Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T18:36:57.821Z Has data issue: false hasContentIssue false
  • English
  • Français

Mesozoic avian bone microstructure: physiological implications

Published online by Cambridge University Press:  08 February 2016

Anusuya Chinsamy ,
Luis M. Chiappe  and
Peter Dodson
Anusuya Chinsamy
Affiliation:
Earth Sciences Division, South African Museum, Post Office Box 61, Cape Town, 8000 South Africa
Luis M. Chiappe
Affiliation:
Department of Vertebrate Paleontology, American Museum of Natural History, Central Park West at Seventy-ninth Street, New York, New York 10024
Peter Dodson
Affiliation:
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, Pennsylvania 19104-6045
Get access Rights & Permissions [Opens in a new window]

Abstract

We report on the bone microstructure of the Late Cretaceous birds Patagopteryx deferrariisi and members of the Enantiornithes. These birds represent the most primitive birds ever studied histologically. The occurrence of growth rings indicating alternating periods of slowed and fast growth suggests that these basal birds had slower growth rates, and differed physiologically from their modern relatives. Our findings also call into question previous ideas suggesting that nonavian theropods developed a full avian degree of homeothermic endothermy, which was later inherited by birds. On the contrary, our findings suggest that birds developed classic endothermy relatively late in their phylogenetic history.

Type
Articles
Information
Paleobiology , Volume 21 , Issue 4 , Fall 1995 , pp. 561 - 574
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.)

References

Literature Cited

Alvarenga, H. M. F. 1993. A origem das aves e seus fósseis. Pp. 16–26in de Andrade, M. A., ed. A vida das aves. Littera Maciel, Belo Horizonte.Google Scholar
Alvarenga, H. M. F., and Bonaparte, J. F. 1992. A new flightless land bird from the Cretaceous of Patagonia. Pp. 51–64in Campbell, K. E., ed. Papers in avian paleontology, honoring Pierce Brodkorb. Natural History Museum of Los Angeles County, Science Series 36.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
Amprino, R., and Godina, G. 1944. Osservazioni sui processi di rimaneggiamento strutturale della sostanza compatta della ossa lunghe degli Ucelli corridori. Anatomischer Anzeiger 95:191–214.Google Scholar
Bakker, R. T. 1986. The dinosaur heresies: new theories unlocking the mystery of the dinosaurs and their extinction. William Morrow, New York.Google Scholar
Bonaparte, J. F. 1991. Los vertebrados fósiles de la Formación Río Colorado de Neuquén y cercanias, Cretácico Superior, Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (Paleontología) 4:17–123.Google Scholar
Bonaparte, J. F., and Powell, J. E. 1980. A continental assemblage of tetrapods from the Upper Cretaceous beds of El Brete, northwestern Argentina (Sauropoda-Coelurosauria-Carnosauria-Aves). Mémoirs de la Société Géologique de France (Nouvelle Série) 139:19–28.Google Scholar
Bonaparte, J. F., Salfitty, J. A., Bossi, G., and Powell, J. E. 1977. Hallazgos de dinosaurios y aves cretácicas en la Formación Lecho de El Brete (Salta), próximo al límite con Tucumán. Acta Geológica Lilloana 14:5–17.Google Scholar
Bock, W. J. 1985. The arboreal theory for the origin of birds. Pp. 199–207in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the International Archaeopteryx Conference, Eichstätt.Google Scholar
de Buffrénil, V. 1982. Morphogenesis of bone ornamentation in extant and extinct crocodilians. Zoomorphology 99:155–166.CrossRefGoogle Scholar
de Buffrénil, V., and Shoevaert, D. 1989. Données quantitatives et observations histologiques sur la pachyostose du squelette du dugong, Dugong dugon (Müller) (Sirenia, Dugongidae). Canadian Journal of Zoology 67:2107–2119.CrossRefGoogle Scholar
Castanet, J., Francillon-Vieillot, H., Meunier, F. J., and de Ricqlès, A. 1993. Bone and individual aging. Pp. 245–283in Hall, B. K. ed. Bone, Vol. 7, CRC Press, Boca Raton.Google Scholar
Cazau, L. B., and Uliana, M. A. 1973. El Cretácico superior continental de la Cuenca Neuquina. V Congreso Geológico Argentino, Actas 3:131–163.Google Scholar
Chiappe, L. M. 1991. Cretaceous birds of Latin America. Cretaceous Research 12:55–63.CrossRefGoogle Scholar
Chiappe, L. M. 1992. Enantiornithine tarsometatarsi and the avian affinity of the Late Cretaceous Avisauridae. Journal of Vertebrate Paleontology 12:344–350.CrossRefGoogle Scholar
Chiappe, L. M. 1993. Enantiornithine (Aves) tarsometatarsi from the Cretaceous Lecho Formation of northwestern Argentina. American Museum Novitates 3083:1–27.Google Scholar
Chiappe, L. M. 1995. Phylogenetic position of the Cretaceous birds of Argentina: Enantiornithes and Patagopteryx deferrariisi in Third Symposium of the Society of Avian Paleontology and Evolution. Courier Forschungsinstitut Senckenberg.Google Scholar
Chiappe, L. M.In press. Late Cretaceous birds of southern South America: anatomy and systematics of Enantiornithes and Patagopteryx deferrariisi. Revista Geológica Chilena, n.s.Google Scholar
Chiappe, L. M., and Calvo, J. O. 1994. Neuquenornis volans, a new late Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia, Argentina. Journal of Vertebrate Paleontology 14:230–246.CrossRefGoogle Scholar
Chinsamy, A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontologia Africana 27:77–82.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. 213–228in Rosenberg, G. D. and Wolberg, L., eds. The Dino Fest: proceedings of a conference for the general public. Paleontological Society Special Publication no. 7, University of Tennessee Press, Knoxville.Google Scholar
Chinsamy, A. 1995. Histological perspectives on growth in the birds Struthio camelus and Sagittarius serpentarius. in Third Symposium of the Society of Avian Paleontology and Evolution. Courier Forschungsinstitut Senckenberg.Google Scholar
Chinsamy, A., and Raath, M. A. 1992. Preparation of bone for histological study. Palaeontologia africana 29:39–44.Google Scholar
Chinsamy, A., and Rubidge, B. 1993. Dicynodont (Therapsida) bone histology: phylogenetic and physiological implications. Palaeontologia africana 30:1–6.Google Scholar
Chinsamy, A., Chiappe, L. M., and Dodson, P. 1994. Growth rings in Mesozoic avian bones: physiological implications for basal birds. Nature (London) 368:196–197.CrossRefGoogle Scholar
Chinsamy, A., Hanrahan, S., Neto, R. M., and Seely, M. 1995. Skeletochronological assessment of age in Angolosaurus skoogi, a lizard living in an aseasonal environment. Journal of Herpetology.CrossRefGoogle Scholar
Cracraft, J. 1986. The origin and early diversification of birds. Paleobiology 12:383–399.CrossRefGoogle Scholar
Cracraft, J. 1988. The major clades of birds. Pp. 339–361in Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 1: Amphibians, Reptiles, Birds. Clarendon Press, Oxford.Google Scholar
Cruz, C. E., Condat, P., Kozlowski, E., and Manceda, R. 1989. Análisis estratigráfico secuencial del Grupo Neuquén (Cretácico superior) en el valle del Río Grande, Provincia de Mendoza. I Congreso Argentino de Hidrocarburos, Actas 2:689–714.Google Scholar
Enlow, D. H. 1963. Principles of bone remodeling. Thomas, Springfield, Ill.Google Scholar
Enlow, D. H., and Brown, S. O. 1957. A comparative histological study of fossil and recent bone tissue. Part 2. Texas Journal of Science 9:186–214.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. 471–530in Carter, J. G., ed. Skeletal biomineralization: patterns, processes and evolutionary trends, Vol. 1. Van Nostrand Reinhold, New York.Google Scholar
