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Mesozoic avian bone microstructure: physiological implications

  • Anusuya Chinsamy (a1), Luis M. Chiappe (a2) and Peter Dodson (a3)
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.

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Alvarenga, H. M. F. 1993. A origem das aves e seus fósseis. Pp. 1626in de Andrade, M. A., ed. A vida das aves. Littera Maciel, Belo Horizonte.
Alvarenga, H. M. F., and Bonaparte, J. F. 1992. A new flightless land bird from the Cretaceous of Patagonia. Pp. 5164in Campbell, K. E., ed. Papers in avian paleontology, honoring Pierce Brodkorb. Natural History Museum of Los Angeles County, Science Series 36.
Amprino, R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Archives de Biologie 58:315330.
Amprino, R., and Godina, G. 1944. Osservazioni sui processi di rimaneggiamento strutturale della sostanza compatta della ossa lunghe degli Ucelli corridori. Anatomischer Anzeiger 95:191214.
Bakker, R. T. 1986. The dinosaur heresies: new theories unlocking the mystery of the dinosaurs and their extinction. William Morrow, New York.
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) 4:17123.
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) 139:1928.
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 14:517.
Bock, W. J. 1985. The arboreal theory for the origin of birds. Pp. 199207in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the International Archaeopteryx Conference, Eichstätt.
de Buffrénil, V. 1982. Morphogenesis of bone ornamentation in extant and extinct crocodilians. Zoomorphology 99:155166.
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 67:21072119.
Castanet, J., Francillon-Vieillot, H., Meunier, F. J., and de Ricqlès, A. 1993. Bone and individual aging. Pp. 245283in Hall, B. K. ed. Bone, Vol. 7, CRC Press, Boca Raton.
Cazau, L. B., and Uliana, M. A. 1973. El Cretácico superior continental de la Cuenca Neuquina. V Congreso Geológico Argentino, Actas 3:131163.
Chiappe, L. M. 1991. Cretaceous birds of Latin America. Cretaceous Research 12:5563.
Chiappe, L. M. 1992. Enantiornithine tarsometatarsi and the avian affinity of the Late Cretaceous Avisauridae. Journal of Vertebrate Paleontology 12:344350.
Chiappe, L. M. 1993. Enantiornithine (Aves) tarsometatarsi from the Cretaceous Lecho Formation of northwestern Argentina. American Museum Novitates 3083:127.
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.
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.
Chiappe, L. M., and Calvo, J. O. 1994. Neuquenornis volans, a new late Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia, Argentina. Journal of Vertebrate Paleontology 14:230246.
Chinsamy, A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontologia Africana 27:7782.
Chinsamy, A. 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geology 18:319329.
Chinsamy, A. 1994. Dinosaur bone histology: implications and inferences. Pp. 213228in 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.
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.
Chinsamy, A., and Raath, M. A. 1992. Preparation of bone for histological study. Palaeontologia africana 29:3944.
Chinsamy, A., and Rubidge, B. 1993. Dicynodont (Therapsida) bone histology: phylogenetic and physiological implications. Palaeontologia africana 30:16.
Chinsamy, A., Chiappe, L. M., and Dodson, P. 1994. Growth rings in Mesozoic avian bones: physiological implications for basal birds. Nature (London) 368:196197.
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.
Cracraft, J. 1986. The origin and early diversification of birds. Paleobiology 12:383399.
Cracraft, J. 1988. The major clades of birds. Pp. 339361in Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 1: Amphibians, Reptiles, Birds. Clarendon Press, Oxford.
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 2:689714.
Enlow, D. H. 1963. Principles of bone remodeling. Thomas, Springfield, Ill.
Enlow, D. H., and Brown, S. O. 1957. A comparative histological study of fossil and recent bone tissue. Part 2. Texas Journal of Science 9:186214.
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. 471530in Carter, J. G., ed. Skeletal biomineralization: patterns, processes and evolutionary trends, Vol. 1. Van Nostrand Reinhold, New York.
Gauthier, J. 1986. Saurischian monophyly and the origin of birds. Pp. 155in Padian, K., ed. The origin of birds and the evolution of flight. Memoirs of the California Academy of Sciences, no. 8.
