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Comparative osteohistology of some embryonic and perinatal archosaurs: developmental and behavioral implications for dinosaurs

Published online by Cambridge University Press:  08 February 2016

John R. Horner
Affiliation:
Museum of the Rockies, Montana State University, Bozeman, Montana 59717-0040. E-mail: [email protected]
Kevin Padian
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720-3140
Armand de Ricqlès
Affiliation:
Équipe Formations Squelettiques, URA CNRS 11 37, Université Paris VII, 75251 Paris cedex 05, France Collège de France, Paris, France

Abstract

Histologic studies of embryonic and perinatal longbones of living birds, non-avian dinosaurs, and other reptiles show a strong phylogenetic signal in the distribution of tissues and patterns of vascularization in both the shafts and the bone ends. The embryonic bones of basal archosaurs and other reptiles have thin-walled cortices and large marrow cavities that are sometimes subdivided by erosion rooms in early stages of growth. The cortices of basal reptiles are poorly vascularized, and osteocyte lacunae are common but randomly organized. Additionally, there is no evidence of fibrolamellar tissue organization around the vascular spaces. Compared with turtles, basal archosaurs show an increase in vascularization, better organized osteocytes, and some fibrolamellar tissue organization. In dinosaurs, including birds, vascularization is greater than in basal archosaurs, as is cortical thickness, and the osteocyte lacunae are more abundant and less randomly organized. Fibrolamellar tissues are evident around vascular canals and form organized primary osteons in older perinates and juveniles.

Metaphyseal (“epiphyseal”) morphology varies with the acquisition of new features in derived groups. The cartilage cone, persistent through the Reptilia (crown-group reptiles, including birds), is completely calcified in ornithischian dinosaurs before it is eroded by marrow processes; cartilage canals, absent in basal archosaurs, are present in Dinosauria; a thickened calcified hypertrophy zone in Dinosauria indicates an acceleration of longitudinal bone growth.

Variations in this set of histological synapomorphies overlap between birds and non-avian dinosaurs. In birds, these variations are strongly correlated with life-history strategies. This overlap, plus independent evidence from nesting sites, reinforces the hypothesis that variations in bone growth strategies in Mesozoic dinosaurs reflect different life-history strategies, including nesting behavior of neonates and parental care.

