The first edentulous ceratosaur from South America The recognition of ontogenetic edentulism in the Jurassic noasaurid Limusaurus inextricabilis shed new light on the dietary diversity within Ceratosauria, a stem lineage of non-avian theropod dinosaurs known for peculiar craniomandibular adaptations. Until now, edentulism in Ceratosauria was exclusive to adult individuals of Limusaurus. Here, an exceptionally complete skeleton of a new toothless ceratosaur, Berthasaura leopoldinae gen. et sp. nov., is described from the Cretaceous aeolian sandstones of the Bauru Basin, Southern Brazil. The specimen resembles adult individuals of Limusaurus by the absence of teeth but based on the unfused condition of several elements (e.g., skull, vertebral column) it clearly represents an ontogenetically immature individual, indicating that it might never have had teeth. The phylogenetic analysis performed here has nested Berthasaura leopoldinae as an early-divergent Noasauridae, not closely related to Limusaurus. It represents the most complete non-avian theropod from the Brazilian Cretaceous and preserves the most complete noasaurid axial series known so far. Moreover, the new taxon exhibits many novel osteological features, uncommon in non-avian theropods, and unprecedented even among South American ceratosaurs. These include not only toothless jaws but also a premaxilla with cutting occlusal edge, and a slightly downturned rostral tip. This indicate that B. leopoldinae unlikely had the same diet as other ceratosaurs, most being regarded as carnivorous. As the ontogenetically more mature specimens of Limusaurus, Berthasaura might have been herbivorous or at least omnivorous, corroborating with an early evolutionary divergence of noasaurids from the ceratosaurian bauplan by disparate feeding modes.
Ceratosauria represents one of the most widespread and diverse clade of extinct theropods1,2. Currently, three main lineages are recognized within Ceratosauria: Ceratosauridae, Abelisauridae and Noasauridae3,4,5. In terms of morphology, mid- to large-sized members of the Abelisauridae and Ceratosauridae are relatively better-known than the gracile small-bodied noasaurids. Most noasaurids consist primarily of fragmentary specimens, with few exceptionally well-preserved taxa restricted to the Malagasy species Masiakasaurus knopfleri6, the Tanzanian Elaphrosaurus bambergi5, and Limusaurus inextricabilis4,7 from China. Despite the fragmentary nature of the noasaurid fossil record, it revealed some osteological features uncommon among non-avian theropods, incluing procumbent and heterodont lower dentition6,8,9 or toothless rostra likely covered by rhamphothecae4. These ceratosaurs indicate a complex evolution of feeding linked to the origin and diversification of the Noasauridae.Not surprisingly, a robust understanding of the evolutionary history and distribution of the morphoanatomical traits of noasaurids, and their meaning within a broader ceratosaur and theropod evolutionary context, is still in progress. As early as in the Late Jurassic, noasaurids present a highly derived combination of characters4,7. The scarcity of knowledge regarding early diverging species and the temporal and ‘morphological’ gaps between Late Jurassic and Late Cretaceous noasaurids, strongly limit our understanding of the evolution of the group5. Recently, a paleontological site named Cemitério dos Pterossauros Quarry (Pterosaur Graveyard)10 from the Lower Cretaceous Goio Êre Formation (Bauru Basin), which crops out at the Northwestern Paraná State, Southern Brazil, revealed several theropod remains11,12. Here, we describe a new edentulous noasaurid yielded from this site which is also the first toothless non-avian theropod known from Brazil. Institucional abbreviations MN—Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil; IVPP—Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; MPCO.V—Museu de Paleontologia de Cruzeiro do Oeste, Cruzeiro do Oeste, Brazil; UA—Université d’Antananarivo, Antananarivo, Madagascar; USNM—National Museum of Natural History, Washington DC. Dinosauria Owen, 1842 Theropoda Marsh, 1881 Abelisauroidea (Bonaparte and Novas, 1985) sensu Wilson et al.13 Noasauridae Bonaparte & Powell, 1980 sensu Wilson et al.13 Berthasaura leopoldinae gen. et sp. nov. The generic name honors the researcher Bertha Maria Júlia Lutz (1894–1976) for her scientific contribution and social activity particularly regarding woman rights in Brazil, combined with saura, feminine of saurus from the Greek for lizard. The specific epithet leopoldinae honors the first Brazilian empress, Maria Leopoldina (1797–1826), for her fundamental role in the independency of Brazil that next year (2022) will complete two centuries; and the samba school Imperatriz Leopoldinense, that in the 2018 carnival developed the theme “A Royal Night at the Museu Nacional” (Uma noite real no Museu Nacional) in commemoration of the bicentenary of the museum. This was before the large fire of September 201814.HolotypeMN 7821-V comprises a nearly complete disarticulated skeleton, including a partial skull and lower jaw (Figs. 1, 2, 3, 4, and 5).Figure 1Berthasaura leopoldinae gen. et sp. nov. holotype (MN 7821-V), line drawing of the skull and mandible. Abbreviations: Bo? basioccipital fragment; Cup?, cutriform process; Ect? ectoperygoid; Hy, hyoids; Ic2, intercentrum 2; La, left angular; Lden, left dentary; Lf, left frontal; Llac, left lacrimal; Llac?, left lacrimal fragment; Lmax, left maxilla; Lna, left nasal; Lpa, left prearticular; Lpal, left palatine; Lpo, left postorbital; Lpar, left parietal; Lpmax, left premaxilla; Lpop, left paraoccipital process; Lqj, left quadratojugal; Lsp, left splenial; Lsq, left squamosal; Lsur, left surangular; Pcr, proximal fragment of cervical rib; Pro, prootic fragment; Pt?, pterygoid; Qf, quadratic flange (pterygoid flange of the quadrate); Qh, quadratic head; Rden, right dentary; Rlac, right lacrimal; Rpop, right paraoccipital process; Rpmax, right premaxilla. Line drawing by G.A.S.Figure 2Berthasaura leopoldinae gen. et sp. nov. holotype (MN 7821-V), interpretative line drawing of the skull and photographs of cranial bones. (a) Interpretative reconstruction of the skull. (b) Left nasal in dorsolateral view. (c) Right lacrimal in lateral view. (d) Left frontal in dorsal view. (e) Left parietal in dorsal view. (f) Left squamosal in lateral view. (g) Left postorbital in lateral view. (h) Left premaxilla in lateral view. (i) Right premaxilla in medial view. (j) Left maxilla in lateral view. (k) Left paraoccipital in caudal view and left (?) quadratic flange. (l, m) Quadratic head in lateral and caudolateral views, respectively. (n) Left splenial in lateral view. (o) Right dentary in lingual view. (p) (p) Left prearticular in lateral view. (q) Left palatine in dorsal view. (r, s) Left pterygoid in lateral and dorsal views, respectively. (t) Left surangular and angular in lateral view. (u) Left ceratohyal in lateral view. Abbreviations: An, Angular; Aof, Antrorbital fenestra; Aofo, Antorbital fossa; Aps, Angular process of surangular; Ch, Choana; Chp, Choanal process; Cap, Caudal process; Cvp, Caudoventral process; Dqjc, Dorsal quadratojugal contact; Emf, External maxillary fenestra; En, External naris; Eo-op, Exoccipital-ophistotic; F, Foramina; Fc, Frontal contact; Jc, Jugal contact; Jr, Jugal ramus; Lam, lamellae; Lc, Lacrimal contact; Lf, Lacrimal fragment? Lfo, Lateral fossa; Lpr, Lacrimal pneumatic reces; Lvp, Lateroventral process of nasal; Mb, Medial body of prearticular; Mfo, Maxillary fossa; Mp, Maxillary process; Nc, Nasal contact; Ncr, Nuchal crest; Nlc, Nasolacrimal canal; Np, Narial process; Nvf, Neurovascular foramina; Nvs, Neurovascular sulcus; O, Orbit; Poc, Postorbital contact; Pop, Paraoccipital process; Ppp, Pterygoid process of palatine; Pqp, Postquadratic process; Ptm, Pterygoid medial process; Qf?, Quadrate flange (pterygoid flange of the quadrate); Qh, Quadratic head; Qj, Quadratojugal; Qjc, Quadratojugal contact; Qrg, Quadrate ridge groove; Rap, Retroarticular process; Rdp, Rostrodosal process of nasal; Rr, Rostral ramus; Sc, Sagittal crest; Si, Symphyseal region; Sp, Squamosal process; Stfo, Supratemporal fossa; Sur, Surangular ramus; Vpar, Vomeropalatine process of pterygoid; Vr, Ventral ramus. Line drawing by G.A.S.Figure 3Photograph and inner structure of the left dentary. (a) Photograph of the dentary in lateral view. (b, c) µCT-scan of the dentary in occlusal and lateral views, respectively. (d) Slice showing the cavities within the trabecular bone connected with the outer bone surface by foramina, in sagittal view. Abbreviations: Cb, Cavities of trabecular bone; Cmc, Caudal open of Meckelian canal; Mc, Meckelian canal; Nvf, neurovascular foramina; Pg, Pits and grooves; S, sediment.Figure 4Berthasaura leopoldinae gen. et sp. nov., holotype (MN 7821-V), nearly complete skeleton. (a) Photograph. (b) Respective line drawing. Abbreviations: Cav, Caudal vertebrae; Che, Chevrons; Cr, Cervical ribs; Cv, Cervical vertebrae; Dcav, Distal caudal vertebrae; Den, Dentaries; F, Frontal; Fe, Femora; Ga, Gastral elements; Hy, Hyoids; Is, Ischia; Lcor, Left coracoid; Lfi, Left fibula; Lh, Left humerus; Lp, Left parietal; Lpmax, Left premaxilla; Lrad, Left radius (ulna hidden); Lsca, Left scapula; Lsur, Left surangular; Lt, Left tibia; Mp, Manual phalanges; Pp, left