Hostname: page-component-5db58dd55d-htx7c Total loading time: 0 Render date: 2026-07-05T18:07:51.041Z Has data issue: false hasContentIssue false
  • English
  • Français

Ontogenetic stages in the long bone histology of sauropod dinosaurs

Published online by Cambridge University Press:  08 April 2016

Nicole Klein  and
Martin Sander
Nicole Klein
Affiliation:
Institut für Paläontologie, Universität Bonn, Nußallee 8, D-53115 Bonn, Germany. E-mail: nklein@uni-bonn.de, martin.sander@uni-bonn.de
Martin Sander
Affiliation:
Institut für Paläontologie, Universität Bonn, Nußallee 8, D-53115 Bonn, Germany. E-mail: nklein@uni-bonn.de, martin.sander@uni-bonn.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Long bones (femora, humeri) are the most abundant remains of sauropod dinosaurs. Their length is a good proxy for body length and body mass, and their histology is informative about ontogenetic age. Here we provide a comparative assessment of histologic changes in growth series of several sauropod taxa, including diplodocids (Apatosaurus, Diplodocus, indeterminate Diplodocinae from the Tendaguru Beds and from the Morrison Formation), basal macronarians (Camarasaurus, Brachiosaurus, Europasaurus), and titanosaurs (Phuwiangosaurus, Ampelosaurus). A total of 167 long bones, mainly humeri and femora, and 18 limb girdle bones were sampled. Sampling was performed by core drilling at prescribed locations at midshaft, and 13 histologic ontogenetic stages (HOS stages) were recognized. Because growth of all sauropod long bones is quite uniform, with laminar fibrolamellar bone being the dominant tissue, HOS stages could be recognized across taxa, although with minor differences. Histologic ontogenetic stages generally correlate closely with body size and thus provide a means to resolve important issue like the ontogenetic status of questionable specimens. We hypothesize that sexual maturity was attained at HOS-8, well before maximum size was attained, but we did not find sexually differentiated growth trajectories subsequent to HOS-8. On the basis of HOS stages, we detected two morphotypes in the Camarasaurus sample, a small one (type 1) and a larger one (type 2), presumably representing different species or sexual dimorphism.

Information

Type
Articles
Information
Paleobiology , Volume 34 , Issue 2 , Spring 2008 , pp. 247 - 263
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Literature Cited