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Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Barreto, C. 1997. Dinosaur growth plates and dinosaur bone growth. Pp. 95100in Wolberg, D. L., Stump, E., and Rosenberg, G. D., eds. DINOfest International. Academy of Natural Sciences, Philadelphia.Google Scholar
Barreto, C., and Wilsman, N. J. 1994. Hypertrophic chondrocyte volume and growth rates in avian growth plates. Research in Veterinary Science 56:5361.CrossRefGoogle ScholarPubMed
Barreto, C., Albrecht, R. M., Bjorling, D. E., Horner, J. R., and Wilsman, N. J. 1993. Evidence of the growth plate and the growth of long bones in juvenile dinosaurs. Science 262:20202023.CrossRefGoogle ScholarPubMed
Breur, G. J., Vanenkevort, B. A., Farnum, C. E., and Wilsman, N. J. 1991. Linear relationship between the volume of hypertrophic chondrocytes and the rate of longitudinal bone growth in growth plates. Journal of Orthopedic Research 9:348359.CrossRefGoogle ScholarPubMed
Caplan, A. I., and Boyan, B. D. 1994. Endochondral bone formation: the lineage cascade. Pp. 146in Hall, B. K., ed. Bone, Vol. 8. Mechanisms of bone development and growth. CRC Press, Boca Raton, Fla.Google Scholar
Carter, D. R., Mikic, B., and Padian, K. 1998. Epigenetic mechanical factors in the evolution of long bone epiphyses. Zoological Journal of the Linnean Society 123:163178.CrossRefGoogle Scholar
Castanet, J., Grandin, A., Abourachid, A., and de Ricqlès, A. 1996. Expression de la dynamique de croissance dans la structure de l'os périostique chez Anas platyrhynchos. Comptes Rendus de l'Academie de Sciences, Sciences de la Vie 319:301308.Google Scholar
Chinsamy, A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontologia Africana 27:7782.Google Scholar
Chinsamy, A. 1993a. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geology 18:319329.Google Scholar
Chinsamy, A. 1993b. Image analysis and the physiological implications of the vascularization of femora in archosaurs. Modern Geology 19:101108.Google Scholar
Chinsamy, A. 1995. Ontogenetic changes in the bone histology of the Late Jurassic ornithopod Dryosaurus lettowvorbecki. Journal of Vertebrate Paleontology 15:96104.CrossRefGoogle Scholar
Currie, P. J., and Padian, K. 1977. Encyclopedia of dinosaurs. Academic Press, San Diego.Google Scholar
Curry, K. A. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654665.CrossRefGoogle Scholar
Dong, Z.-M., and Currie, P. J. 1996. On the discovery of an oviraptorid skeleton on a nest of eggs at Bayan Mandahu, Inner Mongolia, People's Republic of China. Canadian Journal of Earth Sciences 33:631636.CrossRefGoogle Scholar
Enlow, D. H. 1962. A study of the post-natal growth and remodeling of bone. American Journal of Anatomy 110:79101.CrossRefGoogle ScholarPubMed
Enlow, D. H. 1963. Principles of bone remodeling. Charles C. Thomas, Springfield, III.Google Scholar
Enlow, D. H., and Brown, S. O. 1956. A comparative histological study of fossil and Recent bone tissues, Part I. Texas Journal of Science 8:405443.Google Scholar
Enlow, D. H., and Brown, S. O. 1957. A comparative histological study of fossil and Recent bone tissues, Part II. Texas Journal of Science 9:186214.Google Scholar
Eurell, J., and Sterchi, D. 1994. Microwavable Toludine blue stain for surface staining of undecalcified bone sections. Journal of Histotechnology 17:357359.CrossRefGoogle Scholar
Fell, H. B. 1925. The histogenesis of cartilage and bone in the long bones of the embryonic fowl. Journal of Morphology and Physiology 40:417459.CrossRefGoogle 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. 471548in Carter, J. G., ed. Skeletal biomineralization: patterns, processes and evolutionary trends, Vol. 1. Van Nostrand Reinhold, New York.Google Scholar
Fyfe, F. W. 1964. Predominance of epiphyseal over metaphyseal blood supply in nourishment of epiphyseal cartilage, demonstrated by 35S radioautography and vascular ablation. Journal of Anatomy 98:471472.Google Scholar
Geist, N. R., and Jones, T. D. 1996. Juvenile skeletal structure and the reproductive habits of dinosaurs. Science 272:712714.CrossRefGoogle ScholarPubMed
Haines, R. W. 1933. Cartilage canals. Journal of Anatomy 68:4564.Google ScholarPubMed
Haines, R. W. 1938. The primitive form of epiphysis in the long bones of tetrapods. Journal of Anatomy 72:323343.Google Scholar
Haines, R. W. 1942. The evolution of epiphyses and of endochondral bone. Biological Reviews of the Cambridge Philosophical Society 17:267291.CrossRefGoogle Scholar
Haines, R. W. 1969. Epiphyses and sesamoids. Pp. 81115in Gans, C. and d'A Bellairs, A., eds. Biology of the Reptilia, Vol. 1. Academic Press, New YorkGoogle Scholar
Haines, R. W., and Mohuiddin, A. 1968. Metaplastic bone. Journal of Anatomy 103:527538.Google ScholarPubMed