Gauthier, J. 1986. Saurischian monophyly and the origin of birds. Pp. 1–55in Padian, K., ed. The origin of birds and the evolution of flight. Memoirs of the California Academy of Sciences, no. 8.Google Scholar
Gómez Omil, R. J., Boll, A., and Hernández, R. M. 1989. Cuenca Cretácico-Terciaria del Noroeste Argentino (Grupo Salta). Pp. 43–64in Chebli, G. A. and Spalletti, L. A., eds. Cuencas Sedimentarias Argentinas. Serie Correlación Geológica, no. 6.Google Scholar
Houck, M. A., Gauthier, J. A., and Strauss, R. E. 1990. Allometric scaling in the earliest fossil bird, Archaeopteryx lithographica. Science 247:195–198.CrossRefGoogle ScholarPubMed
Houde, P. W. 1986. Ostrich ancestors found in the Northern Hemisphere suggest new hypothesis of ratite origins. Nature (London) 324:563–565.CrossRefGoogle ScholarPubMed
Houde, P. W. 1987. Histological evidence for the systematic position of Hesperornis (Odontornithes: Hesperornithiformes). Auk 104:125–129.CrossRefGoogle Scholar
Huxley, T. H. 1868. On the animals which are most nearly intermediate between birds and reptiles. Annals and Magazine of Natural History 2:66–75.Google Scholar
Klevezal, G. A., and Kleinenberg, S. E. 1967. Age determination of mammals from the layered structures in teeth and bone. [In Russian.] Nauka, Moscow. English translation bySalkind, J.(1969), Israel Program for Scientific Translations, Jerusalem.Google Scholar
Klevezal, G. A., Kallar Salas, A. V., and Kirpichev, S. P. 1972. Determination of age in birds by layers in the periosteal bone Zoologichesky Zhurnal 51:1726–1730 [In Russian.]Google Scholar
Koubek, P., and Hrabe, V. 1984. Estimating the age of male Phasianus colchicus by bone histology and spur length. Folia Zoologica 33:303–313.Google Scholar
Legarreta, L., and Gulisano, C. 1989. Análisis estratigráfico secuencial de la Cuenca Neuquina (Triásico Superior-Terciario Inferior). Pp. 221–243in Chebli, G. and Spalletti, L., eds. Cuencas Sedimentarias Argentinas. Serie Correlación Geológica 6. Universidad Nacional de Tucumán, Tucumán.Google Scholar
Lewis, J. C. 1979. Periosteal layers do not indicate ages of sandhill cranes. Journal of Wildlife Management 43:269–271.CrossRefGoogle Scholar
Martin, L. D. 1983. The origin and early radiation of birds. Pp. 291–338in Bush, A. H. and Clark, G. A. Jr., eds. Perspectives in ornithology. Cambridge University Press, New York.CrossRefGoogle Scholar
Martin, L. D. 1987. The beginning of the modern avialian radiation. Pp. 9–19in Mourer-Chauvire, C., coordinator. L'evolution des oiseaux d'après le témoignage des fossiles. Documents des Laboratoires de Geologie Lyon, no. 99.Google Scholar
Nelson, R. C., and Bookhout, A. T. 1980. Counts of periosteal layers invalid for aging Canada geese. Journal of Wildlife Management 44:518–521.CrossRefGoogle Scholar
Ostrom, J. H. 1969. Osteology of Deinonychus antirrhopus, an unusual theropod from the Lower Cretaceous of Montana. Bulletin of the Peabody Museum of Natural History 30:1–165.Google Scholar
Ostrom, J. H. 1973. The ancestry of birds. Nature (London) 242:136.CrossRefGoogle Scholar
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society of London 8:91–182.CrossRefGoogle Scholar
Peabody, F. E. 1961. Annual growth zones in living and fossil vertebrates. Journal of Morphology 108:11–62.CrossRefGoogle Scholar
Regal, P. J. 1985. Common sense and reconstructions of the biology of fossils: Archaeopteryx and feathers. Pp. 67–74in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the International Archaeopteryx Conference, Eichstatt.Google Scholar
Reid, R. E. H. 1987. Bone and dinosaurian “endothermy.” Modern Geology 11:133–154.Google Scholar
Reid, R. E. H. 1990. Zonal “growth rings” in dinosaurs. Modern Geology 15:19–48.Google Scholar
Reid, R. E. H. 1993. Apparent zonation and slowed late growth in a small cretaceous theropod. Modern Geology 18:391–406.Google Scholar
Ricqlès, A. de. 1980. Tissue structure of dinosaur bone: functional significance and possible relation to dinosaur physiology. Pp. 103–139in 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 Press, Boulder.Google Scholar
Ricqlès, A. de. 1983. Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica 28:225–246.Google Scholar
Ricqlès, A. de. 1990. Zonal “growth rings” in dinosaurs. Modern Geology 15:19–48.Google Scholar
Ricqlès, A. de, Meunier, F. J., Castanet, J., and Francillon-Vieillot, H. 1991. Comparative microstructure of bone. Pp. 1–77in Hall, B. K., ed. Bone. Bone matrix and bone specific products, Vol. 3. CRC Press, Boca Raton.Google Scholar
Ruben, J. A. 1991. Reptilian physiology and the flight capacity of Archaeopteryx. Evolution 45:1–17.CrossRefGoogle ScholarPubMed
Sanz, J. L., Chiappe, L. M., Buscalioni, A. D., and Bonaparte, J. F. 1995. The osteology of Concornis lacustris (Aves:Enantiornithes) from the Lower Cretaceous of Spain and a re-examination of its phylogenetic relationships. American Museum Novitates. 3133:1–33.Google Scholar
Sereno, P., and Rao, C. 1992. Early evolution of avian flight and perching: new evidence from Lower Cretaceous of China. Science 255:845–848.CrossRefGoogle ScholarPubMed
van Soest, R. W. M., and Utrecht, W. L. 1971. The layered structure of bones of birds as a possible indication of age. Bijdragen tot de Dierkunde 41:61–66.CrossRefGoogle Scholar
Varricchio, D. J. 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 13:99–104.CrossRefGoogle Scholar
Walker, C. A. 1981. New subclass of birds from the Cretaceous of South America. Nature (London) 292:51–53.CrossRefGoogle Scholar
Weishampel, D. B., Dodson, P., and Osmólska, H. 1990. The Dinosauria. University of California Press, Los Angeles.Google Scholar
Zavattarri, E., and Cellini, I. 1956. La minuta archtetettura delle ossa degli uccelli e il suo valore nella sistematica dei grandi gruppi. Monitore Zoologico Italliano 64:189–200.Google Scholar