Amprino, R. 1947. La structure du tissue osseux envisagée comme expression de differences dans la vitesse de l'accroissement. Archives de Biologie 58:315–330.Google Scholar
Ayer, J. 2000. The Howe Ranch dinosaurs. Sauriermuseum Aathal, Zürich.Google Scholar
Bonnan, M. F. 2004. Morphometric analysis of humerus and femur shape in Morrison sauropods: implications for functional morphology and paleobiology. Paleobiology 30:444–470.Google Scholar
Carpenter, K. 1999. Eggs, nests, and baby dinosaurs: a look at dinosaur reproduction. Indiana University Press, Bloomington.Google Scholar
Carpenter, K., and McIntosh, J. 1994. Upper Jurassic sauropod babies from the Morrison Formation. Pp. 372 in Carpenter, K., Hirsch, K., and Horner, J., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Chiappe, L. M., and Coria, S. L. 2001. Embryonic skulls of titanosaur sauropod dinosaurs. Science 293:2444–2446.Google Scholar
Chiappe, L. M., Jackson, F., Coria, R. A., and Dingus, L. 2005. Nesting titanosaurs from Auca Mahuevo and adjacent sites: understanding sauropod reproductive behaviour and embryonic development. Pp. 285–302 in Curry Rogers, K. and Wilson, J. A., eds. The sauropods: evolution and paleobiology. University of California Press, Berkeley.Google Scholar
Chinsamy, A. 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus (Owen). Modern Geology 18:319–329.Google Scholar
Chinsamy, A. 1994. Dinosaur bone histology: implications and inferences. Pp. 213–227 in Rosenberg, G. D. and Wolberg, D. L., eds. DinoFest. Paleontological Society Special Publication 7: 213–227.Google Scholar
Chinsamy-Turan, A. 2005. The microstructure of dinosaur bone. Johns Hopkins University Press, Baltimore.Google Scholar
Cormack, D. 1987. Ham's histology. Lippincott, New York.Google Scholar
Currey, J. D. 2002. Bones: structure and mechanics. Princeton University Press, Princeton, N.J. Google Scholar
Curry, K. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654–665.Google Scholar
Dunham, A. E., Overall, K. L., Porter, W. P., and Forster, C. A. 1989. Implications of ecological energetics and biophysical and developmental constraints for life-history variation in dinosaurs. In Farlow, J. O., ed. Paleobiology of the dinosaurs. Geological Society of America Special Paper 238:1–21.Google Scholar
Erickson, G. M. 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20:677–684.Google Scholar
Erickson, G. M., and Tumanova, T. A. 2000. Growth curve of Psittacosaurus mongoliensis Osborn (Ceratopsia: Psittacosauridae) inferred from long bone histology. Zoological Journal of the Linnean Society 130:551–566.Google Scholar
Erickson, G. M., Currie, P. J., Inouye, B. D., and Winn, A. A. 2006. Tyrannosaur life tables: an example of nonavian dinosaur population biology. Science 313:213–217.Google Scholar
Erickson, G. M., Curry-Rogers, K., Varricchio, D. J., Norell, M. A., and Xu, X. 2007. Growth pattern in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letters 3:558–561.Google Scholar
Foster, J. R. 2005. New juvenile sauropod material from Western Colorado, and the record of juvenile sauropods from the Upper Jurassic Morrison Formation. Pp. 141–153 in Tidwell, and Carpenter, 2005.Google Scholar
Francillon-Vieillot, H., de Buffrenil, V., Castanet, J., Geraudie, J., Meunier, F. J., Sire, J. Y., Zylenberberg, L., and de Ricqlès, A. 1990. Microstructure and mineralization of vertebrate skeletal tissues. Pp. 471–530 in Carter, J. E., ed. Skeletal biomineralization: patterns, processes and evolutionary trends. Van Nostrand Reinhold, New York.Google Scholar
Gilmore, C. W. 1925. A nearly complete articulated skeleton of Camarasaurus, a saurischian from the Dinosaur National Monument, Utah. Memoirs of the Carnegie Museum 10:347–384.CrossRefGoogle Scholar
Horner, J. R., and Padian, K. 2004. Age and growth dynamics of Tyrannosaurus rex . Proceedings of the Royal Society of London B 27:1875–1880.Google Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 2000. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. Journal of Vertebrate Paleontology 20:115–129.Google Scholar
Horner, J. R., Padian, K., and de Ricqlès, A. 2001. Comparative osteohistology of some embryonic and perinatal archosaurs: developmental and behavioral implications for dinosaurs. Paleobiology 27:39–58.Google Scholar
Ikejiri, T., Tidwell, V., and Trexler, D. 2005. New adult specimens of Camarasaurus lentus highlight ontogenetic variation within the species. Pp. 154–179 in Tidwell, and Carpenter, 2005.Google Scholar
Janensch, W. 1961. Die Gliedmaßen und Gliedmaßengürtel der Sauropoden der Tendaguru-Schichten. Palaeontographica 3(Suppl. 7):177–235.Google Scholar
Jianu, C. M., and Weishampel, D. B. 1999. The smallest of the largest: a new look at possible dwarfing in sauropod dinosaurs. Geologie en Mijnbouw 78:335–343.Google Scholar
Klein, N., and Sander, P. M. 2006. An unusual bone histology and growth pattern in Ampelosaurus atacis, a titanosaurid sauropod from South France. Journal of Vertebrate Paleontology 26(Suppl. to No. 3):85A.Google Scholar