Horner, J. R. 1982. Evidence of colonial nesting and ‘site fidelity’ among ornithischian dinosaurs. Nature 297:675676.CrossRefGoogle Scholar
Horner, J. R. 1984. The nesting behavior of dinosaurs. Scientific American 250:130137.CrossRefGoogle Scholar
Horner, J. R. 1994. Comparative taphonomy of some dinosaur and extant bird colonial nesting grounds. Pp. 116123in Carpenter, K., Hirsch, K. F., and Horner, J. R., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Horner, J. R. 1996. New evidence for post-eclosion parental attention in Maiasaura peeblesorum. Journal of Vertebrate Paleontology 16(Suppl. 3):42A.Google Scholar
Horner, J. R. 1999. Egg clutches and embryos of two hadrosaurian dinosaurs. Journal of Vertebrate Paleontology 19:607611.CrossRefGoogle Scholar
Horner, J. R. 2000. Dinosaur reproduction and parenting. Annual Review of Earth and Planetary Sciences 28:1945.CrossRefGoogle Scholar
Horner, J. R., and Currie, P. J. 1994. Embryonic and neonatal morphology and ontogeny of a new species of Hypacrosaurus (Ornithischia, Lambeosauridae) from Montana and Alberta. Pp. 312336in Carpenter, K., Hirsch, K. F., and Horner, J. R., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Horner, J. R., and Makela, R. 1979. Nest of juveniles provides evidence of family structure among dinosaurs. Nature 282:296298.CrossRefGoogle Scholar
Horner, J. R., and Weishampel, D. B. 1988. A comparative embryological study of two ornithischian dinosaurs. Nature 332:256257.CrossRefGoogle Scholar
Horner, J. R., and Weishampel, D. B. 1996. Correction to: a comparative embryological study of two ornithischian dinosaurs (1988). Nature 383:103.CrossRefGoogle Scholar
Horner, J. R., Padian, K., and de Ricqlès, A. 1997. Histological analysis of a dinosaur skeleton: Evidence of skeletal growth variation. Journal of Morphology 232:267.Google Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25:295304.CrossRefGoogle 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 20:109123.CrossRefGoogle Scholar
Kember, N. F., and Kirkwood, J. K. 1991. Cell kinetics and the study of longitudinal bone growth: a perspective. Pp. 153162in Dixon, A. D., Sarnat, B. G., and Hoyte, D. A. N., eds. Fundamentals of bone growth: methodology and applications. CRC Press, Boca Raton, Fla.Google Scholar
Kuettner, K. E., and Pauli, B. U. 1983. Vascularity of cartilage. Pp. 281312in Hall, B. K., ed. Cartilage, Vol. 1. Structure, function, and biochemistry. Academic Press, New York.CrossRefGoogle Scholar
Lacroix, P. 1971. The internal remodeling of bones. Pp. 119142in Bourne, G. H., ed. The biochemistry and physiology of bone, Vol. 3. Academic Press, New York.Google Scholar
Nice, M. M. 1962. Development of behavior in precocial birds. Transactions of the Linnaean Society of New York 8:1211.Google Scholar
Norell, M. A., Clark, J. M., Chiappe, L. M., and Dashzeveg, D. 1995. A nesting dinosaur. Science 378:774776.Google Scholar
Reece, R. L., and Butler, R. 1984. Some observations on the development of the long bones of ratite birds. Australian Veterinary Journal 61:403405.CrossRefGoogle Scholar
Reid, R. E. H. 1984a. The histology of dinosaurian bone, and its possible bearing on dinosaurian physiology. Pp. 629633in Ferguson, M. W. J., ed. The structure, development and evolution of reptiles. Academic Press, Orlando.Google Scholar
Reid, R. E. H. 1984b. Primary bone and dinosaurian physiology. Geological Magazine 121:589598.CrossRefGoogle Scholar
Reid, R. E. H. 1987. Bone and dinosaurian “endothermy.” Modern Geology 11:133154.Google Scholar
Reid, R. E. H. 1993. Apparent zonation and slowed late growth in a small Cretaceous theropod. Modern Geology 18:391406.Google Scholar
Reid, R. E. H. 1996. Bone histology of the Cleveland-Lloyd dinosaurs and of dinosaurs in general, Part I. Introduction: introduction to bone tissues. Brigham Young University Geological Studies 41:2571.Google Scholar
Reid, R. E. H. 1997a. How dinosaurs grew. Pp. 403413in Farlow, J. O. and Brett-Surman, M. K., eds. The complete dinosaur. Indiana University Press, Bloomington.Google Scholar
Reid, R. E. H. 1997b. Dinosaurian physiology: the case for “intermediate” dinosaurs. Pp. 450473in Farlow, J. O. and Brett-Surman, M. K., eds. The complete dinosaur. Indiana University Press, Bloomington.Google Scholar
de Ricqlés, A. J. 1968. Recherches paléohistologiques sur les os longs des tétrapodes. I. Origine du tissue osseux plexiforme des dinosauriens sauropodes. Annales de Paléontologie Vertébrés 54:133145.Google Scholar
de Ricqlés, A. J. 1972. Recherches paléohistologiques sur les os longs des Tétrapodes. III. Titanosuchiens, Dinocéphales et Dicynodontes. Annales de Paléontologie Vertébrés 58:1760.Google Scholar
de Ricqlés, A. J. 1975. Recherches paléohistologiques sur les os longs des Tétrapodes. VII. Sur la classification, la signification functionnelle et l'histoire des tissus osseux des Tétrapodes (première partie). Annales de Paléontologie Vertébrés 61:51129.Google Scholar
