
   Web of Science ®Google Scholar
• Horner , J. R. , Padian , K. and de Ricqlès , A. J. 2001 . Comparative osteohistology of some embryonic and perinatal archosaurs: phylogenetic and behavioral implications for dinosaurs . Paleobiology , 27 : 39 – 58 .
   Web of Science ®Google Scholar
• Houssaye , A. , Mazurier , A. , Herrel , A. , Volpato , V. , Tafforeau , P. , Boistel , R. and de Buffrénil , V. 2010 . Vertebral microanatomy in squamates: structure, growth and ecological correlates . Journal of Anatomy , 217 : 715 – 727 .
   PubMed Web of Science ®Google Scholar
• Kinney , J. H. and Nichols , M. C. 1992 . X-ray tomographic microscopy using synchrotron radiation . Annual Review of Materials Science , 22 : 121 – 152 .
   Google Scholar
• Klein , N. and Sander , M. 2008 . Ontogenetic stages in the long bone histology of sauropod dinosaurs . Paleobiology , 34 : 247 – 263 .
   Web of Science ®Google Scholar
• Linnaeus , C. 1758 . Systema naturae per regina tria naturae, secundum classis, ordines, genera, species cum characteribus, differentus, synonymis, locis (tenth edition, reformata) , 824 Stockholm , , Sweden : Laurentii Slavii .
   Google Scholar
• Locke , M. 2004 . Structure of long bones in mammals . Journal of Morphology , 262 : 546 – 565 .
   PubMed Web of Science ®Google Scholar
• Lomolino , M. V. 1985 . Body size of mammals on islands: the island rule re-examined . American Naturalist , 125 : 310 – 316 .
   Web of Science ®Google Scholar
• Mazurier , A. , Volpato , V. and Macchiarelli , R. 2006 . Improved noninvasive microstructural analysis of fossil tissues by means of SR-microtomography . Applied Physics A , 83 : 229 – 233 .
   Web of Science ®Google Scholar
• Mori , R. , Kodaka , T. and Naito , Y. 1999 . Delayed osteon formation in long-bone diaphysis of a 11-year-old giant cow with dermal dysplasia . Journal of Veterinary Medical Science , 61 : 101 – 106 .
   PubMed Web of Science ®Google Scholar
• Mori , R. , Kodaka , T. , Sano , T. , Yamagishi , N. , Asari , A. and Naito , Y. 2003 . Comparative histology of the laminar bone between young calves and foals . Cells Tissues Organs , 175 : 43 – 50 .
   PubMed Web of Science ®Google Scholar
• Mori , R. , Kodaka , T. , Soeta , S. , Sato , J. , Kakino , J. , Hamato , S. , Takaki , H. and Naito , Y. 2005 . Preliminary study of histological comparison on the growth patterns of long-bone cortex in young calf, pig and sheep . Journal of Veterinary Medical Science , 67 : 1223 – 1229 .
   PubMed Web of Science ®Google Scholar
• Nowak , R. M. 1991 . Walker's Mammals of the World, , fifth edition , 1629 Baltimore , Maryland : Johns Hopkins University Press .
   Google Scholar
• Palombo , M. 2007 . How can endemic proboscideans help us understand the “island rule”? A case study of Mediterranean islands . Quaternary International , 169–170 : 105 – 124 .
   Web of Science ®Google Scholar
• Raia , P. and Meiri , S. 2006 . The island rule in large mammals: paleontology meets ecology . Evolution , 60 : 1731 – 1742 .
   PubMed Web of Science ®Google Scholar
• Raia , P. , Barbera , C. and Conte , M. 2003 . The fast life of a dwarfed giant . Evolutionary Ecology , 17 : 293 – 312 .
   Web of Science ®Google Scholar
• Ray , S. , Botha , J. and Chinsamy , A. 2004 . Bone histology and growth patterns of some non-mammalian therapsids . Journal of Vertebrate Paleontology , 24 : 634 – 648 .
   Web of Science ®Google Scholar
• Reid , R. E. H. 1997 . Bone and dinosaurian “endothermy” . Modern Geology , 11 : 133 – 154 .
   Google Scholar
• Roth , V. L. 1982 . Dwarf mammoths from the Santa Barbara, California Channel Islands: size, shape, development and evolution. Ph.D. dissertation , 277 New Haven , Connecticut : Yale University .
   Google Scholar
• Roth , V. L. 1984 . How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species . Journal of Vertebrate Paleontology , 4 : 126 – 145 .
   Google Scholar
• Roth , V. L. 1989 . Fabricational noise in elephant dentitions . Paleobiology , 15 : 165 – 179 .