Klein, N., and Sander, P. M. 2007. Bone histology and growth of the prosauropod dinosaur Plateosaurus engelhardti (von Meyer 1837) from the Norian bonebeds of Trossingen (Germany) and Frick (Switzerland). Special Papers in Palaeontology 77:169–206.Google Scholar
Lee, A., and Werning, S. 2008. Sexual maturity in growing dinodaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences USA 105:582–587.CrossRefGoogle Scholar
Lehmann, T. M., and Coulson, A. B. 2002. A juvenile specimen of the sauropod dinosaur Alamosaurus sanjuanensis from the Upper Cretaceous of Big Bend National Park, Texas. Journal of Paleontology 76:156–172.Google Scholar
Le Loeuff, J. 2005a. Osteology of Ampelosaurus atacis (Titanosauria) from Southern France. Pp. 115–137 in Tidwell, and Carpenter, 2005.Google Scholar
Le Loeuff, J. 2005b. Romanian Late Cretaceous dinosaurs: big dwarfs or small giants? Historical Biology 17:15–17.Google Scholar
Martin, V. 1994. Baby sauropods from the Sao Khua Formation (Lower Cretaceous) in Northeastern Thailand. Gaia 10:147–153.Google Scholar
Mazzetta, G. V., Christiansen, P., and Farin, R. A. 2004. Giants and bizarres: body size of some southern South American Cretaceous dinosaurs. Historical Biology 2004:1–13.Google Scholar
McIntosh, J. 1990. Species determination in sauropod dinosaurs with tentative suggestions for their classification. Pp. 53–69 in Carpenter, K. and Currie, P., eds. Dinosaur systematics: perspectives and approaches. Cambridge University Press, Cambridge.Google Scholar
Reisz, R. R., Scott, D., Sues, H.-D., Evans, D. C., and Raath, M. A. 2005. Embryos of an Early Jurassic prosauropod dinosaur and their evolutionary significance. Science 309:761–764.Google Scholar
Remes, K. 2006. Revision of the Tendaguru sauropod dinosaur Tornieria africana Fraas and its relevance for sauropod paleobiogeography. Journal of Vertebrate Paleontology 26:651–669.Google Scholar
Remes, K. 2007. A second Gondwana diplodocid dinosaur from the Upper Jurassic Tendaguru Beds of Tanzania, East Africa. Palaeontology 50:653–667.Google Scholar
Sander, P. M. 1999. Life history of Tendaguru sauropods as inferred from long bone histology. Mitteilungen Museum für Naturkunde Berlin, Geowissenschaftliche Reihe 2:103–112.Google Scholar
Sander, P. M. 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466–488.2.0.CO;2>CrossRefGoogle Scholar
Sander, P. M., and Klein, N. 2005. Unexpected developmental plasticity in the life history of an early dinosaur. Science 310:1800–1802.Google Scholar
Sander, P. M., and Tückmantel, C. 2003. Bone lamina thickness, bone apposition rates, and age estimates in sauropod humeri and femora. Paläontologische Zeitschrift 77:161–172.Google Scholar
Sander, P. M., Klein, N., Buffetaut, E., Cuny, G., Suteethorn, V., 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
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.Google Scholar
Sander, P. M., Jackson, F., and Chiappe, L. M. In press. Upper Cretaceous titanosaur nesting sites and their implications for sauropod dinosaur reproductive biology. Palaeontographica, Abteilung A.Google Scholar
Schwarz, D., Ikejiri, T., Breithaupt, B. H., Sander, P. M., and Klein, N. 2007. A nearly complete skeleton of an early juvenile diplodocid (Dinosauria: Sauropoda) from the Lower Morrison Formation (Late Jurassic) of North Central Wyoming and its implications for early ontogeny and pneumaticity in sauropods. Historical Biology 19:225–253.Google Scholar
Schweitzer, M. H., Wittmeyer, J. L., and Horner, J. R. 2005. Gender-specific reproductive tissue in ratites and Tyrannosaurus rex . Nature 308:1456–1460.Google Scholar
Seebacher, F. 2001. A new method to calculate allometric length-mass relationships of dinosaurs. Journal of Vertebrate Paleontology 21:51–60.Google Scholar
Tidwell, V., and Carpenter, K., eds. 2005. Thunder-lizards. Indiana University Press, Bloomington.Google Scholar
Tidwell, V., and Wilhite, R. 2005. Ontogenetic variation and isometric growth in the forelimb of the Early Cretaceous sauropod Venenosaurus. Pp. 187–196 in Tidwell, and Carpenter, 2005.Google Scholar
Varricchio, D. J. 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus . Journal of Vertebrate Paleontology 13:99–104.Google Scholar
Wilhite, R. 2003. Biomechanical reconstruction of the appendicular skeleton in three North American Jurassic sauropods. Ph.D. dissertation. Louisiana State University, Baton Rouge.Google Scholar
Wilson, J. A. 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zoological Journal of the Linnean Society of London 136:217–276.Google Scholar
Xu, X., Tan, Q., Wang, J., Zhao, X. and Tan, L. 2007. A gigantic bird-like dinosaur from the Late Cretaceous of China. Nature 447: 884–847.Google Scholar
Supplementary material: PDF

Klein and Sander supplementary material

Appendix

Download Klein and Sander supplementary material(PDF)
PDF 148.7 KB