Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T23:27:59.924Z Has data issue: false hasContentIssue false
  • English
  • Français

Inferring flight parameters of Mesozoic avians through multivariate analyses of forelimb elements in their living relatives

Published online by Cambridge University Press:  06 December 2016

Francisco J. Serrano ,
Paul Palmqvist ,
Luis M. Chiappe  and
José L. Sanz
Francisco J. Serrano
Affiliation:
Departamento de Ecología y Geología, Facultad de Ciencias, Universidad de Málaga. Campus Universitario de Teatinos s/n, 29071 Málaga, Spain. E-mail: fjsa@uma.es, ppb@uma.es.
Paul Palmqvist
Affiliation:
Departamento de Ecología y Geología, Facultad de Ciencias, Universidad de Málaga. Campus Universitario de Teatinos s/n, 29071 Málaga, Spain. E-mail: fjsa@uma.es, ppb@uma.es.
Luis M. Chiappe
Affiliation:
Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007, U.S.A. E-mail: lchiappe@nhm.org
José L. Sanz
Affiliation:
Unidad de Paleontología, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Calle Darwin 2, Cantoblanco, 28049 Madrid, Spain. E-mail: dinoproyecto@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Our knowledge of the diversity, ecology, and phylogeny of Mesozoic birds has increased significantly during recent decades, yet our understanding of their flight competence remains poor. Wing loading (WL) and aspect ratio (AR) are two aerodynamically relevant parameters, as they relate to energy costs of aerial locomotion and flight maneuverability. They can be calculated in living birds (i.e., Neornithes) from body mass (BM), wingspan (B), and lift surface (S L). However, the estimates for extinct birds can be subject to biases from statistical issues, phylogeny, locomotor adaptations, and diagenetic compaction. Here we develop a sequential approach for generating reliable multivariate models that allow estimation of measurements necessary to determine WL and AR in the main clades of non-neornithine Mesozoic birds. The strength of our predictions is supported by the use of those variables that show similar scaling patterns in modern and stem taxa (i.e., non-neornithine birds) and the similarity of our predictions with measurements obtained from fossils preserving wing outlines. In addition, although our WL and AR values are based on estimates (BM, B, and S L) that have an associated error, there is no cumulative error in their calculation, and both parameters show low prediction errors. Therefore, we present the first taxonomically broad, error-calibrated estimation of these two important aerodynamic parameters in non-neornithine birds. Such estimates show that the WL and AR of the non-neornithine birds here analyzed fall within the range of variation of modern birds (i.e., Neornithes). Our results indicate that most modern flight modes (e.g., continuous flapping, flap and gliding, flap and bounding, thermal soaring) were possible for the wide range of non-neornithine avian taxa; we found no evidence for the presence of dynamic soaring among these early birds.

Type
Articles
Information
Paleobiology , Volume 43 , Issue 1 , February 2017 , pp. 144 - 169
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

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

Alerstam, T., Rosén, M., Bäckman, J., Ericson, P. G., and Hellgren, O.. 2007. Flight speeds among bird species: allometric and phylogenetic effects. PLoS Biology 5:e197.CrossRefGoogle ScholarPubMed
Álvarez, J. C., Meseguer, J., Meseguer, E., and Perez, A.. 2001. On the role of the alula in the steady flight of birds. Ardeola 48:161–173.Google Scholar
Bell, A., and Chiappe, L. M. 2011. Statistical approach for inferring ecology of Mesozoic birds. Journal of Systematic Palaeontology 9:119–133.Google Scholar
Benson, R. B., and Choiniere, J. N.. 2013. Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proceedings of the Royal Society of London B 280:20131780.Google Scholar
Bowerman, B. L., and O’Connell, R. T.. 1990. Linear statistical models: an applied approach. Duxbury Press, Belmont, Calif.Google Scholar
Bruderer, B., Peter, D., Boldt, A., and Liechti, F.. 2010. Wing-beat characteristics of birds recorded with tracking radar and cine camera. Ibis 152:272–291.Google Scholar
Brusatte, S. L., O’Connor, J. K., and Jarvis, E. D.. 2015. The origin and diversification of birds. Current Biology 25:888–898.Google Scholar
Burgers, P., and Chiappe, L. M. 1999. The wing of Archaeopteryx as a primary thrust generator. Nature 399:60–62.CrossRefGoogle Scholar
Campbell, K. E., and Marcus, L.. 1992. The relationships of hindlimb bone dimensions to body weight in birds. Natural History Museum of Los Angeles County. Science Series 36:395–412.Google Scholar
Campione, N., and Evans, D.. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:60.CrossRefGoogle ScholarPubMed
Carrano, M. T. 2001. Implications of limb bone scaling, curvature and eccentricity in mammals and non-avian dinosaurs. Journal of Zoology 254:41–55.Google Scholar
Cawley, G. C., and Janacek, G. J.. 2010. On allometric equations for predicting body mass of dinosaurs. Journal of Zoology 280:355–361.CrossRefGoogle Scholar
Chan, N. R., Dyke, G. J., and Benton, M. J.. 2012. Primary feather lengths may not be important for inferring the flight styles of Mesozoic birds. Lethaia 46:146–153.Google Scholar
Chatterjee, S., and Templin, R. J.. 2003. The flight of Archaeopteryx . Naturwissenschaften 90:27–32.CrossRefGoogle ScholarPubMed
Chiappe, L. M. 2007. Glorified dinosaurs: the origin and early evolution of birds. Wiley, Hoboken, N.J.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
Chiappe, L. M., and Meng, Q.. 2016. Birds of stone. Johns Hopkins University Press, Baltimore, Md.Google Scholar
Chiappe, L. M., and Witmer, L.. 2002. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Chiappe, L. M., Ji, S. A., Ji, Q., and Norell, M. A.. 1999. Anatomy and systematics of the Confuciusornithidae (Theropoda, Aves) from the late Mesozoic of northeastern China. Bulletin of the American Museum of Natural History 242:1–89.Google Scholar
Chiappe, L. M., Zhao, B., O’Connor, J. K., Chunling, G., Wang, X., Habib, M., and Cheng, X.. 2014. A new specimen of the Early Cretaceous bird Hongshanornis longicresta: insights into the aerodynamics and diet of a basal ornithuromorph. PeerJ 2:e234.Clarke, J., and M. A. Norell. 2002. The morphology and phylogenetic position of Apsaravis ukhaana from the Late Cretaceous of Mongolia. American Museum Novitates, 3387.Google Scholar
Clifford, D., Cressie, N., England, J. R., Roxburgh, S. H., and Paul, K. I.. 2013. Correction factors for unbiased, efficient estimation and prediction of biomass from log–log allometric models. Forest Ecology and Management 310:375–381.Google Scholar
Close, R. A., and Rayfield, E. J.. 2012. Functional morphometric analysis of the furcula in Mesozoic birds. PLoS One 7:e36664.CrossRefGoogle ScholarPubMed
Cubo, J., and Casinos, A.. 1998. Biomechanical significance of cross-sectional geometry of avian long bones. European Journal of Morphology 36:19–28.Google Scholar
Dececchi, T. A., and Larsson, H. C.. 2013. Body and limb size dissociation at the origin of birds: uncoupling allometric constraints across a macroevolutionary transition. Evolution 67:2741–2752.Google Scholar
De Esteban-Trivigno, S., Mendoza, M., and De Renzi, M.. 2008. Body mass estimation in Xenarthra: a predictive equation suitable for all quadrupedal terrestrial placentals? Journal of Morphology 269:1276–1293.Google Scholar
De Margerie, E., Sanchez, S., Cubo, J., and Castanet, J.. 2005. Torsional resistance as a principal component of the structural design of long bones: comparative multivariate evidence in birds. Anatomical Record A 282A:49–66.Google Scholar
Díaz-Uriarte, R., and Garland, T.. 1996. Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Systematic Biology 45:27–47.Google Scholar
Dyke, G. J., and Nudds, R. L.. 2009. The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous. Lethaia 42:248–254.Google Scholar
Eisenhauer, J. G. 2003. Regression through the origin. Teaching Statistics 25(3): 76–80.CrossRefGoogle Scholar
Elzanowski, A. 2002. Archaeopterygidae (Upper Jurassic of Germany). Pp. 129–159 in L. M. Chiappe, and L. M. Witmer, eds. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Evangelista, D., Cardona, G., Guenther-Gleason, E., Huynh, T., Kwong, A., Marks, D., Ray, N., Tisbe, A., Tse, K., and Koehl, M.. 2014. Aerodynamic characteristics of a feathered dinosaur measured using physical models: effects of form on static stability and control effectiveness. PLoS ONE 9:e85203.Google Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.Google Scholar
Field, D. J., Lynner, C., Brown, C., and Darroch, S. A.. 2013. Skeletal correlates for body mass estimation in modern and fossil flying birds. PLoS ONE 8:e82000.CrossRefGoogle ScholarPubMed
Gao, C., Chiappe, L. M., Zhang, F., Pomeroy, D., Shen, C., Chinsamy, A., and Walsh, M.. 2012. A subadult specimen of the Early Cretaceous bird Sapeornis chaoyangensis and a taxonomic reassessment of sapeornithids. Journal of Vertebrate Paleontology 32:1103–1112.CrossRefGoogle Scholar
Gingerich, P., Smith, B., and Rosenberg, K.. 1982. Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils. American Journal of Physical Anthropology 58:81–100.Google Scholar
Greenwalt, C. H. 1975. The flight of birds. Transactions of the American Philosophical Society new series 65:1–65.Google Scholar
Habib, M. B., and Ruff, C.. 2008. The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society 153:601–624.Google Scholar
Harvey, P. H., and Pagel, M. D.. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.Google Scholar
Hayes, J. P., and Shonkwiler, J. S.. 2006. Allometry, antilog transformations, and the perils of prediction on the original scale. Physiological and Biochemical Zoology 79:665–674.Google Scholar
Hinic-Frlog, S., and Motani, R.. 2010. Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae. Journal of Evolutionary Biology 23:372–385.Google Scholar
Hou, L. H. 1997. Mesozoic birds of China. Feng-huang-ku Bird Park, Taiwan [In Chinese.].Google Scholar
Hurvich, C. M., and Tsai, C. L.. 1990. The impact of model selection on inference in linear regression. American Statistician 44:214–217.Google Scholar
IBM Corporation. 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, N.Y. http://www.ibm.com/software/es/analytics/spss.Google Scholar
Kleinbaum, D. G., Kupper, L. L., and Muller, K. E.. 1997. Applied regression analysis and other multivariable methods. Duxbury Press, Belmont, Calif.Google Scholar
Ksepka, D. T. 2014. Flight performance of the largest volant bird. Proceedings of the National Academy of Sciences USA 111:10624–10629.Google Scholar
Laurin, M. 2004. The evolution of body size, Cope’s rule and the origin of amniotes. Systematic Biology 53:594–622.CrossRefGoogle ScholarPubMed
Longrich, N. 2006. Structure and function of hindlimb feathers in Archaeopteryx lithographica . Paleobiology 32:417–431.Google Scholar
MacLeod, N. 2004. Palaeo-math 101: regression 2. Palaeontological Association Newsletter 56:60–71.Google Scholar
MacNally, R. 2000. Regression and model-building in conservation biology, biogeography and ecology: the distinction between—and reconciliation of—“predictive” and “explanatory” models. Biodiversity and Conservation 9:655–671.CrossRefGoogle Scholar
Maddison, W. P., and Maddison, D. R.. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.Google Scholar
Mendoza, M, Janis, C. M., and Palmqvist, P.. 2006. Estimating the body mass of extinct ungulates: a study on the use of multiple regression. Journal of Zoology 270:90–101.Google Scholar
Meseguer, J., and Sanz-Andrés, A.. 2007. Aerodinámica del vuelo: aves y aeronaves. Cuadernos Aena 9. Aena, Aeropuertos Españoles y Navegación Aérea, Spain.Google Scholar
Meseguer, J., Sanz-Andrés, A., Pedro, A., Pérez Grande, M. I., Franchini, S. N., Sanz García, J. L., and Chiappe, L. M.. 2008. Control de capa limite en el vuelo a bajos números de Reynolds. Ingeniería Aeronáutica y Astronáutica 387:15–24.Google Scholar
Meseguer, J., Chiappe, L. M., Sanz, J. L., Ortega, F., Sanz-Andrés, A., Pérez-Grande, M. I., and Franchini, S.. 2012. Lift devices in the flight of Archaeopteryx . Revista Española de Paleontología 27:125–130.Google Scholar
Middleton, K. M., and Gatesy, S. M.. 2000. Theropod forelimb design and evolution. Zoological Journal of the Linnean Society 128:149–187.CrossRefGoogle Scholar
Midford, P. E., Garland, T., and Maddison, W. P.. 2005. PDAP Package of Mesquite, Version 1.16.Google Scholar
Mitchell-Olds, T., and Shaw, R. G.. 1987. Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161.Google Scholar
Norberg, U. M. 2002. Structure, form, and function of flight in engineering and the living world. Journal of Morphology 252:52–81.Google Scholar
Nudds, R. L. 2007. Wing-bone length allometry in birds. Journal of Avian Biology 38:515–519.Google Scholar
Nudds, R. L., and Rayner, J. M. V.. 2006. Scaling of body frontal area and body width in birds. Journal of Morphology 267:341–346.Google Scholar
Nudds, R. L., Atterholt, J., Wang, X., You, H. L., and Dyke, G. J.. 2013. Locomotory abilities and habitat of the Cretaceous bird Gansus yumenensis inferred from limb length proportions. Journal of Evolutionary Biology 26:150–154.Google Scholar
O’Connor, J., Gao, K., and Chiappe, L. M.. 2010. A new Ornithuromorph (Aves: Ornithothoraces) bird from the Jehol Group indicative of higher-level diversity. Journal of Vertebrate Paleontology 30:311–321.Google Scholar
O’Connor, J. K., Chiappe, L. M., and Bell, A.. 2011. Pre-modern birds: avian divergences in the Mesozoic. Pp. 39–114 in G. Dyke, and G. Kaiser, eds. Living dinosaurs. Wiley-Blackwell, Oxford.Google Scholar
Packard, G. C., Boardman, T. J., and Birchard, G. F.. 2009. Allometric equations for predicting body mass of dinosaurs. Journal of Zoology 279:102–110.Google Scholar
Pennycuick, C. J. 2008. Modelling the flying bird (AP Theoretical Ecology Series) Elsevier-Academic Press, Oxford.Google Scholar
Peters, W. S., and Peters, D. S.. 2009. Life history, sexual dimorphism and “ornamental” feathers in the Mesozoic bird Confuciusornis sanctus . Biology Letters 5:817–882.CrossRefGoogle ScholarPubMed
Prum, R. O., Berv, J. S., Dornburg, A., Field, D. J., Townsend, J. P., Lemmon, E. M., and Lemmon, A. R.. 2015. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–577.Google Scholar
Quinn, G. P., and Keough, M. J.. 2001. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.Google Scholar
Rando, J. C., Alcover, J. A., and Illera, J. C.. 2010. Disentangling ancient interactions: a new extinct passerine provides insights on character displacement among extinct and extant island finches. PLoS ONE 5:e12956.CrossRefGoogle ScholarPubMed
Rawlings, J. O., Pantula, S. G., and Dickey, D. A.. 1998. Applied regression analysis; a research tool. Springer -Verlag, N.Y.Google Scholar
Rayner, J. M. 1988. Form and function in avian flight. Current Ornithology 5:1–66.Google Scholar
Revell, L. J. 2010. Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution 1:319–329.Google Scholar
Rohlf, F. J. 2016. TPSDig2, Version 2.26. http://life.bio.sunysb.edu/morph.Google Scholar
Sanz, J. L., Bonaparte, J. F., and Lacasa, A.. 1988. Unusual early Cretaceous birds from Spain. Nature 331:433–435.Google Scholar
Sanz, J. L., Chiappe, L. M., and Buscalioni, A. D.. 1995. The osteology of Concornis lacustris (Aves, Enantiornithes) from the Lower Cretaceous of Spain and a reexamination of its phylogenetic relationships. American Museum Novitates 3133.Google Scholar
Sanz, J. L., Chiappe, L. M., Pérez-Moreno, B. P., Buscalioni, A. D., Moratalla, J. J., Ortega, F., and Poyato-Ariza, F. J.. 1996. An Early Cretaceous bird from Spain and its implications for the evolution of avian flight. Nature 382:442–444.Google Scholar
Sanz, J. L., Álvarez, J. C., Soriano, C., Hernández-Carrasquilla, F., Pérez-Moreno, B., and Meseguer, J.. 2002. Wing loading in primitive birds. Pp. 253–258. in Z. Zhou, and F. Zhang, eds. Proceedings of the Fifth Symposium of the Society of Avian Paleontology and Evolution. Science Press, Beijing.Google Scholar