pedal phalanx III-1; Pu, Pubes; R, Trunk ribs; Rfi, Right fibula; Rl, Right lacrimal; Rpal, Right palatine; Rpmax, Right premaxilla; Rsca, Right scapula; Rt, Right tibia fragment; Sas, Sacral neural spine; Sav, Sacral vertebrae; Tv, Trunk vertebrae; V, Vomeropterygoid process fragment. Line drawing by G.A.S.Figure 5Interpretative line drawing of Berthasaura leopoldinae gen. et sp. nov., holotype (MN 7821-V), and photographs. (a) Line drawing reconstruction; (b) Intercetrum and axis in cranioventral views; (c) 4th cervical vertebrae in lateral view; (d) First trunk centrum in lateral view; (e) 8th trunk centrum in lateral view; (f) last sacral vertebrae in caudal view; (g) right scapula in medial view; (h) left coracoid in lateral view; (i, j) left humerus in cranial and lateral views, respectively; (k, l) left ulna in lateral and cranial views, respectively; (m) left radius in cranial view; (n) manual ungual in lateral view; (o) manual phalanges II (in dorsal view) and III (in lateral view); (p) left ilium in lateral view; (q) left ilium in ventral view; (r) pubes and ischia; (s, t) left femur in cranial and medial views, respectively; (u) left fibula in medial view; (v) right fibula in lateral view; (w) pedal ungual in lateral view; (x) left pedal phalanx III-1 in lateral view. Abbreviations: Ac, Acetabular margin; Af, Acromion fragment; Aic, Axial intercentrum; Cf, Coracoid foramen; Cg, Colateral vascular groove; Clfl, Fossa for attachment of M. Caudofemoralis longus; Cn, Caudal notch; Cp, Colateral pit; Ctr, Cranial trochanter; Cuf, Cuppedicus fossa; Cvp, Caudoventral process; Dp, Diapophysis; Dpc, Deltopectoral crest; Epi, Epipophysis; F, Flange; Ft, Fourth trochanter; G, Glenoid; Gt, Greater trochanter; Ic, Iliac contact; Ifs, scar for M. iliofibularis; Isc, Ischial contact; Lbs, Lateral brevis shelf; Lis, Left ischium; Lp, Left pubis; Lvf, Lateroventral flange; Mf, Medial fossa; Clfl, Fossa for M. caudofemoralis longus; Ncs, Neurocentral suture; Ns, Neural spine; Od, Odontoid process; Ax, Axial centrum; Of, Obturator foramen; Ol, Oleacron; Opl, Obturator plate; Opr, Obturator process; Pc, Pubic contact; Pf, Pneumatic foramina; Podl, Postzygodiapophyseal lamina; Posf, Post spinal fossa; Poz, Postzygapophysis; Pp, Parapophysis; Pup, Pubic peduncle; Rc, Radial condyle; Ris, Right ischium; Rp, Right pubis; Sac, Supraacetabular crest; Scs, Scapular shaft; Ts, Trochanteric shelf; Uc, Ulnar condyle. Line drawing by G.A.S.Horizon and localityCemitério dos Pterossauros Quarry10, Goio Erê Formation, Early Cretaceous (Aptian-Albian), Caiuá Group, Bauru Basin15. The fossils were collected in layers that crop out in a rural road at Cruzeiro do Oeste Municipality, Paraná State, Southern Brazil.DiagnosisNoasaurid ceratosaur with the following combination of characters that distinguishes it from other members of the clade (autapomorphies are marked with an asterisk): edentulous rostrum (premaxilla, maxilla and dentary); lamellae on the medial surface of the premaxilla*; short dentaries with the length rostral to the mandibular fenestra about 1.5 times the height of the dentary*; protuberance projecting from the caudoventral end of the premaxillary buccal rim*; non-bifurcated rostral end of splenial*; postzygodiapophyseal lamina in mid-cervical vertebrae divided in two parts and reduced to low ridges; maximal length of metacarpus less than 15% of the length of humerus; iliac blade mediolaterally flattened; medial brevis shelf strongly reduced*; deep notch on the caudal margin of the ischial process producing an eminent and caudally-oriented prong*; rounded medial femoral epicondyle.
Ontogenetic assessmentEstablishing the ontogenetic stage in any fossil vertebrate can be quite challenging due to the lack of complete and sometimes comparable ontogenetic sequences16,17,18. The multiple specimens referred to Limusaurus inextricabilis enable the establishment of six ontogenetic stages based mainly on size and osteohistological sections and an attempt to assess variation in anatomy to ontogeny4. This may provide a parameter to infer the degree of maturity of Berthasaura leopoldinae, with the caveat that it is not sure at the time being if these noasaurid species share the same ontogenetic development.From the 73 anatomical features listed by Wang et al.4, they only refer to the fusion of bones in three: fusion of astragalus and calcaneum to each other and to the distal end of tibia, posterior cervical ribs fused with the respective centrum, and fusion of the frontal with the parietal. The holotype of Berthasaura leopoldinae lacks the distal end of tibia + astragalus and cal
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