Gómez Omil, R. J., Boll, A., and Hernández, R. M. 1989. Cuenca Cretácico-Terciaria del Noroeste Argentino (Grupo Salta). Pp. 4364in Chebli, G. A. and Spalletti, L. A., eds. Cuencas Sedimentarias Argentinas. Serie Correlación Geológica, no. 6.
Houck, M. A., Gauthier, J. A., and Strauss, R. E. 1990. Allometric scaling in the earliest fossil bird, Archaeopteryx lithographica. Science 247:195198.
Houde, P. W. 1986. Ostrich ancestors found in the Northern Hemisphere suggest new hypothesis of ratite origins. Nature (London) 324:563565.
Houde, P. W. 1987. Histological evidence for the systematic position of Hesperornis (Odontornithes: Hesperornithiformes). Auk 104:125129.
Huxley, T. H. 1868. On the animals which are most nearly intermediate between birds and reptiles. Annals and Magazine of Natural History 2:6675.
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.
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 51:17261730 [In Russian.]
Koubek, P., and Hrabe, V. 1984. Estimating the age of male Phasianus colchicus by bone histology and spur length. Folia Zoologica 33:303313.
Legarreta, L., and Gulisano, C. 1989. Análisis estratigráfico secuencial de la Cuenca Neuquina (Triásico Superior-Terciario Inferior). Pp. 221243in Chebli, G. and Spalletti, L., eds. Cuencas Sedimentarias Argentinas. Serie Correlación Geológica 6. Universidad Nacional de Tucumán, Tucumán.
Lewis, J. C. 1979. Periosteal layers do not indicate ages of sandhill cranes. Journal of Wildlife Management 43:269271.
Martin, L. D. 1983. The origin and early radiation of birds. Pp. 291338in Bush, A. H. and Clark, G. A. Jr., eds. Perspectives in ornithology. Cambridge University Press, New York.
Martin, L. D. 1987. The beginning of the modern avialian radiation. Pp. 919in Mourer-Chauvire, C., coordinator. L'evolution des oiseaux d'après le témoignage des fossiles. Documents des Laboratoires de Geologie Lyon, no. 99.
Nelson, R. C., and Bookhout, A. T. 1980. Counts of periosteal layers invalid for aging Canada geese. Journal of Wildlife Management 44:518521.
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 30:1165.
Ostrom, J. H. 1973. The ancestry of birds. Nature (London) 242:136.
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society of London 8:91182.
Peabody, F. E. 1961. Annual growth zones in living and fossil vertebrates. Journal of Morphology 108:1162.
Regal, P. J. 1985. Common sense and reconstructions of the biology of fossils: Archaeopteryx and feathers. Pp. 6774in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the International Archaeopteryx Conference, Eichstatt.
Reid, R. E. H. 1987. Bone and dinosaurian “endothermy.” Modern Geology 11:133154.
Reid, R. E. H. 1990. Zonal “growth rings” in dinosaurs. Modern Geology 15:1948.
Reid, R. E. H. 1993. Apparent zonation and slowed late growth in a small cretaceous theropod. Modern Geology 18:391406.
Ricqlès, A. 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 Press, Boulder.
Ricqlès, A. de. 1983. Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica 28:225246.
Ricqlès, A. de. 1990. Zonal “growth rings” in dinosaurs. Modern Geology 15:1948.
Ricqlès, A. de, Meunier, F. J., Castanet, J., and Francillon-Vieillot, H. 1991. Comparative microstructure of bone. Pp. 177in Hall, B. K., ed. Bone. Bone matrix and bone specific products, Vol. 3. CRC Press, Boca Raton.
Ruben, J. A. 1991. Reptilian physiology and the flight capacity of Archaeopteryx. Evolution 45:117.
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. 3133:133.
Sereno, P., and Rao, C. 1992. Early evolution of avian flight and perching: new evidence from Lower Cretaceous of China. Science 255:845848.
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 41:6166.
Varricchio, D. J. 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 13:99104.
Walker, C. A. 1981. New subclass of birds from the Cretaceous of South America. Nature (London) 292:5153.
Weishampel, D. B., Dodson, P., and Osmólska, H. 1990. The Dinosauria. University of California Press, Los Angeles.
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 64:189200.
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