ORYCTOS,VoI.1 : l3l - 136,Octobre 1998

FIRSTEVIDENCE OF ENANTIORNITHINE BIRDS FROM TITE UPPER CRETACEOUS OF EUROPE: POSTCRANIAL BONES FROM CRUZY (HÉRAUTT, SOUTHERN FRANCE)

Eric BUFFBTAUT CNRS,UMR 556I , 16cour du Liégat,75013Paris

Abstract : A coracoid and an incomplete femur from a newly discovered Late Campanian to Early Maastrichtian locality at Cruzy (Hérault, France) are described and identified as the first remains of enantiornithine birds to be reported from the Upper Cretaceousof Europe. This find extends to Europe the already wide known geographical distribution of Late CretaceousEnantiornithes, and confirms the important part played by this peculiar group of birds in avifaunasin many parts of the world until late in the Cretaceous.

Kev words : Aves, Enantiornithes, I-ate Cretaceous. France.

Premiersrestes d'Enantiornithes (Aves)du Crétacésupérieur d'Europe : ossementspost-crâniens trouvés à Cruzy (Hérault, Sud de la France)

Résumé : Un coracoïde et un fémur incomplet provenant d'un nouveau gisement d'âge Campanien supérieur à Maastrichtien inférieur à Cruzy (Hérault, France) sont décrits et identifiés comme les premiers restesd'oiseaux du groupe des Enantiornithes à être signalésdans le Crétacé,supérieur d'Europe. Cette découverteétend à I'Europe la distribution géographiqueconnue déjà vastedes Enantiornithes aluCrétacésupérieur, et confirme que ce groupe par- ticulier d'oiseaux jouait un rôle important dans les avifaunes de nombreusesparties du monde jusque tard dans le Crétacé.

Mots clés : Aves, Enantiornithes, Crétacé supérieur;France.

Résumé français étendu : Les avifaunes du Crétacê supérieur européen demeurent mal connues. Un oiseau de grande taille, incapable de voler, a été décit sousle nom de Gargantuavisphiloinos dans quelquesgisements d'âge Campaniensupérieur à Maastrichtien inférieur du Sud de la France, mais les formes volantes de petite taille étaient jusqu'ici inconnues. Le gisement de Massecaps,récemment découvert près de Cruzy (Hérault), a livré quelques ossementsd'oiseaux, parmi une riche faune de vertébréscomprenant des poissons,des amphibiens,des chéloniens, des squamates,des crocodiliens et des dinosaures. Ces derniers sont représentésnotamment par I'ornithopode Rhabdodon et le sauropodeAmpelosanffus, assemblage qui indique un âge Campanien supérieur à Maastrichtien inférieur. Les oiseaux sont représentéspar un coracoïde et un fragment proximal de fémur, qui montrent tous deux des traits caractéristiquesdu groupe éteint des Enantiornithes. Le coracoïde présenteune grande expansion posté- rieure, et les processusprocoracoïde et latéraux des oiseaux modernes sont absentsà son exffémité antérieure,ce qui est caractéristiquedes Enantiornithes. I1 suggèreun animal de la taille d'un goéland actuel. Le fragment de fémur se caractérisepar une dépressioncaudolatérale marquée, limitée latéralement par ce qui est probablement I'homologue du trochanter postérieur des Dromaeosauridaeet d'Archaeopteryx; il s'agit là encore d'un caractère présent chez les Enantiornithes.A partir du matériel actuellement disponible, on peut dire que I'oiseau de Cruzy appartient très clairement aux Enantiornithes, mais il n'est guère possible de I'identifier plus précisément. En Europe, les Enantiornithes n'étaient jusqu'ici connus que dans le Crêtacé inférieur d'Espagne ; les spécimensde Cruzy constituentla première preuve de leur existenceau,Crétacé supérieur dans cette partie du monde. Cette décou- verte étend à l'Europe l'aire de répartition connue déjà vaste des Enantiornithes au Crétacésupérieur (Amérique du Sud, Amérique du Nord, Asie), et confirme que ces oiseauxjouaient un rôle important dans les avifaunesde nom- breusesparties du monde jusque tard dans le Crétacé.Il n'est donc pas impossible qu'ils aient été victimes de l'ex- tinction en massede la limite Crétacé-Tertiaire.

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INTRODUCTION (Buffetaut et al, 1995; Buffetaut &.Le Loeuff, 1993); smaller flying birds had not yet been reported. The The Late Cretaceous avifauna of Europe i s still discovery of a very distinctive coracoid and a frag- largely unknown. Purported bird bones from the mentary femur at aLate Cretaceousvertebrate locali- Maastrichtian of Transylvania (Harrison 8. Walker, ty at Cruzy near Béziers in southern France now I97 5) are now usually regarded as belonging to troo- reveals that representatives of the peculiar group of dontid dinosaurs (Osmolska & Barsbold, 1990) , Cretaceous birds known as Enantiornithes were pre- although they are in need of a revision in the light of sent in Europe during the Late Cretaceous. recent discoveriesof Cretaceousbirds. As far as sou- thwestern Europe is concerned,Sauvage ( 1897-1898) reported remains of a bird from the Late Cretaceous GEOLOGICALANI) Yizo (also spelled Viso) locality in Portugal, but he PALAEONTOLOGICAL SETTING 'Whether neither described nor illustrated them. this purported bird material consisted of the specimens The fossils described here were found in the from Viso later briefly mentioned (but not figured) as course of systematic excavations at the Massecaps caudal vertebrae of a pterosaur by Lapparent and locality near the village of Cruzy (Hérault, southern Zbyszewski (T957) is uncertain. Pending a revision France), conducted by the Association Culturelle et of the specimens from Viso, nothing definite can be Archéologique Cruziate, the Musée des Dinosaures said about them. So far, the only undisputed record of d'Espéraza, and the Centre National de la Recherche Late Cretaceousbirds from Europe was that of a very Scientifique. This newly discoveredlocality has yiel- large bird known from several specimens from the ded an abundant and diverse vertebrate fauna, which Upper Cretaceous of Provence and Languedoc, includes lepisosteid fish, amphibians, turtles, large which has been described as Gargantuavis philoinos varanid lizards, ornithopod, sauropod and theropod

Figure l. Right coracoid of enantiornithinebird from the Upper Cretaceous(Late Campanian/Early Maastrichtian)of Cruzy (Hérault,F'rance) , Muséede Cruzy,Ml92. A : dorsalview ; B : ventralview ; C : medialview. Scalebar : 20 mm. Photographsby Claude Abrial. Coracoïde droit d'enantiornithe du Crétacésupérieur (Campaniensupérieur I Maastrichtien i nférieur) de Cruzy (Hérault,France), Muséede Cruzy,Ml92. A : vue dorsale; B : vue ventrale; C : vue médiale. Echelle: 20 mm. C Photos: ClaudeAbrial.

r32 BUFFETAUT - FRENCH ENANTIORNITHINE BIRDS dinosaurs, and birds. The bones occur as disarticula- (the acrocoracoid process) is blunt, with a well-mar- ted elements in variegated clays apparently indicative ked groove on its ventrolateral surface. of a fluvial deposit. The dinosaur assemblage,domi- nated by the ornithopod Rhabdodon and the titano- saurid sauropod Ampelosaurus, is that usually found in Late Campanian to Early Maastrichtian vertebrate sites in southern France (Le Læuff et al. 1994 ; Buffetaut &Le Læuff ,, 1997 ; Buffetaut et al., T997). The available bird material, kept at the Cruzy Museuffio consists of a neafly complete coracoid and the proximal end of a femur.

CORACOID

The first bird bone found at Cruzy by Didier Clavel, in 1996, is a fairly well preservedright cora- coid (Cruzy Museum, M192) which exhibits the very peculi ar features characteristic of the Enantiornithes (the recognition of the peculiar character of the Enantiornithes, or <Enantiornis leali (B), from the Maastrichtian of Argentina nerve foramen perforates a medial bony ridge and (mirror image after Walker, 1981). Both specimensin dorsal opens into a groove on the medial surface.This fora- view, brought to the samesize (the coracoidof Enantiornis is in fact about twice the length of the one found at Cruzy). men opens inside the fossa in some enantiornithes, Comparaison entre le coracoïde d'enantiornithe de Cruzy but in the Cruzy specimen it opens outside it, as in (A ; dessin de H. frrg) et le coracoïded'Enantiornis leali Enantiornis leali (Chiappe, L996 a). The anterior part (B), du Maastrichtien d'Argentine (image inversée d'après of the bone lacks the procoracoid and lateral pro- Walker, 1981). Les deux spécimenssont en vue dorsale,et cesses of modern birds ; obviously, the triosseal ramené,sà la même taille (le coracoïded'Enantiornis est en canal, at the junction between the coracoid, the sca- fart à peu près deux fois plus long que celui trouvé à Cruzy). pula and the furcula, was surrounded more by the scapula than by the coracoid, which is a characteris- The bird coracoid from Cruzy is in all respects tic feature of the Enantiornithes (Walker, 1981 ; very similar to previously described enantiornithine Martin, 1995 ; Chiappe, I996b). The contribution of coracoids (V/alker, 1981 ; Martin, 1995 ; Chiappe, the coracoid to the triosseal canal in the Cruzy bird is I996a,b), such as those of Enantiornis leali (see in the form of a notch for the supracoracoideusten- Fig.2), from the Maastrichtian of Argentina (V/alker, don, just anterior to the convex articular facet for the 1981), Neuquenornis volans, from the Coniacian- scapula, and separatedfrom the acrocoracoid process Santonian of Argentina (Chiappe & Calvo, 1994),, by a well-marked tubercle (as in Enantiornis leali : and Concornis lacustris,, from the Barremian of Chiappe, I996a). The anteriormost tip of the bone Spain (Sanz et al., 1995). Its posterior triangular r33 ORYCTOS,Vol. 1, 1998 expansion seems to be somewhat broader than in distinct <>.There may be a small fossa on the Neuquenornis volans and in Nanantius valifanovi, articular head for insertion of the ligamentum capitis from the Upper Cretaceous (probably Late femoris, but this region has undergone some abrasion Campanian) of Mongolia (Kurochkin, 1996), but and details are not easily discernible. Lateral to the figured specimens of the latter seem to be incomple- <>, there is a trochanteric crest, as in other enan- tely preserved in that area. Although the general tiornithines (Chiappe, I996b). The most striking shape is the same, the anterior part of the coracoid enantiornithine character of this fragment is a rather from Cruzy seems to exhibit stronger reliefs than in deep excavation on the caudolateral face of the bone, the enantiornithine Gobipteryx minuta, from the close to its proximal end. This excavation opens cau- Upper Cretaceous of Mongolia (Elzanowski, 1995), dally and is limited ventrolaterully by a sharp border. but the differences may be due to the embryonic This is very similar (Fig.a) to the condition described condition of the latter. The coracoids of the and illustrated by Chiappe and Calvo (1994) in enan- Enantiornithes are very different from those of other tiornithine femora from the Maastrichtian of El Brete birds, but within the group, there seems to be relati- (Argentina). vely little variation. The coracoid from Cruzy is 53 In Neuqltenornis volans, the lateral border mm long, which suggests a bird about the size of a extends farther proximally (Chiappe & Calvo, 1994). herring gull (Larus argenteus). According to Chiappe (I99I, 1996b) and Chiappe and Calvo (1994), this structure is homologous to the posterior trochanter of dromaeosaurids and FEMUR Archaeopteryx, and very well developed in enantior- nithines. A secondbird bone was discoveredat Massecaps at the end of the summer excavationsof 1997. It is the proximal head of a femur (M I93), with only a small CONCLUSIONS portion of the hollow shaft preserved (Fig.3). This specimen shows a well-defined, rounded Although both the coracoid and the femoral frag- articular heîd , which is medially and slightly dorsal- ment from Cruzy exhibit characteristic features of the ly oriented, and separatedfrom the shaft by a a very Enantiornithes, it is difficult to be more specific in

Fig.3. Fig.3. Proximal end of enantiornithine left femur from Cruzy, in cranial (A) and caudal (B) views. Scale bar : 20 mm. Drawing by H. Tong. Extrémité proximale de fémur gauche d'enantiornithe de Cruzy, en vues craniale (A) et caudale(B). Barre d'échelle : 20 mm. Dessin de H. Tong

Fig.4. Proximal ends of enantiornithine left femora, in lateral view, showing the posterior trochanter (arrows). A, B : two enantiornithines from the Maastrichtian Lecho Formation of El Breta, Argentina. C : Neuquenornis volans, from the Coniacian - Santonianof Neuquen,Argentina. D : enantior- Fig.4. nithine femur from Cruzy (Ml93). Not to scale.A,B,C after Chiappe and Calvo (1994). Extrémités proximales de fémurs gauchesd'enantiornithes, en vue lat&ale, montrant le trochanter postérieur (flèches). A,B : deux enantiornithes de Ia Formation Lecho (Maastrichtien) d'El Brete, Argentine. C : Neuquenornis P fr volans, du Coniacien-santoniende Neuquen,Argentine. D : A I B IC D fémur d'enantiornithe de Cruzy (Ml93). Echelles différentes. A,B,C d'aprèsChiappe et Calvo (1994).

