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26. This research was funded by a NSF graduate research lab. GenBank accession numbers for sequence data are fellowship to Z.G., the University of Tennessee, a Research EF 090312-EF090397. Enhancement Grant from Texas State University to C.C.N., and NSF grant DEB-9306721 to A.M.S. We thank Supporting Online Material D. Bolnick, B. Fitzpatrick, S. Gavrilets, C. Jiggins, J. Ott, the www.sciencemag.org/cgi/content/full/1135875/DC1 EEB discussion group at Texas State University, and two Materials and Methods anonymous reviewers for comments on an earlier version SOM Text of this manuscript, and A. Stephenson for assistance in the Figs. S1 to S10

A Giant European Dinosaur and a New Sauropod Clade

Rafael Royo-Torres,* Alberto Cobos, Luis Alcalá Fossils of a giant sauropod dinosaur, Turiasaurus riodevensis, have been recovered from terrestrial deposits of the Villar del Arzobispo Formation (Jurassic-Cretaceous boundary) of Riodeva (Teruel Province, Spain). Its humerus length (1790 millimeters) and estimated mass (40 to 48 metric tons) indicate that it may have been the most massive terrestrial animal in Europe and one of the largest in the world. Phylogenetic analysis indicates that the fossil represents a member of a hitherto unrecognized group of primitive European eusauropods that evolved in the Jurassic. REPORTS Tables S1 to S4 References

3 October 2006; accepted 16 November 2006 Published online 30 November 2006; 10.1126/science.1135875 Include this information when citing this paper.

ments, eight teeth (Fig. 2), six cervical vertebrae (Fig. 1K) with ribs (Fig. 1, L and M) (probably cervicals 3 to 8), two proximal dorsal vertebrae, a middle dorsal vertebra (Fig. 1I), fragments of other dorsal vertebrae, eight dorsal r ibs (five incomplete), a partial sacrum, two distal caudal vertebrae (Fig. 1T), a p rox- imal fragment of the left scapula, a left sternal

plate (Fig. 1J), a distal fragment of the left 3 femur, a proximal fragment of the left tibia 10 a(f(FFinbidiuggl..a(Fig. a1n1 1, ,,(F iP inRN gca. ao nmn1and ddHp QlS )e,))t,eaO), ( tCr wc igoPohmT-tla p1edistally l2afets1ttp re1aelg t deoaaflltu incompleteCp sPa hsTa atn-lr1aadn2g6ag pel1ues)ss,, left n2, May 8o MtoshaseutNrog epiowgdaWsnto iancrldds [h sauauvcrheopab osedSeesnisa mf oroeusnadn ueri ousn- ionfd 2Piv8ai0rdaum tayl,2pe f(o.fiugR nde.S m c3la)oi,nses cota nottsre iiasbtcuinhtgeo dt hof etors ki nt uhla elns f a arrmaegae- PShpaoaluesionen)d.toi nlót gheicMo u dseeoT d eerl uaeF l-uDnidnaópcioólnis,C oT nejruunetol, g.orga www.sciencemag.org SCIENCE VOL 314 22 DECEMBER 2006 1925 REPORTS Diagnosis. Autapomorphies of Turiasaurus include the following: prezygapophyseal and postzygapophyseal articular facets on middle dorsal vertebrae strongly convex and con- cave, respectively; strongly convex subcircular hyposphene on middle dorsal vertebrae; distal caudal vertebrae strongly opisthocoelous; accessory process p rojecting caudodorsally from the dorsal margin of the shafts of p roxi- mal cervical ribs; distal humeral condyles strongly expanded cranially and caudally; radius and ulna distal condyles very compressed mediolaterally; carpal with two subcircular distal p rocesses separated b y a depression; cnemial crest of tibia reduced and directed cranially; fibula with roughened oval medial trochanter on middle-distal p art; and metatarsal V with slitrtyona gnlyd dex hpoarnizdoend. distal end. Locality and horizon. Riodeva (fig. S1), Teruel Province, Aragón, Spain (grid coordinates Universal Transverse Mercator 659049 and 4443553), site RD-10 (known as Barrihonda#El Humero), in the Villar del Arzobispo Formation (Tithonian-Berriasian), conformably overlying the Higueruelas Formation (7). In Riodeva, the top of the Higueruelas is dated as early Tithonian based on the occurrence ofthe forami- niferan Anchispirocyclina lusitanica (10). The teeth of Turiasaurus (Fig. 2) have heart-shaped spatulate crowns that are ar- ranged in the typical sauropodomorph over- lapping imbricate arrangement. The tooth enamel is wrinkled, and crown-to-crown oc- clusion has produced V-shaped wear facets (11, 12). There are also some isolated and very reduced marginal tooth denticles on the mesial and distal edges of the teeth. The cervical and dorsal vertebral centra are opisthocoelous and possess simple but well-developed pleurocoels. The neural spines appear to have b een shallowly divided (bifurcate) on the midline, as in the distal cervicals and proximal dorsals of E uhelopus (13) and M amenchisaurus (14). The dorsal neural spines are broader transversely than craniocaudally, a synapomorphy of Eusauropoda (11), and terminate dorsally in laterally directed triangular p rocesses (Fig. 1I). The internal bone structure is solid in the p resacral vertebrae and ribs. A p otentially diag- nostic character, p reviously observed only in the Late Cretaceous Asian titanosaurs Opis- thocoelicaudia (15) and B orealosaurus (16), is the presence of strongly opisthocoelous artic- ulations in distal caudal vertebrae (Fig. 1T). Based on our p hylogenetic results, this ap- pears to represent a convergence between these taxa and Turiasaurus. In contrast to that of Brachiosaurus, which has a deltopectoral crest medially p rojected (11), the humerus of Turiasaurus has a robust deltopectoral crest oriented cranially, and the proximal third of the bone slants noticeably medially in cranial view (Fig. 1B). The u lna has a triradiate proximal end, and the radius p ossesses a subrectangular distal condyle, as in other sauropods (11). The ratio of the length of the longest metacarpal long. The proximal end of the tibia is com- (Mc II) to that of the radius is 0.369. The m an- pressed mediolaterally, representing a p rimitive ual p halangeal formula is reduced to 2-2-2-2-?, state recorded in b asal sauropods (11, 12). The with p halanges t hat are broader than they are astragalus is wedge-shaped in cranial view,

right). Lingual [(A), (D), and (G)], distal [(B), (E), and (H)], and labial [(C), (F), and (I)] views are

shown. 3 10 2 This analysis also groups European, Asian, and South American Middle-Upper Jurassic Euhelopodidae- related sauropods in a monophyletic clade. The figure represents a 50% majority-rule consensus cladogram based on 11 most parsimonious trees. The data matrix contains 309 characters and 33 taxa (12), adding three genera from the Villar del Arzobispo Formation: Galveosaurus, Losillasaurus, and Turiasaurus (table S3). The analysis was done with PAUP* 4.0b 10 (29): tree length = 611; consistency index = 0.5205; retention index = 0.7233.

1926 22 DECEMBER 2006 VOL 314 SCIENCE www.sciencemag.org and its distal surface is convex mediolaterally. Neosauropoda and belongs to a new clade, The ascending process of the astragalus ex- named Turiasauria (24), together w ith Losilla- tends over the cranial two-thirds ofthe proximal saurus and Galveosaurus. Turiasauria is di- surface, u nlike the condition in neosauropods agnosed by vertical cervical neural spines, where this process reaches the caudal m argin posterior centroparapophyseal laminae on dor- (11). The metatarsals are robust and display the sal vertebrae, absence of p respinal and p ost- typical sauropod #spreading$ graviportal mor- spinal laminae on dorsal vertebrae, absence of phology (11). The p edal p halanges are broader the scapular acromial crest, proximal end of than they are long, and the unguals of digits II humerus deflected medially (Fig. 1B), p romi- and III have mediolaterally compressed and nent humeral deltopectoral crest, and finally b y dorsoventrally tall proximal ends, as in other a vertical ridge developed on the caudal side of sauropods (11, 12). the distal half of the ulna. The geographic and Turiasaurus differs from other sauropods stratigraphic r anges of this clade are u ncertain, from the Iberian Range. A ragosaurus (17) is a but Turiasauria probably r epresents a sauropod taxon distinct from Turiasaurus, as demon- radiation that originated in Europe earlier than strated b y differences in b oth morphology and the Tithonian. Members of this clade may also age. Losillasaurus (18) and Galveosaurus (19#21), have b een present in France, Portugal, and which also come from the Villar del A rzobispo England, w here teeth similar to those of Formation, are also different from the new Turiasaurus have been recovered from the Riodeva taxon. Turiasaurus p ossesses features Jurassic [such as $Neosodon% (12, 25) and that distinguish it from L osillasaurus, among Cardiodon (12)]. All of these teeth share the them p resacral v ertebrae with bifurcate neural following characters, and may b e referable to spines. Moreover, the p rezygapophyses of Turiasauria: heart-shaped crowns (when un- Turiasaurus have a r ugose ventral process that worn), a pointed and asymmetrical crown apex is b etter developed toward the proximal than that is strongly compressed labiolingually, and toward the p rezygapophyses themselves. A crowns with convex labial surfaces with a similar character is developed in the postzyg- bulge that extends from the base toward the apophyses but in a more dorsal p osition. Also, apex. the dorsal vertebrae of Turiasaurus have Many of the elements of Turiasaurus are convex and robust p rezygapophyses and a comparable in size with those of some of the convex hyposphene w ith a circular contour. largest known sauropods (tables S2 and S3). For Distal caudal vertebrae are opisthocoelous. example, the humerus of the type specimen is With respect to the appendicular skeleton, the 1790 mm long, similar to the value estimated for main differences are in the humeral condyles, Argentinosaurus (1810 mm) (5) and longer than which are well marked on the cranial face. that of P aralititan (1690 mm) (5). Only the Furthermore, in Turiasaurus, the r adial and humeri of b rachiosaurids, which can exceed ulnar distal ends are strongly compressed 2000 mm in length (6, 22) are longer. However, mediolaterally, and the carpal has two distal brachiosaurs, including B rachiosaurus itself, processes. Turiasaurus also p ossesses features have apomorphically elongated forelimbs (11), that distinguish it from Galveosaurus. In which means t hat comparisons b ased solely on Turiasaurus the cervical vertebrae have a solid humerus length might underestimate the relative internal b one structure, the dorsal vertebrae body size of a nonbrachiosaurid such as Turia- are broader transversely, and the cervical and saurus. This explains why hindlimb elements of dorsal n eural spines are bifid. Pleurocoels in Turiasaurus are actually larger than those of the dorsal vertebrae are smaller and shallower. biggestBrachiosaurus specimens (table S3). For The humeral distal condyles of Turiasaurus are example, in Turiasaurus, the length of meta- more marked cranially. Furthermore, Turiasaurus tarsal II is 295 mm, whereas in B rachiosaurus also differs from Portuguese sauropods known (HMN SII) it is 276 mm (6). In Turiasaurus, the from the Oxfordian-Kimmeridgian. The follow- ungual phalanx on p edal digit Iis 300 mm long, ing features distinguish it fromLourinhasaurus: and 240 mm long in B rachiosaurus (HMN SII) absence of a large p ostspinal lamina on the (6). The largest sauropod specimens that had dorsal v ertebrae, a differently shaped humerus been reported from Europe are an isolated with more marked distal condyles, and an brachiosaurid cervical vertebra from the Lower elliptical morphology of the proximal end of Cretaceous Wessex Formation in southern the t ibia (12, 22). D inheirosaurus p ossesses England (26) and an isolated proximal caudal the following features that are absent in vertebra from another site in Riodeva (9). We Turiasaurus: an elongate p neumatic fossa on estimate t hat Turiasaurus b ody mass was be- the lateral surfaces of the cervical neural tween 40 and 48 m etric tons (27), weighing spines, robust h orizontal lamina linking the more than any other European sauropod. Partic- hyposphene with the posterior centrodi- ularly large sauropod genera, with b ody lengths apophyseal lamina in dorsal vertebrae, and exceeding 30 m and estimatedmasses of40,000 kg prespinal and p ostspinal laminae on dorsal or m ore, h ave previously b een recognized only vertebrae (23). within the neosauropod radiations [diplodocoids Phylogenetic analysis (Fig. 3 and table S1) (1) and titanosauriforms (2, 3, 28)], and it might indicates t hat Turiasaurus lies outside of have b een supposed that t ruly gigantic forms REPORTS were restricted to N eosauropoda. Turiasaurus however, demonstrates that at least one of the more b asal (non-neosauropod) lineages achieved gigantic size independently.

References and Notes 1. D. D. Gillete, RJ .. Vertebr. Paleontol. 1e1rs, 417 (1991). 2. M. Jeo. Wedel, R. L. Cifelli, R. K. Sanders, J . Vertebr. Paleontol. a20rte, 109 (2000). 3. J. F. Bonaparte, R. A. Coria, A meghiniana 30, 271 (1993). 4. F. E. tN.ovC iaesn, L. NSaalt.gaB deorn, Jar. Calvo, F. dAagvniaol i7n,, Rev. M us. A J.rgB .en St.m Cienc. Nat. Bernardino Rivadavia 071, 37 (2005). 5. JG. B. Smith et al., Science 1299288, 1704 (2001). 6. G. S. Paul, Hunteria 2, 1(1988). 7. L. oLguqacueet, A. Cobos, R. 0R5o)y.o-Torres, E. Espílez, L. Alcalá, RG.eoR ogyacoe-Ttoa r3e8s,, 27 (2005). 8. R. RRooyyoo--TToorrrreess,, A. Cobos, Geo-Temas 6, 59 (2004). 9. R. RFeoyzoer-,ToA rrbreI sn, A. Cobos, aGeläoognatc.eU tna v38. S, 23 (2005). 10. R. Fezer, Arb Inst. Geol. Paläont. Univ. S tuttgart 84, 1(1988).