Senter, P. 2006. Scapular orientation in theropods and basal birds, and the origin of flapping flight. Acta Palaeontologica Polonica 51:305.Google Scholar
Serrano, F. J., Palmqvist, P., and Sanz, J. L.. 2015. Multivariate analysis of neognath skeletal measurements: implications for body mass estimation in Mesozoic birds. Zoological Journal of the Linnean Society 173:929–955.Google Scholar
Simmons, E. L. 2010. Forelimb skeletal morphology and flight mode evolution in pelecaniform birds. Zoology 113:39–46.Google Scholar
Simmons, E. L., Hieronymus, T. L., and O’Connor, P. M.. 2011. Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds. Journal of Morphology 3:958–971.Google Scholar
Smith, R. J. 1984. Allometric scaling in comparative biology: problems of concept and method. American Journal of Physiology Regulatory Integrative and Comparative Physiology 246:152–160.CrossRefGoogle ScholarPubMed
Smith, R. J. 1993. Logarithmic transformation bias in allometry. American Journal of Physiological Anthropology 90:215–228.CrossRefGoogle Scholar
Smith, R. J. 2002. Lead review: estimation of body mass in paleontology. Journal of Human Evolution 43:271–287.CrossRefGoogle Scholar
Smith, R. J. 2009. Use and misuse of the reduced major axis for line-fitting. American. Journal of Physiological Anthropology 140:476–486.Google Scholar
Snowdon, P. 1991. A ratio estimator for bias correction in logarithmic regressions. Canadian Journal of Forest Research 21:720–724.Google Scholar
Sokal, R. R., and Rohlf, J. F.. 1986. Introduction to biostatistics. Freeman, San Francisco.Google Scholar
Tennekes, H. 2009. The simple science of flight: from insects to jumbo jets. MIT Press, Cambridge.Google Scholar
Videler, J. J. 2005. Avian flight. Oxford Ornithology Series. Oxford University Press. Oxford.Google Scholar
Viscor, G., and Fuster, J. F.. 1987. Relationships between morphological parameters in birds with different flying habits. Comparative Biochemistry and Physiology A 87:231–249.Google Scholar
Wang, X., Nudds, R. L., and Dyke, G. J.. 2011. The primary feather lengths of early birds with respect to avian wing shape evolution. Journal of Evolutionary Biology 24:1226–1231.CrossRefGoogle ScholarPubMed
Wang, X., Nudds, R. L., Palmer, C., and Dyke, G. J.. 2012. Size scaling and stiffness of avian primary feathers: implications for the flight of Mesozoic birds. Journal of Evolutionary Biology 25:547–555.Google Scholar
Wellnhofer, P. 2008. Archaeopteryx, der urvogel von Solnhofen. Verlag Dr. Friedrich Pfeil, München.Google Scholar
Yalden, D. W. 1971. The flying ability of Archaeopteryx . Ibis 113:349–356.Google Scholar
Yalden, D. W. 1984. What size was Archaeopteryx? Zoological Journal of the Linnean Society 82:177–188.Google Scholar
You, H. L., Lamanna, M. C., Harris, J. D., Chiappe, L. M., O’Connor, J. M., Ji, S., Jun-chang, L., Chong-xi, Y., Da-qing, L., Xing, Z., Lacovara, K.J., Dodson, P., and Ji, Q.. 2006. A nearly modern amphibious bird from the Early Cretaceous of northwestern China. Science 312:1640–1643.Google Scholar
Zhang, F., and Zhou, Z.. 2000. A primitive enantiornithine bird and the origin of feathers. Science 290:1955–1959.Google Scholar
Zhang, F., Zhou, Z., and Benton, M. J.. 2008. A primitive confuciusornithid bird from China and its implications for early avian flight. Science in China D: Earth Sciences 51:625–639.Google Scholar
Zhou, Z., and Zhang, F.. 2002. A long-tailed, seed-eating bird from the Early Cretaceous of China. Nature 418:405–409.Google Scholar
Zhou, Z., and Zhang, F.. 2003. Anatomy of the primitive bird Sapeornis chaoyangensis from the Early Cretaceous of Liaoning, China. Canadian Journal of Earth Sciences 40:731–747.Google Scholar
Zhou, Z., Chiappe, L. M., and Zhang, F.. 2005. Anatomy of the Early Cretaceous bird Eoenantiornis buhleri (Aves: Enantiornithes) from China. Canadian Journal of Earth Sciences 42:1331–1338.Google Scholar
Zhou, Z., Zhang, F., and Li, Z. H.. 2009. A new basal ornithurine bird (Jianchangornis microdonta gen. et sp. nov.) from the Lower Cretaceous of China. Vertebrata PalAsiatica 47:299–310.Google Scholar