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Estimating the effects of sampling biases on pterosaur diversity patterns: implications for hypotheses of bird/pterosaur competitive replacement

Published online by Cambridge University Press:  08 April 2016

Richard J. Butler
Affiliation:
Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. E-mail: p.barrett@nhm.ac.uk
Paul M. Barrett
Affiliation:
Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. E-mail: p.barrett@nhm.ac.uk
Stephen Nowbath
Affiliation:
Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, United Kingdom. E-mail: P.Upchurch@ucl.ac.uk
Paul Upchurch
Affiliation:
Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, United Kingdom. E-mail: P.Upchurch@ucl.ac.uk

Abstract

Pterosaurs were the first flying vertebrates and formed important components of terrestrial and marginal marine ecosystems during the Mesozoic. They became extinct during the latest Cretaceous (latest Maastrichtian), at, or near, the Cretaceous/Paleogene boundary, following an apparent decline in diversity in the Late Cretaceous. This reduction in species richness has been linked to the ecological radiation of birds in the Early Cretaceous and the proposal that birds competitively excluded pterosaurs from many key niches. However, although competition is often posited as a causal mechanism for many of the clade-clade replacements observed in the fossil record, these hypotheses are rarely tested. Here we present a detailed examination of pterosaur diversity through time, including both taxic and phylogenetically corrected diversity estimates and comparison of these estimates with a model describing temporal variation in the number of pterosaur-bearing formations (a proxy for rock availability). Both taxic and phylogenetic diversity curves are strongly correlated with numbers of pterosaur-bearing formations, suggesting that a significant part of the signal contained within pterosaur diversity patterns may be controlled by geological and taphonomic megabiases rather than macroevolutionary processes. There is no evidence for a long-term decline in pterosaur diversity through the Cretaceous, although a reduction in morphological, ecological, and phylogenetic diversity does appear to have occurred in the latest Cretaceous. Competitive replacement of pterosaurs by birds is difficult to support on the basis of diversity patterns.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alroy, J., Aberhan, M., Bottjer, D. J., Foote, M., Fürsich, F. T., Harries, P. J., Hendy, A. J. W., Holland, S. M., Ivany, L. C., Kiessling, W., Kosnik, M. A., Marshall, C. R., McGowan, A. J., Miller, A. I., Olszewski, T. D., Patzkowsky, M. E., Peters, S. E., Villier, L., Wagner, P. J., Bonuso, N., Borkow, P. S., Brenneis, B., Clapham, M. E., Fall, L. M., Ferguson, C. A., Hanson, V. L., Krug, A. Z., Layou, K. M., Leckey, E. H., Nürnberg, S., Powers, C. M., Sessa, J. A., Simpson, C., Tomašových, A., and Visaggi, C. C. 2008. Phanerozoic trends in the global diversity of marine invertebrates. Science 321:97100.Google Scholar
Andres, B., and Ji, Q. 2008. A new pterosaur from the Liaoning Province of China, the phylogeny of the Pterodactyloidea, and convergence in their cervical vertebrae. Palaeontology 51:453469.Google Scholar
Averianov, A. O. 2007. New records of azhdarchids (Pterosauria, Azhdarchidae) from the Late Cretaceous of Russia, Kazakhstan, and Central Asia. Paleontological Journal 41:189197.Google Scholar
Barrett, P. M., Page, V., and McGowan, A. J. 2007. Dinosaur diversity through time: the influence of the rock record. Journal of Vertebrate Paleontology 27(Suppl.):44A.Google Scholar
Barrett, P. M., Butler, R. J., Edwards, N. P., and Milner, A. R. 2008. Pterosaur distribution in time and space: an atlas. Zitteliana B 28:61107.Google Scholar
Bennett, S. C. 1995. A statistical study of Rhamphorhynchus from the Solnhofen Limestone of Germany: year-classes of a single large species. Journal of Paleontology 69:569580.CrossRefGoogle Scholar
Bennett, S. C. 1996. Year-classes of pterosaurs from the Solnhofen Limestone of Germany: taxonomic and systematic implications. Journal of Vertebrate Paleontology 16:432444.CrossRefGoogle Scholar
Benton, M. J. 1995. Diversification and extinction in the history of life. Science 268:5258.Google Scholar
Benton, M. J. 1996. On the nonprevalence of competitive replacement in the evolution of tetrapods. Pp. 185210in Jablonski, D., Erwin, D. H., and Lipps, J. H., eds. Evolutionary paleobiology. University of Chicago Press, Chicago.Google Scholar
Benton, M. J., and Emerson, B. C. 2007. How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology 50:2340.Google Scholar
Buffetaut, E. 1995. The importance of “Lagerstätten” for our understanding of the evolutionary history of certain groups of organisms: the case of pterosaurs. II International symposium on lithographic limestones (Lleida-Cuenca, Spain, 9–16 July 1995), Extended abstracts, pp. 4952. Ediciones de la Universidad Autónoma de Madrid, Madrid.Google Scholar
Buffetaut, E., Clarke, J. B., and Le Loeuff, J. 1996. A terminal Cretaceous pterosaur from the Corbières (southern France) and the problem of pterosaur extinction. Bulletin de la Société Géologique de France 167:753759.Google Scholar
Buffetaut, E., Laurent, Y., Le Loeuff, J., and Bilotte, M. 1997. A terminal Cretaceous giant pterosaur from the French Pyrenees. Geological Magazine 134:553556.Google Scholar
Carrano, M. 2008. Patterns of diversity among latest Cretaceous dinosaurs in North America. Journal of Vertebrate Paleontology 28(Suppl.):61A.Google Scholar
Colbert, E. H. 1980. Evolution of the vertebrates. Wiley Interscience, New York.Google Scholar
Crampton, J. S., Beu, A. G., Cooper, R. A., Jones, C. M., Marshall, B., and Maxwell, P. A. 2003. Estimating the rock volume bias in paleobiodiversity studies. Science 301:358360.Google Scholar
Dalla Vecchia, F. M. 2006. The tetrapod fossil record from the Norian-Rhaetian of Friuli (northeastern Italy). In Harris, J. D., Lucas, S. G., Spielmann, J. A., Lockley, M. G., Milner, A. R. C., and Kirkland, J. I., eds. The Triassic-Jurassic terrestrial transition. New Mexico Museum of Natural History and Science Bulletin 37:432444.Google Scholar
Davies, T. J., Meiri, S., Barraclough, T. G., and Gittleman, J. L. 2007. Species co-existence and character divergence across carnivores. Ecology Letters 10:146152.Google Scholar
Fountaine, T. M. R., Benton, M. J., Dyke, G. J., and Nudds, R. L. 2005. The quality of the fossil record of Mesozoic birds. Proceedings of the Royal Society B 272:289294.Google Scholar
Hammer, O., Harper, D. A. T., and Ryan, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1), Article 4.Google Scholar
Hardin, G. 1960. The competitive exclusion principle. Science 131:12921297.Google Scholar
Henderson, M. D., and Peterson, J. E. 2006. An azhdarchid pterosaur cervical vertebra from the Hell Creek Formation (Maastrichtian) of southeastern Montana. Journal of Vertebrate Paleontology 26:192195.Google Scholar
Hone, D. W. E., and Benton, M. J. 2007. Cope's Rule in the Pterosauria, and differing perceptions of Cope's Rule at different taxonomic levels. Journal of Evolutionary Biology 20:11641170.Google Scholar
Kellner, A. W. A. 2003. Pterosaur phylogeny and comments on the evolutionary history of the group. In Buffetaut, E. and Mazin, J.-M., eds. Evolution and paleobiology of pterosaurs. Geological Society of London Special Publication 217:105137.Google Scholar
Lloyd, G. T., Davis, K. E., Pisani, D., Tarver, J. E., Ruta, M., Sakamoto, M., Hone, D. W. E., Jennings, R., and Benton, M. J. 2008. Dinosaurs and the Cretaceous terrestrial revolution. Proceedings of the Royal Society of London B 275:24832490.Google Scholar
, J., and Ji, Q. 2006. Preliminary results of a phylogenetic analysis of the pterosaurs from western Liaoning and surrounding areas. Journal of the Paleontological Society of Korea 22:239261.Google Scholar
Martill, D. M., and Naish, D. 2006. Cranial crest development in the azhdarchoid pterosaur Tupuxuara, with a review of the genus and tapejarid monophyly. Palaeontology 49:925941.Google Scholar
McGowan, A. J., and Dyke, G. J. 2007. A morphospace-based test for competitive exclusion among flying vertebrates: did birds, bats and pterosaurs get in each others space? Journal of Evolutionary Biology 20:12301236.Google Scholar
McGowan, A. J., and Smith, A. B. 2008. Are global Phanerozoic marine diversity curves truly global? A study of the relationship between regional rock records and global Phanerozoic marine diversity. Paleobiology 34:80103.Google Scholar
Miller, K. G., Kominz, M. A., Browning, J. V., Wright, J. D., Mountain, G. S., Katz, M. E., Sugarman, P. J., Cramer, B. S., Christie-Blick, N., and Pekar, S. F. 2005. The Phanerozoic record of global sea-level change. Science 310:12931298.Google Scholar
Norell, M. A. 1992. The effect of phylogeny on temporal diversity and evolutionary tempo. Pp. 89118in Novacek, M. J. and Wheeler, Q. D., eds. Extinction and phylogeny. Columbia University Press, New York.Google Scholar
Nudds, R. L., Dyke, G. J., and Rayner, J. M. V. 2004. Forelimb proportions and the evolutionary radiation of Neornithes. Biology Letters 271:S324S327.Google Scholar
Penny, D., and Phillips, M. J. 2004. The rise of birds and mammals: are microevolutionary processes sufficient for macroevolution? Trends in Ecology and Evolution 19:516522.Google Scholar
Peters, S. E. 2005. Geological constraints on the macroevolutionary history of marine animals. Proceedings of the National Academy of Sciences USA 102: 12326–2331.CrossRefGoogle ScholarPubMed
Peters, S. E., and Foote, M. 2001. Biodiversity in the Phanerozoic: a reinterpretation. Paleobiology 27:583601.Google Scholar
Price, L. I. 1953. A presença de pterosauria no Cretáceo Superior do estado da Paraíba. Notas Preliminares e Estudos, Divisao de Geologia e Mineralogia, Brasil 71:110.Google Scholar
Reitz, S. R., and Trumble, J. T. 2002. Competitive displacement among insects and arachnids. Annual Review of Entomology 47:436465.Google Scholar
Romer, A. S. 1966. Vertebrate paleontology. University of Chicago Press, Chicago.Google Scholar
Sepkoski, J. J. Jr. 1996. Competition in macroevolution: the double wedge revisited. Pp. 211255in Jablonski, D., Erwin, D. H., and Lipps, J. H., eds. Evolutionary paleobiology. University of Chicago Press, Chicago.Google Scholar
Sepkoski, J. J. Jr., Bambach, R. K., Raup, D. M., and Valentine, J. W. 1981. Phanerozoic marine diversity and the fossil record. Nature 293:435437.Google Scholar
Slack, K. E., Jones, C. M., Ando, T., Harrison, G. L., Fordyce, R. E., Arnason, U., and Penny, D. 2006. Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution. Molecular Biology and Evolution 23:11441155.CrossRefGoogle ScholarPubMed
Smith, A. B. 1994. Systematics and the fossil record. Blackwell Scientific, Oxford.Google Scholar
Smith, A. B., and McGowan, A. J. 2007. The shape of the Phanerozoic palaeodiversity curve: how much can be predicted from the sedimentary rock record of Western Europe? Palaeontology 50:765774.Google Scholar
Unwin, D. M. 1987. Pterosaur extinction: nature and causes. Mémoires de la Société géologique de France, n.s. 150:105111.Google Scholar
Unwin, D. M. 1988. Extinction and survival in birds. Pp. 295318in Larwood, G. P., ed. Extinction and survival in the fossil record. Clarendon, Oxford.Google Scholar
Unwin, D. M. 2003. On the phylogeny and evolutionary history of pterosaurs. Geological Society of London Special Publication 217:139190.Google Scholar
Unwin, D. M. 2005. The pterosaurs from deep time. Pi Press, New York.Google Scholar
Upchurch, P., and Barrett, P. M. 2005. Phylogenetic and taxic perspectives on sauropod diversity. Pp. 104124in Curry Rogers, K. A. and Wilson, J. A., eds. The sauropods: evolution and paleobiology. University of California Press, Berkeley.Google Scholar
Valentine, J. W. 1969. Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Palaeontology 12:684709.Google Scholar
Wang, S. C., and Dodson, P. 2006. Estimating the diversity of dinosaurs. Proceedings of the National Academy of Sciences USA 103:1360113605.Google Scholar
Wang, X.-L., Kellner, A. W. A., Zhou, Z.-H., and Campos, D. de. A. 2005. Pterosaur diversity and faunal turnover in Cretaceous terrestrial ecosystems in China. Nature 437:875879.Google Scholar
Weishampel, D. B., Barrett, P. M., Coria, R. A., Le Loeuff, J., Xu, X., Zhao, X., Sahni, A., Gomani, E. M. P., and Noto, C. R. 2004. Dinosaur distribution. Pp. 517606in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria, 2d ed.University of California Press, Berkeley.Google Scholar
Wellnhofer, P. 1991. The illustrated encyclopedia of pterosaurs. Salamander Books, London.Google Scholar
Wessa, P. 2008. Free statistics software. Office for Research Development and Education, Version 1.1.22-r4, http://www.wessa.net/Google Scholar
Witton, M. P., and Naish, D. 2008. A reappraisal of azhdarchid pterosaur functional morphology and paleoecology. PLoS ONE 3(5):e2271. doi: 10.1371/journal.pone.0002271Google Scholar