We report avian cervical vertebrae from the Quercy fissure fillings in France, which are densely covered with villi-like tubercles. Two of these vertebrae stem from a late Eocene site, another lacks exact stratigraphic data. Similar cervical vertebrae occur in avian species from Eocene fossils sites in Germany and the United Kingdom, but the new fossils are the only three-dimensionally preserved vertebrae with pronounced surface sculpturing. So far, the evolutionary significance of this highly bizarre morphology, which is unknown from extant birds, remained elusive, and even a pathological origin was considered. We note the occurrence of similar structures on the skull of the extant African rodent Lophiomys and detail that the tubercles represent true osteological features and characterize a distinctive clade of Eocene birds (Perplexicervicidae). Micro-computed tomography (μCT) shows the tubercles to be associated with osteosclerosis of the cervical vertebrae, which have a very thick cortex and much fewer trabecles and pneumatic spaces than the cervicals of most extant birds aside from some specialized divers. This unusual morphology is likely to have served for strengthening the vertebral spine in the neck region, and we hypothesize that it represents an anti-predator adaptation against the craniocervical killing bite ("neck bite") that evolved in some groups of mammalian predators. Tuberculate vertebrae are only known from the Eocene of Central Europe, which featured a low predation pressure on birds during that geological epoch, as is evidenced by high numbers of flightless avian species. Strengthening of the cranialmost neck vertebrae would have mitigated attacks by smaller predators with weak bite forces, and we interpret these vertebral specializations as the first evidence of "internal bony armor" in birds.

Central Research Laboratories Natural History Museum Vienna Vienna Austria

CR2P Centre de recherche en Paléontologie CNRS MNHN Sorbonnes Université Bâtiment de Géologie Paris France

Department of Palaeobiology Institute of Geology Czech Academy of Sciences Prague 6 Czech Republic

Geological Paleontological Department Natural History Museum Vienna Vienna Austria

Institute of Systematics and Evolution of Animals Polish Academy of Sciences Kraków Poland

Ornithological Section Senckenberg Research Institute and Natural History Museum Frankfurt Frankfurt am Main Germany

Zobrazit více v PubMed

Báez, A.M. & Rage, J.‐C. (1998) Pipid frogs from the upper Cretaceous of in Beceten, Niger. Palaeontology, 41, 669–691.

Böhme, M. (2008) Ectothermic vertebrates (Teleostei, Allocaudata, Urodela, Anura, Testudines, Choristodera, Crocodylia, Squamata) from the upper Oligocene of Oberleichtersbach (northern Bavaria, Germany). Courier Forschungsinstitut Senckenberg, 260, 161–183.

Broeckhoven, C. , Diedericks, G. & Mouton, P.L.F.N. (2015) What doesn't kill you might make you stronger: functional basis for variation in body armour. Journal of Animal Ecology, 84, 1213–1221. PubMed

Cuthbert, R. (2003) Sign left by introduced and native predators feeding on Hutton's shearwaters Puffinus huttoni . New Zealand Journal of Zoology, 30, 163–170.

de Buffrénil, V. , Rage, J.‐C. , Dauphin, Y. & Sire, J.‐Y. (2011) An enamel‐like tissue, osteodermine, on the osteoderms of a fossil anguid (Glyptosaurinae) lizard. Comptes Rendus Palevol, 10, 427–438.

Eisenberg, J.F. & Leyhausen, P. (1972) The phylogenesis of predatory behavior in mammals 1. Zeitschrift für Tierpsychologie, 30, 59–93. PubMed

Fajardo, R.J. , Hernandez, E. & O'Connor, P.M. (2007) Postcranial skeletal pneumaticity: a case study in the use of quantitative microCT to assess vertebral structure in birds. Journal of Anatomy, 211, 138–147. PubMed PMC

Gardner, J.D. (2012) Revision of Piceoerpeton Meszoely (Caudata: Scapherpetontidae) and description of a new species from the late Maastrichtian and ?Early Paleocene of western North America. Bulletin de la Société Géologique de France, 183, 611–620.

Georgalis, G.L. , Čerňanský, A. & Klembara, J. (2021) Osteological atlas of new lizards from the Phosphorites du Quercy (France), based on historical, forgotten, fossil material. Geodiversitas, 43, 219–293.

Georgalis, G.L. , Prendini, E. & Roček, Z. (2023) New information on the Eocene frog Thaumastosaurus (Anura, Pyxicephalidae) from the Phosphorites du Quercy, France. Zoological Journal of the Linnean Society, 199, 744–770.

Georgalis, G.L. , Rabi, M. & Smith, K.T. (2021) Taxonomic revision of the snakes of the genera Palaeopython and Paleryx (Serpentes, Constrictores) from the Paleogene of Europe. Swiss Journal of Palaeontology, 18, 140.

Glynne, E. , Daza, J.D. & Bauer, A.M. (2020) Surface sculpturing in the skull of gecko lizards (Squamata: Gekkota). Biological Journal of the Linnean Society, 131, 801–813.

Gutzwiller, S.C. , Su, A. & O’Connor, P.M. (2013) Postcranial pneumaticity and bone structure in two clades of neognath birds. The Anatomical Record, 296, 867–876. PubMed

Hilton, G.M. & Cuthbert, R.J. (2010) The catastrophic impact of invasive mammalian predators on birds of the UK overseas territories: a review and synthesis. Ibis, 152, 443–458.

Ivanov, M. (2008) Early Miocene amphibians (Caudata, Salientia) from the Mokrá‐Western quarry (Czech Republic) with comments on the evolution of early Miocene amphibian assemblages in Central Europe. Geobios, 41, 465–492.

Jansen, M. , Álvarez, L.G. & Koehler, G. (2009) Description of a new species of Xenopholis (Serpentes: Colubridae) from the Cerrado of Bolivia, with comments on Xenopholis scalaris in Bolivia. Zootaxa, 2222, 31–45.

Kingdon, J. , Agwanda, B. , Kinnaird, M. , O'Brien, T. , Holland, C. , Gheysens, T. et al. (2012) A poisonous surprise under the coat of the African crested rat. Proceedings of the Royal Society B: Biological Sciences, 279, 675–680. PubMed PMC

Lazagabaster, I.A. , Rovelli, V. , Fabre, P.H. , Porat, R. , Ullman, M. , Davidovich, U. et al. (2021) Rare crested rat subfossils unveil afro–Eurasian ecological corridors synchronous with early human dispersals. Proceedings of the National Academy of Sciences, 118, e2105719118. PubMed PMC

Leyhausen, P. (1965) Über die Funktion der relativen Stimmungshierarchie (dargestellt am Beispiel der phylogenetischen und ontogenetischen Entwicklung des Beutefangs von Raubtieren). Zeitschrift für Tierpsychologie, 22, 412–494. PubMed

Lyver, P.O.B. (2000) Identifying mammalian predators from bite marks: a tool for focusing wildlife protection. Mammal Review, 30, 31–44.

Mayr, G. (2007) Bizarre tubercles on the vertebrae of Eocene fossil birds indicate an avian disease without modern counterpart. Naturwissenschaften, 94, 681–685. PubMed

Mayr, G. (2010) A new avian species with tubercle‐bearing cervical vertebrae from the Middle Eocene of Messel (Germany). In: Boles, W.E. & Worthy, T.H. (Eds.) Proceedings of the VII international meeting of the Society of Avian Paleontology and Evolution. Records of the Australian Museum, Vol. 62. Sydney: Australian Museum, pp. 21–28.

Mayr, G. (2022) Paleogene fossil birds, 2nd edition. Cham: Springer.

Mayr, G. , Carrió, V. & Kitchener, A.C. (2023) On the “screamer‐like” birds from the British London Clay: an archaic anseriform‐galliform mosaic and a non‐galloanserine “barb‐necked” species of Perplexicervix . Palaeontologia Electronica, 26, a33.

Molnar, J. & Watanabe, A. (2023) Morphological and functional regionalization of trunk vertebrae as an adaptation for arboreal locomotion in chameleons. Royal Society Open Science, 10, 221509. PubMed PMC

Mourer‐Chauviré, C. (2006) The avifauna of the Eocene and Oligocene Phosphorites du Quercy (France): an updated list. Strata, série, 1(13), 135–149.

Muzzopappa, P. , Iori, F.V. , Muniz, F.P. & Martinelli, A.G. (2022) A new species of Baurubatrachus (Anura, Neobatrachia) from the late Cretaceous Adamantina Formation of Brazil furnishes evidence on the diversity of this bizarre genus. Ameghiniana, 59, 297–316.

O'Donnell, C.F. , Clapperton, B.K. & Monks, J.M. (2015) Impacts of introduced mammalian predators on indigenous birds of freshwater wetlands in New Zealand. New Zealand Journal of Ecology, 39, 19–33.

Pélissié, T. , Orliac, M. , Antoine, P.‐O. , Biot, V. & Escarguel, G. (2021) Beyond Eocene and Oligocene epochs: the causses du Quercy geopark and the Grande Coupure. Geoconservation Research, 4, 573–585.

Peters, D.S. (1995) Idiornis tuberculata n. spec., ein weiterer ungewöhnlicher Vogel aus der Grube Messel (Aves: Gruiformes: Cariamidae: Idiornithinae). Courier Forschungsinstitut Senckenberg, 181, 107–119.

Ratz, H. , Moller, H. & Fletcher, D. (1999) Predator identification from bite marks on penguin and albatross chicks. Marine Ornithology, 27, 149–156.

Roček, Z. (1981) Cranial anatomy of frogs of the family Pelobatidae Stannius, 1856, with outlines of their phylogeny and systematics. Acta Universitatis Carolinae, Biologica, 1980, 1–164.

Roček, Z. (1994) Taxonomy and distribution of Tertiary discoglossids (Anura) of the genus Latonia v. Meyer, 1843. Geobios, 27, 717–751.

Roček, Z. (2019) A contribution to the herpetofauna from the late Miocene of Gritsev (Ukraine). Comptes Rendus Palevol, 18, 817–847.

Roček, Z. , Wuttke, M. , Gardner, J.D. & Singh Bhullar, B.A. (2014) The euro‐American genus Eopelobates, and a re‐definition of the family Pelobatidae (Amphibia, Anura). Palaeobiodiversity and Palaeoenvironments, 94, 529–567.

Sargeant, A.B. & Eberhardt, L.E. (1975) Death feigning by ducks in response to predation by red foxes (Vulpes fulva). American Midland Naturalist, 94, 108–119.

Schlüter, T. , Kohring, R. & Mehl, J. (1992) Hyperostotic fish bones (“tilly bones”) from presumably Pliocene phosphorites of the Lake Manyara area, northern Tanzania. Paläontologische Zeitschrift, 66, 129–136.

Smit, T.H. , Odgaard, A. & Schneider, E. (1997) Structure and function of vertebral trabecular bone. Spine, 22, 2823–2833. PubMed

Solé, F. , Fischer, V. , Le Verger, K. , Mennecart, B. , Speijer, R.P. , Peigné, S. et al. (2022) Evolution of European carnivorous mammal assemblages through the Palaeogene. Biological Journal of the Linnean Society, 135, 734–753.

Steklis, H.D. & King, G.E. (1978) The craniocervical killing bite: toward an ethology of primate predatory behavior. Journal of Human Evolution, 7, 567–581.

Syromyatnikova, E.V. (2019) Redescription of Pelobates praefuscus Khosatzky, 1985 and new records of Pelobates from the late Miocene‐Pleistocene of Eastern Europe. Historical Biology, 31, 888–897.

Szyndlar, Z. & Georgalis, G.L. (2023) An illustrated atlas of the vertebral morphology of extant non‐caenophidian snakes, with special emphasis on the cloacal and caudal portions of the column. Vertebrate Zoology, 73, 717–886.

Tapanila, L. , Pruitt, J. , Pradel, A. , Wilga, C.D. , Ramsay, J.B. , Schlader, R. et al. (2013) Jaws for a spiral‐tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion . Biology Letters, 9, 20130057. PubMed PMC