134 BUFFETAUT - FRENCH ENANTIORNITHINE BIRDS

their identification. As far as the coracoid is concer- ACKNOWLEDGMENTS ned, the closestresemblances seemto be with that of Enantiornis leali Walker, 1981, a member of the Field work at Cruzy wassupported by the Institut family Enantiornithidae, of the order National des Sciencesde I'Univers (CNRS), the Enantiornithiformes (following Martin's classifi ca- Association Culturelle et Archéologique Cruziate, tion, 1995), or Alexornithiformes (following and the Muséedes Dinosaures (Espéraza). I thank all Kurochkin's classification, 1996), although they are the volunteers who took part in the excavations. clearly not identical (Fig.2),but it may be safer at the Special thanks to all membersof the Association moment to simply refer the bird material from Cruzy Culturelleet ArchéologiqueCruziate, and their pre- to the subclassEnantiornithes, pending the discovery sident FrancisFages for their invaluablehelp. I am of additional material grateful to Angela Milner (The Natural History Previously known European enantiornithine Museuffi,London), for accessto castsin her care,and birds were Concornis, and possibly lberomesornis to Lionel Cavin,Joëlle Salomon and Haiyan Tong for and Noguerornis from the Lower Cretaceousof Spain their help in the first stagesof the identificationof the (see Chiappe, I996b ; Kurochkin, 1996), but the enantiornithinecoracoid from Cruzy. group was so far unknown in the Upper Cretaceousof Europe. The discovery of an enantiornithine bird in the late Campanian or early Maastrichtian of France REFERENCES shows that the group was still present in that part of BUFFETAUT, E. 1996. Birds at the Cretaceous-Tertiaryboundary : the world late in the Cretaceous.It extendsto Europe a hidden mass extinction ? ; pp.I7-I8. In DROBNE, K., GORICAN, S. & KOTNIK, B. The role of impact processesin the known Late Cretaceous distribution of the the geological and biological evolution of planet Earth. Enantiornithes, which were already known from the Znanstv enoraziskovalni center SAZU, Lj ublj ana. Upper Cretaceousof Argentina, Mexico, the United BUFFETAUI E. & LE LOEUFF, J. 1997. Late Cretaceous States, and Central Asia ( see reviews in Martin, dinosaursfrom the foothills of the Pyrenees.Geology Today,13, 1995 ; Kurochkin, 1996), and confirms the very vast 2: 60-68. distribution of this group of birds until late in the 1998. A new giant ground bird from the Upper Cretaceousof southern France. Journal of Mesozoic. In Europe as in many other parts of the the Geological SocieQ,London, 155 : I-4. world (Martin, 1983, 1995;Chiappe, 1995; MECHIN, P. & MECHIN Feduccia, 1996 ; Kurochkin, 1996), enantiornithine SALESSY, A. 1995. A large French Cretaceousbird. Nature, birds seem to have been a significant component of 377 : 110. the Late Cretaceous avifauna. Although their fossil AVIN, L.; DUFFAUD, record for the last million years of the Cretaceousis S.; GHEERBRANT, E.; LAURENT, Y.; MARTIN, M.; RAGE, J.C.; TONG, H. & VASSE, D. 1997. Late Cretaceousnon- still too scanty to provide a detailed picture of the marine vertebrates from southern France : a review of recent last stagesof their evolution ary history, the idea that finds. GeobiosMémoire Spécial,20: 101-108. the enantiornithine radiation came to an end during CHIAPPE, L.M. 1991. Cretaceous avian remains from Patagonia the mass extinction of the Cretaceous-Tertiaryboun- shednew light on the early radiation of birds. Alcheringa,15, 3- dary (Feduccia, 1995, 1996) finds some support in 4 : 333-338. their continued presence in many parts of the world 1995.The first 85 million vearsof avian evolution. Nature,378 : 349-355. until late in the Cretaceousand their complete absen- I996a. Early avian evolution in the southernhemis- in ce the Tertiary. As already suggested elsewhere phere : the fossil record of birds in the Mesozoic of Gondw ana. (Buffetaut, 1996), the fact that the Enantiornithes, to Memoirsof the QueenslandMuseum,39,3 : 533- 554. judge from their bone histology, had a less advanced, 1996b. Late Cretaceous birds of southern South more reptile-like, physiology than modern birds America : anatomy and Systematics of Enantiornithes and (Chinsamy et al 1995) may help to explain why they Patagopteryx deferrariisi. Miinchner Geowissenschaftliche Abhandlungen,A, 30 :203-244. did not survive into the Tertiarv while other birds did. -& CALVO, J.G. 1994.Neuquenornis volans, a new Late Cretaceous bird (Enantiornithes : Avisauridae) from Patagonia, Argentina. Journal of Vertebrate Paleontology, 14 :230-246.

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Note reçue le 0l - I0- 1997 acceptéele 31-10-1997

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