Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Fine structure of bone in dinosaurs, birds and mammals

Abstract

After observation of detailed structural evidence for the origin of birds from dinosaurs1, and in light of evidence that dinosaur bone tissue resembles the histology in mammals2, the histology of bone has become one of the focal points in discussions of the physiology of dinosaurs and Mesozoic birds3,4,5,6,7,8,9,10. Most of this microstructural information has focused on features related to the vascular organization and the amount of remodelled bone around vascular canals. However, the finer structures have received less attention, although differences in such structures have been observed among modern vertebrates10,11. Here we present evidence that canaliculi—the submicrometre-sized channels that interconnect bone cells and vascular canals—and the collagen fibre bundles in bone are differently organized among certain dinosaur lineages. Ornithomimid dinosaurs12 are more like birds than mammals in these features. In canalicular structure, and to some extent in fibre bundle arrangement, ornithischian dinosaurs are more like mammals. These differences in both canalicular and lamellar structure are probably linked to differences in the process and rate13 of bone formation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Relationships of certain dinosaur taxa.
Figure 2: Canalicular organization in transverse thin sections of various bone types.
Figure 3: Percentage frequency distributions of canalicular directions in samples of birds, ornithomimids, mammals and ornithischians.
Figure 4: Lamellar organization as seen with crossed polars in transverse thin sections of various bones.
Figure 5: Degree of variability of lamellar thicknesses in samples of mammals, birds, coelurosaurs and lizard.

Similar content being viewed by others

References

  1. Ostrom, J. H. The ancestry of birds. Nature 242, 136 (1973).

    Article  ADS  Google Scholar 

  2. Enlow, D. H. & Brown, S. O. A comparative histological study of fossil and recent bone tissue. Part II. Tex. J. Sci. 9, 186–214 (1957).

    Google Scholar 

  3. Currey, J. D. The histology of the bone of a prosauropod dinosaur. Palaeontology 5, 238–246 ( 1962).

    Google Scholar 

  4. Bakker, R. T. Anatomical and ecological evidence of endothermy in dinosaurs. Nature 281, 81–85 ( 1972).

    Article  ADS  Google Scholar 

  5. de Ricqlès, A. in A Cold Look at the Warm-Blooded Dinosaurs (eds Thomas, R. D. K. & Olson, E. C.) Ser. 28, 103–139 (Amer. Assoc. Adv. Sci. Selected Symp., Westview Press, Boulder, 1980).

    Google Scholar 

  6. Reid, R. E. H. The histology of dinosaurian bone, and its possible bearing on dinosaurian physiology. Symp. Zool. Soc. Lond. 52, 629 –663 (1984).

    Google Scholar 

  7. Reid, R. E. H. On supposed Haversian bone from the hadrosaur Anatosaurus, and the nature of compact bone in dinosaurs. J. Paleont. 59 , 140–148 (1985).

    Google Scholar 

  8. Chinsamy, A. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeont. Afr. 27, 77–82 (1990).

    Google Scholar 

  9. Varricchio, D. J. Bone microstructure of the upper Cretaceous theropod dinosaur Troodon formosus. J. Vert. Paleont. 13, 99–104 (1993).

    Article  Google Scholar 

  10. Gebhardt, W. Über funktionell wichtige Anordnungsweisen der feineren und gröberen Bauelemente des Wirbeltierknochens. II. Spezieller Teil. 1. Der Bau der Haversshen Lamellensysteme und seine funktionelle Bedeutung. W. Roux Archiv für Entwicklungsmechanic der Organismen 20, 187 –334 (1906).

    Article  Google Scholar 

  11. Amprino, R. & Godina, G. La struttura della ossa nei vertebrate. Ricerche comparative negli amfibi e negli amnioti. Commentat. Pontif. Acad. Scient. 11, 329–463 (1947).

    Google Scholar 

  12. Sereno, P. C. The evolution of dinosaurs. Science 284, 2137–2147 (1999).

    Article  CAS  Google Scholar 

  13. de Ricqlès, A., Meunier, F. J., Castanet, J. & Francillon-Vieillot, H. in Bone 3, Bone Matrix and Bone Specific Products (ed. Hall, B. K.) 1–78 (CRC, Boca Raton, Florida, 1991).

    Google Scholar 

  14. Curtis, T. A., Ashrafi, S. H. & Weber, D. F. Canalicular communication in the cortices of human long bones. Anat. Rec. 212, 336– 344 (1985).

    Article  CAS  Google Scholar 

  15. Pawlcki, R. Metabolic pathways of the fossil dinosaur bones Part III. Intermediary and other osteocytes in the systems of metabolic pathways of dinosaur bone. Folia Histochem. Cytobiol. 22, 91– 98 (1984).

