Abstract
The Oligo-Miocene flamingo Harrisonavis croizeti represents an intermediate form between the highly specialized extant flamingo cranial morphology and the more generalized ancestral phoenicopteriform one, characterized by the extinct taxon Palaelodus. However, the original description of H. croizeti lacked detail and the lectotypic skull was lost; thus, it is not known how the ancestral phoenicopterid cranial morphology differed from that of recent forms. Here, we describe new cranial material from Oligo-Miocene deposits of France, including a mostly complete skull with an articulated upper bill, a disarticulated upper bill, and pieces of lower bill. We assign this material to H. croizeti and compare it to all previously reported fossil flamingo cranial material as well as to all six living species. We also use 3D computed tomographic data to reconstruct the skull of H. croizeti in three dimensions. The skull and bill of H. croizeti are similar to those of living species, although they display less specialized filter feeding traits, including a straighter bill with less surface area for filtration lamellae and points of articulation with the lower bill which are less developed. The less specialized form of H. croizeti suggests the extant Phoenicopterus retains a skull morphology more similar to the ancestral condition of crown group flamingos, and the extant Phoenicoparrus form is more derived.
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References
Baumel, J. J., & Witmer, L. M. (1993). Osteologia. In J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, & J. C. Vanden Berge (Eds.), Handbook of avian anatomy (2nd ed., pp. 45–132). Cambridge, Massachusetts: Nuttall Ornithological Club.
Cheneval, J. (1984). Les oiseaux aquatiques (Gaviiformes a Anseriformes) du gisement aquitanien de Saint-Gerand-le-Puy (Allier, France): revision systematique. Palaeovertebrata, 14(2), 33–115.
Cheneval, J., & Escuillie, F. (1992). New data concerning Palaelodus ambiguus (Aves: Phoenicopteriformes: Palaelodidae): ecological and evolutionary interpretations. Natural History Museum of Los Angeles County, Science Series, 36, 209–224.
De Pietri, V. L., Costeur, L., Guntert, M., & Mayr, G. (2011). A revision of the Lari (Aves, Charadriiformes) from the early Miocene of Saint-Gérand-le-Puy (Allier, France). Journal of Vertebrate Paleontology, 31(4), 812–828.
Del Hoyo, J. (1992). Family Phoenicopteridae (Flamingos). In J. del Hoyo, A. Elliott, & J. Sargatal (Eds.), Handbook of the Birds of the World (Vol. 1, pp. 507–526). Barcelona, Spain: Lynx Edicions.
Furbringer, M. (1888). Untersuchungen zur Morphologie und Systematik der Vogel (Vols. 1-2). Amsterdam: von Holkema.
Gervais, P. (1852). Zoologie et Paleontologie Francaise (Vols. 1-3). Paris, France: Arthus Bertrand.
Harrison, C. J. O., & Walker, C. A. (1976). Cranial material of Oligocene and Miocene flamingos: with a description of new species from Africa. Bulletin of the British Museum (Natural History), Geology, 27(4), 305–314.
Jenkin, P. M. (1957). The filter-feeding and food of flamingos (Phoenicopteri). Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 240(674), 401–493.
Kashin, G. N. (1978). The replacement of a preoccupied generic name in class Aves. Paleontologicheskij Zhurnal, 12(1), 145–146.
Linnaeus, C. (1758). Systema Naturae (10th ed. Vols. 1-2, Vol. 1). Holmiae: Laurentii Salvii.
Mayr, G. (2009). Paleogene Fossil Birds. Springer.
Mayr, G. (2014a). The Eocene Juncitarsus—its phylogenetic position and significance for the evolution and higher-level affinities of flamingos and grebes. Comptes Rendus Palevol, 13, 9–18. Accessed 16 December 2014.
Mayr, G. (2014b). Cranial and vertebral morphology of the straight-billed Miocene phoenicopteriform bird Palaelodus and its evolutionary significance. Zoologischer Anzeiger. doi:10.1016/j.jcz.2014.10.002.
Milne-Edwards, A. (1863). Memoire sur la distribution geologique des oiseaux fossiles et description de quelques especes nouvelles. Annales des Sciences Naturelles, 4(20), 133–176.
Mlikovsky, J. (2002). Cenozoic birds of the world. Part 1: Europe. Prague, Czech Republic: Ninox Press.
Olson, S. L., & Feduccia, A. (1980). Relationships and evolution of flamingos (Aves: Phoenicopteridae). Smithsonian Contributions to Zoology, 316, 1–84.
Sangster, G. (2005). A name for the flamingo-grebe clade. Ibis, 147(3), 612–514.
Sibley, C. G., & Ahlquist, J. E. (1990). Phylogeny and classification of birds: a study in molecular evolution. New Haven, Connecticut: Yale University Press.
Torres, C. R., Ogawa, L. M., Gillingham, M. A. F., Ferrari, B., & van Tuinen, M. (2014). A multi-locus inference of the evolutionary diversification of extant flamingos (Phoenicopteridae). BMC Evolutionary Biology, 14(36).
Tumarkin-Deratzian, A. R., Vann, D. R., & Dodson, P. (2006). Bone surface texture as an ontogenetic indicator in long bones of the Canada goose Branta canadensis (Anseriformes: Anatidae). Zoological Journal of the Linnean Society, 148, 133–168.
Uys, C. J., Broekhaysen, G. J., Martin, J., & MacLeod, J. G. (1963). Observations on the breeding of the greater flamingo Phoenicopterus ruber Linnaeus in the Bredasdorp district, South Africa. Ostrich, 34(4), 129–154.
Vanden Berge, J. C., & Zweers, G. A. (1993). Myologia. In J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, & J. C. Vanden Berge (Eds.), Handbook of avian anatomy (2nd ed., pp. 189–247). Cambridge, Massachusetts: Nuttall Ornithological Club.
Worthy, T. H., Tennyson, A. J. D., Archer, M., & Scofield, R. P. (2010). First record of Palaelodus (Aves: Phoenicopteriformes) from New Zealand. Records of the Australian Museum, 62, 77–88.
Watanabe, J., & Matsuoka, H. (2013). Ontogenetic change of morphology and surface texture of long bones in the Gray Heron (Ardea cinerea, Ardeidae). In U. B. Gohlich & A. Kroh (Eds.), Proceedings of the 8th International Meeting of the Society of Avian Paleontology and Evolution (pp. 279–306). Vienna: Verlag Naturhistorisches Museum Wien.
Wattinne, A. (1999). Organisation de la sédimentation carbonatée stromatolitique sur le horst de Saint-Germain (Limagne Bourbonnaise) : exemple des dépôts aquitaniens de la carrière de Montaigu-le-Blin. Mémoire de Géologue de l’IGAL, 123, 1–230.
Zweers, G., de Jong, F., & van den Berge, J. C. (1995). Filter feeding in flamingos (Phoenicopterus ruber). The Condor, 97(2), 297–324.
Acknowledgments
We thank the following individuals for specimen access: D. Berthet (Museé des Confluences, Lyon, France), S. Chapman (Natural History Museum, London, UK), L. Costeur (Natural History Museum, Basel, Switzerland), J. Gerwin (North Carolina Museum of Natural Sciences, Raleigh, NC, USA), C. Milenski (National Museum of Natural History, Washington, DC, USA), A Prieur and E. Robert (Faculté des Sciences de Lyon, Villeurbane, France), and F. Vigouroux (Museé des Confluences, Lyon, France). We thank the following individuals for aid with collection of CT data: C. Charles (ENS de Lyon, Lyon, France), J. Hinton (National Museum of Natural History, Washington, DC, USA), S. Robinson (North Carolina State University, Raleigh, NC, USA), and G. Schultz (University of Basel, Basel, Switzerland). For helpful discussion, we thank J. Clarke (University of Texas at Austin, Austin, TX, USA), S. Emslie (University of North Carolina at Wilmington, Wilmington, NC, USA), D. Ksepka (North Carolina State University, Raleigh, NC, USA), G. Mayr (Senckenberg Museum, Frankfurt, Germany), and T. Worthy (Flinders University, Adelaide, Australia). We thank three anonymous reviewers for comments on the manuscript.
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Torres, C.R., De Pietri, V.L., Louchart, A. et al. New cranial material of the earliest filter feeding flamingo Harrisonavis croizeti (Aves, Phoenicopteridae) informs the evolution of the highly specialized filter feeding apparatus. Org Divers Evol 15, 609–618 (2015). https://doi.org/10.1007/s13127-015-0209-7
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DOI: https://doi.org/10.1007/s13127-015-0209-7