11. JP. A. Wilson, Z ool. J B. Linn. S oc. 136, 215 (2002). 3 13.C12. CD..aB P.Wl ifo.i Upchurch,mrWnaienias, hP Praameslapsee,oP. lB,neM. Prt.koDBarrett, el.loeS dyis,noiC cnAa,,HP. 6Dodson, 2 .,01 O 04s( m)1,9óp l2spk9.a),.2in The 5E 9d#Dinosauria,s.3( 2U2n.iv.o f ,1 208 14. C. C. gYrou.8 n,g, H. C. Chao, Vert. Paleontol. Paleoanthropol. ya M M.onB oorgsr.u 8k-B, 1(1972). M 15. M. Borsuk-Bialynicka, Palaeontol. Polonica 37, 5 n (1977). o 16. H. ,Y9o u07, Q (2. 0Ji0, M. C. Lamanna, J. Li, Y. Li, A cta Geol. S in. gr 1187..JE M.stL78, .u .Ld. S.aC907 Gna esz,oan(2004). Alo..v DG a.as,B lvJ ues.-cV Ta.rleiomS napni,,t Ma4 f.5éL ,( .1J C .9aL 8s.7aS )n.aonvza,s,P J a.leV o.nS taonl.tafé, mageo. 19. JE.v Lo.lB ucaricóo, 3J 2.,I .9 C 9anu( 2d0o,0G 1.).C uenca-Bescós, J .I .R uiz-Omeñaca, nce 2222220143..... TJBA2B NB...u,ea.FiT.nc r Ftr1n i rluioddinevgenS S...aááa s BA n (Lnaa1rroccaudhn9hpgria5epenioanp7zazora--e)eHHR aslilse tu . issrteeainerrd hsaanuro vt ,nn,1aeO ááfG 5di.nnn.,a4ddv topoS M Z eieedbaazz dasltam (2yht,, s5 0euZ Z ze,0reooe5sw1 soarueru ,o)o3t.sR ta aake(i sclo sxx,1aava .M losreilcyatr991 M 1 s et92em0u)ms0.3..1S 4-A ,eb,rrag6uelsa.tedt 1 vse3.e( nG d2( t2é0.t 0oa0Co 0lx5i.e6o)P nn.)c.or.tuN gaatl. ww.sciddea from w 25. E. Buffetaut, M. Martin, Rev. Paléobiol. 7, 17 (1993). ol 26.D Cr.et Naaciesoh,uD s. ReM s.. M2 5ar,ti7 ll8,7D .( 20C 0o4op).er,K .A .S tevens, wno 27. See s.M upapzozretttina,g material onsne Science Online. D 28. G. V. Mazzetta, P. Chistiansen, R. A. Fariña, Hist. Biol. 16, 71 (2004). 29. D. L. Swofford, PAUP*. PM heyltohgoedsn)e,tcv ie rAsinoanly s4is.0 Ubsi1 n0g Parsimony (*and Other M ethods), version 4.0b 10 (Sinauer, Sunderland, MA, 2002). 30. We thank our colleagues at the Foundation; P. Upchurch; Gobierno de Aragón (Departamentos Educación, Presidencia, Industria, Economía, Ciencia); Projects FOCONTUR and 252/2002, 142/2003, 142/02/2004, and 197/2005 (Dirección General Patrimonio Cultural); Dinópolis; Diputación Provincial Teruel and Gabinete Geológico; Ayuntamiento Riodeva; the Spanish Army; and the Ministerio Educación (492839C1 and CGL2006- 13903). V. Fonte and M. Prendergast helped in editing text. We thank two anonymous reviewers for their comments. We dedicate this work to the memory of J. Roig.

Supporting Online Material www.sciencemag.org/cgi/content/full/314/5807/1925/DC1 SOM Text Figs. S1 to S4 Tables S1 to S5 References

21 July 2006; accepted 25 October 2006 10.1126/science.1132885