Ricqlés, A. J. de. 1976. Recherches paléohistologiques sur les os longs des Tétrapodes. VII. Sur la classification, la signification functionnelle et l'histoire des tissus osseux des Tétrapodes (deuxième partie). Annales de Paléontologie Vertébrés 62:71119.Google Scholar
Ricqlés, A. J. de. 1979. Quelques remarques sur l'histoire évolutive des tissus squelettiques chez les Vertébrés et plus particulièrement chez les Tétrapodes. Année Biologique 18:135.Google Scholar
Ricqlés, A. J. de. 1980. Tissue structure of dinosaur bone: functional significance and possible relation to dinosaur physiology. Pp. 103139in Thomas, R. D. K. and Olson, E. C., eds. A cold look at the warm-blooded dinosaurs. American Association for the Advancement of Science Selected Symposium No. 28. Westview, Boulder, Colo.Google Scholar
Ricqlés, A. J. de. 1983. Cyclical growth in the long bones of a sauropod dinosaur. Acta Palaeontologia Polonica 28:225232.Google Scholar
Ricqlés, A. J. de. 1992. Paleoherpetology now: a point of view. Pp. 97120in Adler, K., ed. Herpetology: current research on the biology of amphibians and reptiles. Proceedings of the first world congress of herpetology. Society for the Study of Amphibians and Reptiles, Oxford, Ohio.Google Scholar
Ricqlés, A. J. de, Horner, J. R., and Padian, K. 1998. Growth dynamics of the hadrosaurid dinosaur Maiasaura peeblesorum. Journal of Vertebrate Paleontology 18:72A.Google Scholar
Ricqlès, A. J. de, Padian, K., and Horner, J. R. 1997. Comparative biology and the bone histology of extinct tetrapods: what does it tell us? Proceedings of the fifth international congress of vertebrate morphology. Journal of Morphology 232:246.Google Scholar
Ricqlès, A. J. de, Padian, K., Horner, J. R., and Francillon-Viellot, H. 2000. Paleohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny, and biomechanical implications. Zoological Journal of the Linnean Society 129:349385.CrossRefGoogle Scholar
Ricqlès, A. J. de, Padian, K., and Horner, J. R.In press. The bone histology of basal birds in phylogenetic and ontogenetic perspective. In Gauthier, J. A., ed. Perspectives on the origin and early evolution of birds. Yale University Press, New Haven, Conn.Google Scholar
Rimblot-Baly, F., de Ricqlès, A., and Zylberberg, L. 1995. Analyse paléohistologique d'une série de croissance partielle chez Lapparentosaurus madagascariensis (Jurassique moyen): essai sur la dynamique de croissance d'un dinosaure sauropode. Annales de Paléontologie 81:4986.Google Scholar
Romanoff, A. L. 1960. The avian embryo. Macmillan, New York.Google Scholar
Starck, J. M. 1989. Zeitmuster der Ontogenesen bei nestflüchtenden und nesthockenden Vögeln. Courier Forschungsinstitut Senckenberg 114:1319.Google Scholar
Starck, J. M. 1993. Evolution of avian ontogenies. Current Ornithology 10:275366.CrossRefGoogle Scholar
Starck, J. M. 1994. Quantitative design of the skeleton in bird hatchlings: does tissue compartmentalization limit post-hatching growth rates? Journal of Morphology 222:113131.CrossRefGoogle Scholar
Starck, J. M. 1996. Comparative morphology and cytokinetics of skeletal growth in hatchlings of altricial and precocial birds. Zoologischer Anzeiger 235:5375.Google Scholar
Starck, J. M. 1998. Structural variants and invariants in avian embryonic and postnatal development. Pp. 5988in Starck, and Ricklefs, 1998a.CrossRefGoogle Scholar
Starck, J. M., and Ricklefs, R. E., eds. 1998a. Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York.CrossRefGoogle Scholar
Starck, J. M., and Ricklefs, R. E., 1998b. Patterns of development: the altricial-precocial spectrum. Pp. 330in Starck, and Ricklefs, 1998a.CrossRefGoogle Scholar
Sterchi, D., and Eurell, J. 1995. An evaluation of methylmethacrylate mixtures for hard tissue embedding. Journal of Histotechnology 18:4549.CrossRefGoogle Scholar
Thorpe, B. H. 1988. Pattern of vascular canals in the bone extremities of the pelvic appendicular skeleton in broiler type fowl. Research in Veterinary Science 44:112124.CrossRefGoogle Scholar
Varricchio, D. J. 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 13:99104.CrossRefGoogle Scholar
Varricchio, D. J., Jackson, F., Borlowski, J., and Horner, J. R. 1997. Nest and egg clutches for the theropod dinosaur Troodon formosus and evolution of avian reproductive traits. Nature 385:247250.CrossRefGoogle Scholar
Wilsman, N. J., and Van Sickle, D. C. 1972. Cartilage canals: their morphology and distribution. Anatomical Record 173:7994.CrossRefGoogle ScholarPubMed
Wise, D. R., and Jennings, A. R. 1973. The development and morphology of the growth plates of two longbones of the turkey. Research in Veterinary Science 14:161166.CrossRefGoogle Scholar