   Web of Science ®Google Scholar
• Roth , V. L. 1992 . Inferences from allometry and fossils: dwarfing of elephants on islands . Oxford Surveys in Evolutionary Biology , 8 : 259 – 288 .
   Google Scholar
• Roth , V. L. 2001 . “ Ecology and evolution of dwarfing in insular elephants; pp ” . In The World of Elephants: Proceedings of the 1st International Congress , Edited by: Cavarretta , G. , Gioia , P. , Mussi , M. and Palombo , M. 507 – 509 . Rome , , Italy : Consiglio Nazionale delle Ricerche .
   Google Scholar
• Rowe , T. , Kappelman , J. , Carlson , W. D. , Ketcham , R. A. and Denison , C. 1997 . High-resolution computed tomography: a breakthrough technology for Earth scientists . Geotimes , 42 : 23 – 27 .
   Google Scholar
• Rühli , F. J. , Kuhn , G. , Evison , R. , Müller , R. and Schultz , M. 2007 . Diagnostic value of micro-CT in comparison with histology in the qualitative assessment of historical human skull bone pathologies . American Journal of Physical Anthropology , 133 : 1099 – 1111 .
   PubMed Web of Science ®Google Scholar
• Sanchez , S. , Germain , D. , de Ricqlés , A. , Abourachid , A. , Goussard , F. and Tafforeau , P. 2010 . Limb-bone histology of temnospondyls: implications for understanding the diversification of palaeoecologies and patterns of locomotion of Permo-Triassic tetrapods . Journal of Evolutionary Biology , 23 : 2076 – 2090 .
   PubMed Web of Science ®Google Scholar
• Sander , P. M. 2000 . Longbone histology of the Tendaguru sauropods: implications for growth and biology . Paleobiology , 26 : 466 – 488 .
   Web of Science ®Google Scholar
• Sander , P. M. and Andrássy , P. 2006 . Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? . Palaeontolographica Abteilung A , 277 : 143 – 159 .
   Web of Science ®Google Scholar
• Sander , P. M. , Mateus , O. , Laven , T. and Knötschke , N. 2006 . Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur . Nature , 441 : 739 – 741 .
   PubMed Web of Science ®Google Scholar
• Sander , P. M. , Klein , N. , Buffetaut , E. , Cuny , G. , Suteethorn , V. and Le Loeuff , J. 2004 . Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration . Organisms, Diversity and Evolution , 4 : 165 – 173 .
   Google Scholar
• Starck , J. M. and Chinsamy , A. 2002 . Bone microstructure and developmental plasticity in birds and other dinosaurs . Journal of Morphology , 254 : 232 – 246 .
   PubMed Web of Science ®Google Scholar
• Stock , C. and Furlong , E. L. 1928 . The Pleistocene elephants of Santa Rosa Island, California . Science, new series , 68 ( 1754 ) : 140 – 141 .
   PubMedGoogle Scholar
• Stover , S. , Pool , R. , Martin , R. and Morgan , J. 1992 . Histological features of the dorsal cortex of the third metacarpal bone middiaphysis during post-natal growth in thoroughbred horses . Journal of Anatomy , 181 : 455 – 469 .
   PubMed Web of Science ®Google Scholar
• Tafforeau , P. , Boistel , R. , Boller , E. , Bravin , A. , Brunet , M. , Chaimanee , Y. , Cloetens , P. , Feist , M. , Hoszowska , J. , Jaeger , J.-J. , Kay , R. F. , Lazzari , V. , Marivaux , L. , Nel , A , Nemoz , C. , Thibault , X. , Vignaud , P. and Zabler , S. 2006 . Some applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens . Applied Physics A , 83 : 195 – 202 .
   Web of Science ®Google Scholar
• Van den Bergh , G. , Sondaar , P. Y. , De Vos , J. and Aziz , F. 1996 . “ The proboscideans of South-East Asian islands ” . In The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives , Edited by: Shoshani , J. and Tassy , P. 240 – 248 . Oxford , , U.K : Oxford University Press .
   Google Scholar
• Vlassenbroeck , J. , Dierick , M. , Masschaele , B. , Cnudde , V. , Hoorebeke , L. and Jacobs , P. 2007 . Software tools for quantification of X-ray microtomography . Nuclear Instruments and Methods in Physics Research Section A , 580 : 442 – 445 .
   Web of Science ®Google Scholar
• Zar , J. H. 1996 . Biostatistical Analysis, , third edition , 662 Upper Saddle River , New Jersey : Prentice Hall .
   Google Scholar