    Google Scholar 

  16. Gauthier, J. in The Origin of Birds and the Evolution of Flight (ed. K. Padian). Mem. Calif. Acad. Sci. 8, 1–55 (1986).

    Google Scholar 

  17. Holtz, T. R. The phyletic position of the Tyrannosauridae: implications for theropod systematics. J. Paleont. 68, 1100– 1117 (1994).

    Article  Google Scholar 

  18. de Ricqlès, A. Recherches paléohistologiques sur les os longs de Tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissues osseux des Tétrapodes. Partie 1. Ann. Paléont. (Vertebres) 61, 51–129 ( 1975).

    Google Scholar 

  19. Pawlcki, R., Korbel, A. & Kubiak, H. Cells, collagen fibrils and vessels in dinosaur bone. Nature 211, 655–657 (1966).

    Article  ADS  Google Scholar 

  20. Rimblot-Baly, F., de Ricqlès, A. & Zylberberg, L. Analyse paléohistologique d'une série de croissance partielle chez Lapparentosaurus madagascariensis (Jurassique moyen): essai sur la dynamique de croissance d'un dinosaure sauropode. Ann. Paléont. (Invert. - Vert.) 81 , 49–86 (1995).

    Google Scholar 

  21. Amprino, R. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Arch. Biologie 58, 315–330 (1947).

    Google Scholar 

  22. Giraud-Guille, M. M. Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif. Tissue Int. 42, 167– 180 (1988).

    Article  CAS  Google Scholar 

  23. McMahon, J. M., Boyde, A. & Bromage, T. G. Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain. Anat. Rec. 242, 147–158 (1995).

    Article  CAS  Google Scholar 

  24. Raspanti, M., Guizzardi, S., Strocchi, R. & Ruggeri, A. Collagen fibril patterns in compact bone: preliminary ultrastructural observations. Acta Anat. 155, 249–256 (1996).

    Article  CAS  Google Scholar 

  25. Castanet, J., Grandin, A., Abourachid, A. & de Ricqlès, A. Expression de la dynamique de croissance dans la structure de l'os périostique chez Anas platyrhynchos. C. R. Acad. Sci. Paris 319, 301–308 (1996).

    CAS  PubMed  Google Scholar 

  26. Boyde, A. in The Biochemistry and Physiology of Bone (ed. Bourne, G.) 259– 310 (Academic, New York & London, 1972).

    Book  Google Scholar 

  27. Currey, J. D. The Mechanical Adaptations of Bones (Princeton Univ. Press, Englewood Cliffs, New Jersey, 1984).

    Book  Google Scholar 

  28. Martin, R. B. & Burr, D. B. Structure, Function, and Adaptation of Compact Bone Fig. 2. 4. (Raven, New York, 1989).

    Google Scholar 

  29. Crawford, G. N. C. The evolution of the Haversian pattern in bone. J. Anatomy 74, 284–299 (1940).

    CAS  Google Scholar 

  30. Xu, X., Tang, Z. -L. & Wang, Z.-L. A therizinosauroid dinosaur with integumentary structures from China. Nature 399, 350– 354 (1999).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Ostrom for identifying two ornithomimid specimens; S. Herring, A. de Ricqlés, M. Smith and N. Wolf for assistance with the manuscript; and B. Evans, S. McCallum, D. McDougall, S. Ott-Ralph and D. Sherrard for helpful discussion. A. Busbey, P. Currie, G. Erickson, J. Joslin, A. Kemp, O. Rieflin, S. Rohwer, H.-D. Sues, C. Wood and the Woodland Park Zoo kindly made specimens available. B. Witte collected and prepared dinosaur specimens; S. Andres, D. Bennett, G. Bergsma, V. Carr, C. Chihara, J. Cyrus, M. Dyakanoff, J. Haag, H. Heller, M. Hoffman, N. Huston, D. Jacobson, K. Jensen, J. Johnston, J. Kim, K. Krigbaum, T. Lee, B. Leu, M. Mielkey, B. Moorthy, J. Morton, E. Moye, H. Mull, J. Nguyen, B. Olsen, C. Pardo, L. Rende, O. Rieflin, L. Ruhwedel, T. Schommer, M. Shields, A. Smith, B. Summers, T. Ting, H. Wada, J. Weber and H. Witt ground thin sections or helped in other aspects of the study. We are grateful to the Burke Museum, the Hayashibara Museum, the University of Washington College of Arts and Sciences, and Departments of Geological Sciences and Orthodontics for support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John M. Rensberger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rensberger, J., Watabe, M. Fine structure of bone in dinosaurs, birds and mammals. Nature 406, 619–622 (2000). https://doi.org/10.1038/35020550

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35020550

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing