New alvarezsaurid (Dinosauria, Theropoda) from uppermost ...

Cretaceous Research xxx (2012) 1e24

Contents lists available at SciVerse ScienceDirect

Cretaceous Research journal homepage: www.elsevier.com/locate/CretRes

New alvarezsaurid (Dinosauria, Theropoda) from uppermost Cretaceous of north-western Patagonia with associated eggs Federico L. Agnolin a, b, * , Jaime E. Powell c, d, Fernando E. Novas a, d, Martin Kundrát e a Laboratorio de Anatomía Comparada y Evolución de los Vertebrados, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470, C1405DJR Buenos Aires, Argentina b Fundación de Historia Natural “Félix de Azara”, Departamento de Ciencias Naturales y Antropología, CEBBAD e Universidad Maimónides, Valentín Virasoro 732, 1405BDB Buenos Aires, Argentina c Instituto “Miguel Lillo”, Miguel Lillo 205, 4000 San Miguel de Tucumán, Argentina d CONICET, Argentina e Subdepartment of Evolution and Development, Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 January 2011 Accepted in revised form 19 November 2011 Available online xxx

The Alvarezsauridae represents a branch of peculiar basal coelurosaurs with an increasing representation of their Cretaceous radiation distributed worldwide. Here we describe a new member of the group, Bonapartenykus ultimus gen. et sp. nov. from CampanianeMaastrichtian strata of Northern Patagonia, Argentina. Bonapartenykus is represented by a single, incomplete postcranial skeleton. The morphology of the known skeletal elements suggests close affinities with the previously described taxon from Patagonia, Patagonykus, and both conform to a new clade, here termed Patagonykinae nov. Two incomplete eggs have been discovered in association with the skeletal remains of Bonapartenykus, and several clusters of broken eggshells of the same identity were also found in a close proximity. These belong to the new ooparataxon Arriagadoolithus patagoniensis of the new oofamily Arriagadoolithidae, which provides first insights into unique shell microstructure and fungal contamination of eggs laid by alvarezsaurid theropods. The detailed study of the eggs sheds new light on the phylogenetic position of alvarezsaurids within the Theropoda, and the evolution of eggs among Coelurosauria. We suggest that plesiomorphic alvarezsaurids survived in Patagonia until the latest Cretaceous, whereas these basal forms became extinct elsewhere. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: Alvarezsauridae Patagonykinae Arriagadoolithidae Cretaceous Patagonia Argentina

1. Introduction Alvarezsauridae is a group of theropod dinosaurs erected by Bonaparte (1991) in order to include the ornithomimid-like genus Alvarezsaurus from the ConiacianeSantonian of Patagonia, Argentina. Lately, new species have been included in this family, namely the Patagonian Patagonykus, (from the Turonian of Patagonia; Novas, 1996, 1997), and several derived avian-like Eurasian and North American genera, such as Mononykus, Shuvuuia, and Parvicursor (Perle et al., 1993; Karhu and Rautian, 1996; Chiappe et al., 1998; Hutchinson and Chiappe, 1998; Naish and Dyke, 2004; Alifanov and Barsbold, 2009; Xu et al., 2010). Recently a very basal alvarezsaurian was found in early Late Jurassic deposits in

* Corresponding author. Laboratorio de Anatomía Comparada y Evolución de los Vertebrados, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470, C1405DJR Buenos Aires, Argentina. E-mail addresses: [email protected], [email protected] (F.L. Agnolin).

China, indicating that this theropod clade originated earlier than previously thought (Choiniere et al., 2010). In South America, the oldest alvarezsaurid record belongs to the Turonian Patagonykus (Novas, 1996, 1997), and was temporally followed by the genera Alvarezsaurus and Achillesaurus (Bonaparte, 1991; Martinelli and Vera, 2007) in ConiacianeSantonian beds. Recently, on the basis of very poorly preserved specimens, Salgado et al. (2009) reported the presence of an indeterminate alvarezsaurid from the uppermost Cretaceous of Patagonia. In this way, the fossil alvarezsaurid record from South America is still very patchy and biased, being restricted to a couple of findings in Late Cretaceous beds. The aim of the present paper is to describe a new basal Patagonykus-like Alvarezsauridae from the Upper Cretaceous Allen Formation (CampanianeMaastrichtian) at the locality of Salitral Ojo de Agua, North Patagonia, Argentina (Fig. 1). The specimen is represented by a nearly articulated but poorly preserved and weathered partial skeleton of a single individual associated with two eggs. The eggs are 7 cm in diameter, measured across a preserved

0195-6671/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.cretres.2011.11.014

Please cite this article in press as: Agnolin, F.L., et al., New alvarezsaurid (Dinosauria, Theropoda) from uppermost Cretaceous of north-western Patagonia with associated eggs, Cretaceous Research (2012), doi:10.1016/j.cretres.2011.11.014

2

F.L. Agnolin et al. / Cretaceous Research xxx (2012) 1e24

Fig. 1. Map showing the location of the Salitral Ojo de Agua fossiliferous locality, indicated by a star; modified from Martinelli and Forasiepi (2004).

portion (Fig. 2). Furthermore, several clusters of broken eggshell pieces of the same type were also found close to the fossil bones of Bonapartenykus. Both the eggs and eggshell clusters were sampled to analyze the microstructure of their shells, which as we suggest here, had been formed within oviducts of alvarezsaurid theropods, thus expressing their specific reproductive signature. This is the first time that a specific eggshell microstructure pattern may be directly linked to alvarezsaurid theropods, namely the Patagonian alvarezsaurid Bonapartenykus ultimus. In this way, the objective of the present paper is twofold: it documents the persistence of basal alvarezsaurids in South America

Fig. 2. Sketch showing the finding of the holotype of Bonapartenykus ultimus (MPCA, 1290) and associated eggs. Abbreviations: dv, dorsal vertebra; eg, eggs; fem, femur; il, ilium; pub, pubis; sc, scapulocoracoid; tib, tibia. Scale bar represents 20 cm.

up to the latest Cretaceous, and also allows recognition of alvarezsaurid egg morphology and structure. Abbreviations. MPCA, Museo Provincial “Carlos Ameghino”, Cipolletti, provincia de Río Negro, Patagonia, Argentina; MGPIFD-GR, Museo de Paleontología y Geología del Instituto de Formación Docente Continua de General Roca, General Roca, provincia de Río Negro, Argentina. 2. Material and methods Phylogenetic analysis was performed using TNT (Goloboff et al., 2008). All characters were equally weighted and treated as unordered. Tree bisection and reconnection (TBR) was utilized as the branch-swapping algorithm for the heuristic search. Heuristic searches were performed on 1000 pseudoreplicate datasets, with 10 random addition sequence replicates for each search. The maximum number of trees saved for each random addition sequence replicate was set to 100. Based on the dataset of Choiniere et al. (2010), a phylogenetic analysis was conducted to evaluate the phylogenetic affinities of the new alvarezsaurid genus (Supplementary Information parts 1e3). The data matrix includes 423 characters and 104 terminal taxa (Supplementary Information part 3). This analysis concluded in 1000 shortest trees, of which the strict consensus resulted in a single tree of 2188 steps, a Consistence index of 23, and a Retention index of 61. To the Choiniere et al. (2010) dataset we added the characters 422 and 423. Moreover, we included several terminal taxa that were not scored in the dataset of these authors, such as: Ceratonykus oculatus Alifanov and Barsbold, 2009, Xixiakykus zhangi Xu et al., 2010, Linhenykus monodactylus Xu et al., 2011, and Albinykus baatar Nesbitt et al., 2011. Regarding eggshell morphological analysis, the selected samples were broken into fragments, some of which were prepared as standard petrographic thin sections (w 30 mm) to be studied using both transmitted and polarized light microscopy. The other



3

fragments were mounted on aluminium stubs, coated in gold (30 nm), and imaged under the Zeiss Supra 35-VP (Carl Zeiss SMT, Oberköchen, Germany) field emission scanning electron microscope (SEM) equipped with a VPSE detector for low vacuum conditions, a Robinson BSD for backscattered electron imaging, and coupled with an EDAX Apex 4 (Ametekh, Mahwah, USA) EDS-detector for dispersive X-ray microanalysis. Structural parameters such as shell/ layer/crystalline unit dimensions and pore width were measured with software of the Zeiss Supra 35-VP SEM facility. 3. Systematic paleontology Theropoda Marsh, 1881 Coelurosauria Huene, 1920 Alvarezsauria Bonaparte, 1991 Alvarezsauridae Bonaparte, 1991 Patagonykinae nov. Diagnosis. Largest known alvarezsaurids, diagnosable on the basis of the following unambiguous synapomorphies, not recorded in any other dinosaur: (1) presence of a longitudinal ridge on the lateral surface of coracoid (422-1), and (2) strongly sculptured ventral half of coracoid (423-1). In addition, both Bonapartenykus and Patagonykus share a medially deflected coracoid, a condition unknown in other alvarezsaurs, but currently widespread among Paraves (Makovicky et al., 2005; ch. 261-1). Included taxa. Patagonykus puertai Novas, 1996; Bonapartenykus ultimus gen. et sp. nov. Agnolin, Powell, Novas and Kundrát. Temporal range. SantonianeMaastrichtian (Upper Cretaceous). Geographic distribution. Neuquén and Río Negro provinces, northwest Patagonia, Argentina.

Fig. 3. Dorsal vertebra of Bonapartenykus ultimus (holotype, MPCA, 1290) in A, cranial, B, right lateral and C, posterior views. Abbreviations: dp, diapophysis; f, fossae; hy, hyposphene; la, spinopostzygapophyseal lamina; ls, ligamental scars; nc, neural canal; par, parapophysis; pf, postespinal fossa; poz, postzygapophysis; prz, prezygapophysis. Scale bar represents 5 cm.

Bonapartenykus ultimus gen. et sp. nov. Figs. 2e7 Derivation of name. The generic name derives from the surname of the great Argentinean palaeontologist José F. Bonaparte and the Latin word onykus (claw). The specific name derives from the Latin word ultimus (latest), because the present record constitutes the geologically youngest alvarezsaurid from South America. Holotype. MPCA, 1290 (Museo Provincial “Carlos Ameghino”, provincia de Río Negro, Patagonia, Argentina), a nearly articulated but badly preserved partial skeleton consisting of an incomplete mid-dorsal vertebra, a nearly complete left scapulocoracoid, incomplete right scapulocoracoid, incomplete left tibia and femur, nearly complete left pubis articulated with the incomplete pubic peduncle of ilium, and the anterior blade of the left ilium. The specimen was associated with two partially preserved eggs that were separated from this individual by less than 20 cm (Fig. 2). Referred specimens. MGPIFD-GR 166 and MGPIFD-GR 184; both appear to belong to the same individual, consisting of a fragmentary blade of left scapula, an incomplete left coracoid and distal right pubis, and four cervical and a single caudal vertebra described in detail by Salgado et al. (2009). Although Salgado et al. (2009) described the specimen as belonging to a proximal portion of the pubis, the element may belong to the distal end of the bone. In fact, as occurs in the distal pubis of the holotype of Bonapartenykus, in MGPIFD-GR 166 the preserved portion of the pubis shows a welldeveloped internal ridge that represents the reduced pubic apron characteristic of the new genus. The scapula may be referred to

Fig. 4. Scapulocoracoids of Bonapartenykus ultimus (holotype, MPCA, 1290). A, B, left scapulocoracoid in lateral and cranial views respectively. C, D, right scapulororacoid in lateral and caudal views respectively. Abbreviations: cf, coracoidal foramen; cor, coracoid; gl, glenoid fossa; lr, logitudinal ridge; r, rugosities; sb, scapular blade; sc, scapula; vf, ventral flange. Scale bar represents 2.5 cm.


4


hadrosaurids, ankylosaurs, and several titanosaurid sauropods; theropods are represented by several incomplete remains of abelisaurids, indeterminate tetanurans, and probable coelurosaurian taxa (Powell, 1987; Coria and Salgado, 2001, 2005; Coria, 2001). In addition, recent findings include an incomplete large alvarezsaurid (Salgado et al., 2009) and the gigantic unenlagiid theropod Austroraptor cabazzai (Novas et al., 2009). Diagnosis. Alvarezsaurid theropod diagnosable on the basis of the following autapomorphies: (1) mid-dorsal vertebrae with spinopostzygapophyseal laminae ending abruptly above the postzygapophyses; (2) ventral portion of coracoid strongly medially deflected and decorated with delicate but profuse grooves (convergently acquired with Xixianykus); (3) fused scapulocoracoids (convergently acquired with Ceratonykus); (4) scapula with a very wide notch on the posterior margin of the bone; and (5) ilium and pubis fused. Oofamily Arriagadoolithidae nov. Diagnosis. As for the oo-genus, by monotypy. Included ootaxa. Arriagadoolithus patagoniensis oosp. nov., Kundrát, Novas, Agnolin and Powell; Triprismatoolithus stephensi Jackson and Varricchio, 2010. Arriagadoolithus patagoniensis oogen. et oosp. nov. Figs. 8e15

Fig. 5. Pelvic girdle elements of Bonapartenykus ultimus (holotype, MPCA, 1290). A, left pubis in lateral view. B, left ilium in lateral view. Abbreviations: cf, cuppedicus fossa; pb, pubic boot; pp, pubic pedicle of ilium. Scale bar represents 2.5 cm.

Derivation of name. Named in honor to Mr. Beto Arriagada, the owner of the Arraigada Farm in Río Negro Province, Argentina where the alvarezsaurid eggs and eggshell specimens were collected; the rest of the generic name derives from two Greek words oo relating to an egg or ovum, and lithos meaning a stone; patagoniensis, named after Patagonia. Holotype. MPCA, 1290, two partially preserved eggs and several isolated eggshells, associated with the holotype specimen of the alvarezsaurid theropod Bonapartenykus ultimus (Fig. 2).

Bonapartenykus ultimus on the basis of a very wide and deep notch on the caudal margin of the scapular blade, and the coracoid in which the ventral portion is strongly deflected medially and decorated with delicate but profuse grooves (see Diagnosis). MGPIFD-GR 177, consists of a highly distorted right femur originally described as belonging to Iguanodontia (Coria et al., 2007). The specimen differs from ornithopods in lacking a pendant fourth trochanter and a basitrochanteric fossa, suggesting its exclusion from Iguanodontia or Ornithopoda (Coria and Salgado, 1996). The specimen is reminiscent of the femur of Patagonykus in having a relatively welldeveloped and ridge-like fourth trochanter and associated muscle scar. Regrettably, most the shaft of the femur in the holotype of Bonapartenykus is highly distorted; thus, the morphology of the fourth trochanter is unknown. However, MGPIFD-GR 177 further resembles Bonapatenykus in having a very large and rugous proximal bulge for the m. iliofemoralis externus. In this way, it is probable that the specimens described by Salgado et al. (2009) may, in fact, belong to Bonapartenykus, and that they may pertain to a single individual, on the basis of similar size and preservation. Locality and horizon. Salitral Ojo de Agua, Río Negro Province, northwestern Patagonia, Argentina (Fig. 1). This specimen was found in fluvial sandstones belonging to the Upper levels of the Allen Formation (CampanianeMaastrichtian; Upper Cretaceous; Martinelli and Forasiepi, 2004). This locality has yielded a large variety of non-avian dinosaurs, including remains of ornithischian

Diagnosis. The unique combination of following microstructure characters distinguish Arriagadoolithus from remaining egg-types: three layers (external, prismatic, mammillary) of distinct calcite texture in eggs with a diameter of ca. 70 mm (?maximum width) and unknown length; average value of eggshell thickness 1 mm; variable ornamentation of the outer shell surface including low irregularshaped nodes, isolated node-like ridges, and low long ridges interconnected with each other to form a net, thus the combination of plexi-ramo-tuberculate and unique dendro-reticulate ornament may represent autapomorphic character of this oospecies; microlaminated external layer (90e100 mm) with two distinct textures; unevenly distributed squamate texture in the prismatic layer; visible prismatic columns, tubocanaliculate and obliquicanaliculate pore system with funnel-like openings on the outer surface; large pneumatic canals expanded into spatial chambers (up to 270 mm in diameter) within the prismatic layer (this latter feature may represent an autapomorphy of this oospecies); prismatic to mammillary layer thickness ratio 4.9:1 to 4.4:1.

4. Description Based on extrapolations on Mononykus (Perle et al., 1994), the presumed total length of the skeleton of Bonapartenykus was approximately 2.5 m long.



5

Fig. 6. Left femur of Bonapartenykus ultimus (holotype, MPCA, 1290) in A, lateral, B, cranial and C, medial views. Abbreviations: ct, cranial trochanter; fh, femoral head; gt, greater trochanter; ms, muscle scar. Scale bar represents 5 cm.

4.1. Dorsal vertebra (Fig. 3) An incomplete mid-dorsal vertebra is available. This is identified as mid-dorsal because the parapophyses are located on the laterodorsal corner of the cranial articular surface, the high transverse compression of the centrum, the craniocaudally extended neural spine, and the deeply excavated infradiapophyseal laminae. The vertebra is poorly preserved, lacking most of the centrum. The diapophyses, and parapophyses are worn, and the former lack its distal ends. The hypantrum is broken. The neural spine does not preserve its original margins. The centrum lacks pleurocoels, as occurs in other alvarezsaurids (Choiniere et al., 2010). The cranial articular surface of the centrum is deeply concave and surrounded by a sharp bony margin, contrasting with the nearly flat surface present in Patagonykus (Novas, 1997) and Haplocheirus (Choiniere et al., 2010), and with the opisthocoelous condition seen in Mononykinae, such as Mononykus and Shuvuuia (Chiappe et al., 2002). In this way, the condition of the cranial articular surface of the centrum suggests that mid-dorsal vertebrae of Bonapartenykus may be procoelous, a condition that contrasts with other alvarezsaurians. The neural spine is transversely thick and subrectangular in contour, being proportionally taller than in Mononykinae, but resembling the condition seen in more basal forms such as Haplocheirus (Choiniere et al., 2010). Both pre- and postspinal fossae are very deep, as also occurs in Mononykus and Patagonykus (Perle et al., 1994; Chiappe et al., 2002). The spinopostzygapophyseal lamina is wide and thick, ending abruptly, and failing to reach the rear margin of the postzygapophysis, a feature unique to the new genus.

The neural canal is wide, being dorsoventrally low and transversely wide. The prezygapophyses are craniocaudally short and transversely wide in dorsal view, showing a subcircular contour and a shallow concavity at its caudal margin. The parapophyses are transversely narrow and dorsoventrally tall, connected to the margins of the cranial articular surface through a tiny ridge. The diapophyses are craniocaudally narrow, and connected to the parapophyses by a deep ridge, as also occurs in Patagonykus. The preserved portion of the centrodiapophyseal lamina indicates that it was craniocaudally wider than in other alvarezsaurids (e.g., Patagonykus, Mononykus; Perle et al., 1994; Novas, 1997). In dorsal view the postzygapophyses are ellipsoidal in contour, being transversely compressed. They show a notched caudal margin, contrasting with the gently convex condition seen in remaining alvarezsaurids, including Patagonykus (Novas, 1997). The postzygapophyses are transversely wide and cranicaudally shortened, superficially resembling Patagonykus (Novas, 1996, 1997). However, the postzygapophyses of Bonapartenykus lack the lateroventral projection autapomorphically exhibited by Patagonykus (Novas, 1997). The hyposphene is well developed, being dorsoventrally deep as in Patagonykus, thus contrasting with the condition of Mononykinae, in which the dorsals are devoid of hyposphenee hypantrum articulations (Chiappe et al., 2002). Both hyposphene laminae are dorsally connected by a thin transverse lamina, in contrast with maniraptorans, in which hyposphene laminae are not connected (Norell et al., 2001a,b). In Bonapartenykus the cranial surface of the hyposphene is well defined and ovoidal in contour. Several fossae are distributed at the base of the neural arch, and their position is almost coincident to that of Patagonykus (Novas, 1997).


6


Fig. 7. Left tibia of Bonapartenykus ultimus (holotype, MPCA, 1290) in A, cranial, B, lateral and C, caudal views. Abbreviations: cc, cnemial crest; ap, facet for the ascending process of the astragalus. Scale bar represents 5 cm.

Fig. 8. Arriagadoolithus patagoniensis, associated eggs of Bonapartenykus ultimus, (holotype, MPCA, 1290). A, external view of an incomplete egg. B, detail showing external ornamentation of the egg. Scale bar represents 1 cm in A, 5 mm in B.



A narrow but deep fossa lies caudal to the base of the prezygapophyses. Another deep, wide fossa is placed cranially to the centrodiapophyseal lamina. Finally, a wide fossa is lateral to the hyposphene and subdivided by a tiny dorsoventrally oriented ridge. 4.2. Scapulocoracoid (Fig. 4) Both scapulocoracoids are well preserved. The scapular blade is only represented by its proximal half. It is medially deflected, as also occurs in Alvarezsaurus (Bonaparte, 1991), whereas in remaining alvarezsaurids it is straight (Chiappe et al., 2002). This scapular blade is craniocaudally narrow and lateromedially compressed, with both cranial and caudal margins subparallel, as occurs in most alvarezsaurids (Chiappe et al., 2002). Along the caudal margin of the scapular blade, close to the glenoid cavity, there is a well-developed and proximodistally extended notch, a condition that superficially resembles Mononykus, although in the latter genus it is deeper and dorsoventrally narrower (Perle et al., 1994). The acromion in Bonapartenykus is broken, but its preserved margins allow reconstruction of its shape as subtriangular, a condition that is present in Maniraptora, Oviraptorosauria and other Alvarezsauridae; in most non-maniraptoran dinosaurs the acromion is truncated and proximodistally deep (Rauhut, 2003). The glenoid fossa is caudolaterally oriented, with prominent supraglenoid and subglenoid buttresses. The scapular portion of the glenoid is lateromedially expanded and wider than the coracoidal portion. The latter is dorsoventrally deep and transversely compressed. The scapular portion of the glenoid is perpendicular to the main axis of the coracoid, whereas the coracoidal portion is subparallel to the main axis of the bone. The coracoid is proximodistally shallow and craniocaudally long. Its ventral half is strongly medially flexed, a condition superficially reminiscent of Paraves (Norell et al., 2001a,b). The coracoid lacks a bicipital tubercle, as in other known alvarezsaurians (e.g. Patagonykus, Alvarezsaurus; Chiappe et al., 2002), with the single exception of Haplocheirus (Choiniere et al., 2010). The cranial margin of the coracoid is transversely thick, as in Patagonykus (Novas, 1997), and cranially truncated, as is diagnostic of Coelurosauria (Gauthier, 1986; Xu and Wang, 2003). Caudally, the coracoid is dorsoventrally low, and ends in an acute projection. The coracoidal foramen, placed near the glenoid facet, is wide and rounded in contour. Caudal to the glenoid fossa there are several ridges which may correspond to the insertion of the M. coracobrachialis brevis (Jasinoski et al., 2006). There is a longitudinal ridge along the lateral margin of the coracoid that delimitates two zones, a laterodorsal smooth surface and a medioventrally directed margin. The latter is strongly vermiculated laterally, whereas its medial surface is smooth. Although in Patagonykus a similar condition is present, the medial portion of the coracoid is not as strongly inflected medially as in Bonapartenykus, and its lateral surface shows only isolated and poorly developed anastomosed grooves (Novas, 1997). In other Alvarezsauridae (e.g., Alvarezsaurus, Mononykus; Bonaparte, 1991; Perle et al., 1994; Chiappe et al., 2002) the coracoid is transversely flattened, without a medial deflection or a longitudinal ridge. In Ceratonykus a very poorly developed and faintly defined ridge is present, being restricted to the caudal end of the bone (Alifanov and Barsbold, 2009); however, this crest is unlike that of Bonapartenykus and Patagonykus, being very probably a convergent trait. The medial margin of the bone is extremely thin dorsoventrally, and is medially curled; thus the medial margin of coracoid is slightly dorsally projected. 4.3. Pubis (Fig. 5A) Both proximal and distal ends of a right pubis are preserved. The pubic shaft is more laterally compressed and narrower

7

anteroposteriorly than in Patagonykus. It is slightly opisthopubic (ca. 85 from pubic pedicle of ilium) similar to the condition seen in Patagonykus, whereas in known Mononykinae it is strongly opisthopubic (Novas, 1997; Karhu and Rautian, 1996). In cranial view, the shaft is nearly straight, contrasting with the sigmoidal curvature in Patagonykus. The proximal end of the bone is poorly preserved. As in Patagonykus the pubic shaft lacks the caudal sulcus for the ischial articulation that is present in derived alvarezsaurids (Hutchinson and Chiappe, 1998). The condition of Bonapartenykus indicates that the ischium was not in contact with the pubis along all of its length. On its medial side, the distal end shows a small ridge on its cranial margin, which represents a reduced pubic apron, a plesiomorphy also exhibited by Patagonykus, but absent in more derived alvarezsaurids, such as Xixianykus, Parvicursor and Shuvuuia (Xu et al., 2010). The pubis shows a distal pubic boot, a plesiomorphy for alvarezsaurids, also present in Patagonykus (Novas, 1996). The preserved portion of boot indicates that it was strongly transversely compressed and craniocaudally short. The posterior margin of the boot appears to be rounded in side view, whereas in Patagonykus it is acute and strongly directed backwards (Novas, 1997). 4.4. Ilium (Fig. 5B) A small portion of the right ilium is preserved. The pubic pedicle is mediolaterally compressed and strongly fused with the pubis, a condition unique among alvarezsaurids. The cuppedicus fossa is reduced, as diagnostic of Alvarezsauridae (Novas, 1996). This fossa is shallow, transversely narrow, and elongate. Contrasting with Bonapartenykus and other basal alvarezsaurids, the reduction of the fossa is extreme in Alvarezsaurus and Parvicursorinae, in which it is totally absent (Chiappe et al., 2002). Above the cuppedicus fossa a low, wide, and smooth ridge exists, as in Alvarezsaurus (Martinelli and Vera, 2007). 4.5. Femur (Fig. 6) The preserved left femur lacks its distal end, and the proximal one is strongly abraded. The diaphysis is crushed and deformed, but appears to have been sub-cylindrical. The preserved portion of this bone indicates a stout and short femur, different from those of Asian alvarezsaurids (e.g., Mononykus, Parvicursor, Shuvuuia; Chiappe et al., 2002) and Alvarezsaurus (Bonaparte, 1991). The femoral head, as well as most of the cranial and greater trochanters were not preserved; however, the preserved portion of the base of the cranial trochanter indicates that it was separated from the greater trochanter by a cleft, as also occurs in Alvarezsaurus, Patagonykus, Xixianykus, and also probably in Achillesaurus (Martinelli and Vera, 2007; Xu et al., 2010). The base of the cranial trochanter indicates that it was similar to Patagonykus in general size and proportions, but appears to be more craniocaudally expanded. In lateral view, a large, sculptured bulge is present, which probably constitutes the scar for the insertion of the m. iliofemoralis externus (Carrano and Hutchinson, 2002). 4.6. Tibia (Fig. 7) Both proximal and distal extremes are poorly preserved, and the shaft is strongly distorted. This bone is very short and robust, being probably only slightly larger than the femoral length. The tibial shaft is laterally bowed, being different from the straight-shafted Mononykus (Perle et al., 1994), Shuvuuia (Suzuki et al., 2002), and Parvicursor (Karhu and Rautian, 1996), resembling in this aspect to Xixianykus (Xu et al., 2010). Only the base of the cnemial crest is preserved. It is more distally extended than in Patagonykus (Novas, 1997), being similar in this feature to Mononykus (Perle et al., 1994).


8




Lateral to the base of the cnemial crest there is a small bump, whereas in Mononykinae this bump is developed as a welldeveloped ridge (Chiappe et al., 2002; Xu et al., 2010). The distal end of the bone is strongly abraded, being craniocaudally compressed, as in other Alvarezsauridae. The medial ridge that bound the ascending process of the astragalus is well developed, a plesiomorphic feature absent from the remaining alvarezsaurids (e.g., Alvarezsaurus, Achillesaurus, Patagonykus, Mononykinae; Martinelli and Vera, 2007; Xu et al., 2010). 4.7. Eggs (Figs. 8e15) The geometry of the preserved portions of the two eggs suggests that another pole of the eggs might have been eroded away. There is no evidence to indicate that the eggs were originally symmetrical or asymmetrical; therefore, we consider that information about the overall shape of the Bonapartenykus eggs is currently unavailable. No embryonic remains have been found inside the two eggs using conventional computed tomography at the Museum of the Rockies (Jack Horner, pers. comm. to JEP). Two major patterns of surface ornament have been recognized in the Arriagadoolithus patagoniensis eggshell. The first is a network of randomly connected low ridges with nodes formed either along ridges or at positions where they cross each other. This pattern, called here dendro-reticulate ornament, might be specific to A. patagoniensis. Although found only in the eggshell fragments (Fig. 9A), the absence of dendro-reticulate ornament in the eggs themselves may be due to the fact that preserved polar surfaces exhibit extensive abrasion (Fig. 8A). The second is a combination of widely spaced low, irregularly shaped nodes and discontinuous nodal ridges, sometimes interconnected by lower rami. This pattern, called here the plexi-ramo-tuberculate, was recognized in the eggs (Fig. 8A) and the eggshell fragments (Fig. 9B). Magnification of the outer surface of the eggshell specimens revealed the distribution of micro-cracks and granulate surface texture (Fig. 9C) that are reminiscent of relief typical of the uppermost layer of ostrich eggshell, the cuticle (Fig. 9D). The shell of A. patagoniensis consists of three structural layers of calcite: external, prismatic, and mammillary layers (Fig. 9E). The total thickness of the eggshell ranges from 0.9 mm (measured from the internode area to the intercone concavity) to 1.2 mm (measured from top of the surficial node to the apex of the mammillary cone), with an average value of 1.0 mm (measured from the internode area to the apex of the mammillary cone). Energy dispersive X-ray (EDX) spectra were collected from the structural layers in order to find out about the chemical composition and taphonomy of the preserved shells of A. patagoniensis. While elemental composition throughout the central mammillae is consistent with calcite (Fig. 10A, E), the most distal mammillary spherulites, which are in contact with the prismatic layer, had been replaced with the silica (Fig. 10A, F). Extensive erosion of the calcite crystals visible at the interface of the external and prismatic layers (Fig. 10B) may be due to secondary intrusion of the silicon dioxide that led to large lateral deposits throughout this level (Fig. 10D, G).

9

Very diverse spectra were measured in miniature rocky objects that filled the pneumatic pores (Fig. 10C, D). These are dominated by either silica or the silicate-calcite mixture enriched with iron, aluminium, magnesium, bromine, and kalium (Fig. 10H, I), suggesting the presence of dolomite, haematite, and aluminates inside the pneumatic system of the A. patagoniensis shells. In conclusion, the EDX spectra and the SEM imaging are indicative of two taphonomic phenomena that led to recrystallization of primary carbonate matrix and its selective replacement along contact zones of the prismatic layer with the two other structural layers. Furthermore, the spectra suggest that shell calcite did not erode to make a significant contribution to the filling matrix; thus, expansion of the pneumatic canals within the prismatic layer reflects the original character of A. patagoniensis and that was not caused by gradual disintegration of the prisms. The pneumatic system of the A. patagoniensis shell is characterized by the presence of randomly distributed wide pneumatic canals that vary from perpendicular to oblique directions relative to the shell surface (tubocanaliculate and obliquicanaliculate pore system) (Fig. 9A, B). The canals exhibit a flared opening at the outer eggshell surface (Figs. 10C, D, 11A). In ostrich, both single outer pores and clusters of pores that open into a characteristic curved or branched system of shallow grooves are distributed on shell surface (Fig. 11B). The pneumatic canals in A. patagoniensis open only through individual pores on the outer surface; the pores are adjacent to a node or a ridge and open between the top and base of these surficial elevations. Although some of the openings preserved in the eggshell are plausibly larger (256 mm) than in the original condition (Fig. 11C), we suggest that diameters of 141 mm and 127 mm measured in intact outer pores of the vertical (Fig. 10C) and oblique (Fig. 10D) pneumatic canals, respectively, are more likely to reflect the original state. These diameters contrast strongly with the maximum limit of outer pore diameters in ostrich eggshell (Fig. 10D). In A. patagoniensis, both the oblique and vertical canals expand inside the prismatic layer to reach a diameter of 226e271 mm (Fig. 10C, D) that is far larger than most spacious sectors in pneumatic canal system in ostrich eggshell (Fig. 11F). In some cases, however, we found micro-canals traversing the external layer at the surface of the node that are only 7 mm wide (Fig. 10E). We tentatively interpret these as pneumatic canals rather than burrowing traces because of the funnel-like appearance of the pore and rugose relief of the lumen. Notably, pore openings exposed at the inner surface of A. patagoniensis (Fig. 11G) appear to be quite similar in size to those of ostrich (Fig. 11H). The mammillary layer, which is the innermost of the three structural layers of calcite, exhibits closely packed cones (mammillae). These mammillae consist of acicular crystallites radiating from the former organic cores (Fig. 12A). Owing to the intrusion of silica described above, it is possible to recognize the contact zone between the mammillary and overlying prismatic layer only at certain locations (Fig. 12B). We estimate that the thickness of the mammillary layer falls within the interval 150e170 mm, calculated on most distally extended mammillary spherulites that are found in contact with tabular prisms (Fig. 12A).

Fig. 9. AeC, E, Arriagadoolithus patagoniensis, a new dinosaur ooparataxon associated with skeletal remains of the alvarezsaurid theropod Bonapartenykus ultimus from the Allen Formation, Río Negro, Argentina. D, eggshell sample from the recent ostrich, Struthio camelus, for comparative purposes. A, the fossil eggshell sample showing ornament on its outer surface, which consists of irregular low branching ridges arranged in a net-like pattern; the dendro-reticulate ornament. Note the distribution of large pore openings. B, fossil eggshell sample showing ornament consisting of low, irregularly shaped nodes, isolated discontinuous ridges, and relief patterns intermediate between these; the plexi-ramo-tuberculate ornament. Note the distribution of large and smaller pore openings. C, enlargement of the outer surface of the fossil eggshell showing micro-cracks (black arrow) and surface texture (white arrow); these features may indicate the presence of the cuticle layer in Arriagadoolithus patagoniensis. D, enlargement of the ostrich eggshell showing the cracked outer surface (black arrows) of the cuticle and its surface texture (white arrow). E, radial view of the broken eggshell sample showing three structural layers: mammillary, prismatic and external, viewed under the SEM. Upper black bar on the left-hand side of the image points to contact between external and prismatic layers; lower black bar indicates approximate transition from prismatic to mammillary layer. Note the ridge (left side) and the node (right side) on the eggshell surface. Abbreviations: crr, crossing ridges; oopp, outer opening of pneumatic pore; rea, ridge-enclosed area; in, isolated node; ir, isolated ridge.




The contact between the two calcite layers is rather gradual because some spherulites may extend deeper into the prismatic zone than others. Blade-like crystallites of the spherulite grade into the long, splayed wedges. The crystallite cleavage planes of adjacent mammillary cones intersect at acute angles and form an intricate interlacing pattern. The mammillary cones display an incomplete apex in samples selected from the eggshell clusters. Although the cones bear clear marks of erosion, visible throughout the inner surface, some show relatively intact concavities inside a porous crystallite matrix of radial micro-architecture (Fig. 12C). These fossil patterns correspond to those in recent birds in which mammillae are cratered because of calcium resorption in order to sustain advanced ossification of embryonic skeleton at late stages of in-ovo development (Fig. 12D, G). Based on these similarities, we suggest that the analyzed eggshells of A. patagoniensis had also been cratered in the same way to provide calcium for the embryonic skeleton, and are derived either from hatched egg or egg that contained a late stage alvarezsaurid embryo. It has remained unclear, however, whether the eggs associated with the Bonapartenykus bones represent the preservation of the adult alvarezsaurid above laid eggs, hence indicating brooding behaviour in alvarezsaurid theropods, as reported for Troodon (Varricchio et al., 1997, 1999) and oviraptorids (Norell et al., 1995; Dong and Currie, 1996; Clark et al., 1999; Grellet-Tinner and Chiappe, 2004). No nest structure had been observed in the excavated area; thus this interpretation seems to be implausible. Alternatively, the assemblage of Bonapartenykus bones þ two eggs may represent an alvarezsaurid containing eggs prior to oviposition. Such an interpretation has been proposed for an assemblage of oviraptorosaurian bones þ two eggs from the Upper Cretaceous of China (Sato et al., 2005). The presence of only two eggs might be in favour of this hypothetical explanation. The prismatic layer is approximately 740 mm thick. The calculated prismatic to mammillary layer thickness ratio ranges from 4.9:1 to 4.4:1. The prismatic layer consists of closely packed prismatic columns (Fig. 12E), variably shaped along the vertical aspect of the layer. The single prismatic column displays a combination of tabular texture and very fine lamination (at least 26 per 2 mm) with presence of vesicles (Fig. 12F). Squamatic texture can be seen locally in the upper part of the prismatic layer (Fig. 12G) where it may obscure the columnar pattern. The individual margins of the prismatic columns are also hardly seen in proximity to the mammillary layer, mostly owing to moderate diagenetic alteration and extensive replacement of calcite prisms by silica. These conditions prevent contacts between prismatic columns and mammillary spherulites from being seen along a larger exposure than is normally visible in unaltered specimens (Fig. 12H). The external layer is separated by abrupt contact with the underlying prismatic layer (Fig. 13A). The contact is somewhat obscured by intrusion of silica at some locations. However, the two layers differ in their microstructure (Fig. 13B). The thickness of the external layer varies mostly between 90 and 100 mm. The layer itself

11

consists of minute blocky crystals (columns). Surface texture visible on the broken plane suggests that two different microstructural units (sub-layers) can be recognized. The upper sub-layer is characterized by a crystalline texture that is more pronounced in a vertical direction, although the separate columns show welldeveloped horizontal laminae. In the lower sub-layer, horizontal lamination dominates over vertical emargination, and is continuous throughout the faint columns (Fig. 13C, D). The width of the columns varies from 25 to 26 mm. The sharp interface separates the two sub-layers and is of particular interest here as series of micropores associated with two micro-objects have been detected (Fig. 13E, F). Squamous micro-objects consist mainly of calcite and silica; however, aluminium and arsenic are present in this mixture as well (Fig. 13G). This may explain how non-calcite matrix might have infiltrated the lower sub-layer and spread laterally along the contact zone with the prismatic layer. On the other hand, these micropores could equally have made it possible for microorganisms to enter the external layer. Putative candidates for these are globular micro-objects (1 mm), which consist of calcite and silica with a high content of nitrogen, iron (presumably represented by haematite) and aluminium (likely bounded into aluminate) (Fig. 13H). A thin layer of fibrous texture has been found to underlie the mammillary layer in shell samples selected among the clustered eggshells (Fig. 14A). The layer consists of a dense plexus of randomly oriented fibre-like structures accreted to the basalmost surface of mammillary conuses (Fig. 14B, C). EDX spectra collected from these fibrous objects show considerably higher content of carbon (Fig. 14H, I) than is present in calcite of the mammillary layer (Fig. 10E). Silica, iron, and aluminium are also present as minor components. Notably, an amorphous mineralized matrix has been also detected to underlie the mammillary conus in A. patagoniensis (Fig. 14D). Based on the EDX spectrum, it is composed of pure calcite with a significantly high allotment of carbon (Fig. 14J). The fibrous structures are similar in morphology and topography to the shell membrane in recent birds (Fig. 14EeG), as well as to objects that were interpreted as permineralizaed remnants of the shell membrane in dinosaur eggs (Sochava, 1969; Kolesnikov and Sochava, 1972; Kohring, 1999; Varricchio et al., 2002; Grellet-Tinner, 2005). It is unclear, however, if the higher contents of carbon detected in the alvarezsaurid permineralized shell membrane represent organic residues of the original shell membrane, or are derived from bacteria that facilitated fossilization of the membrane fibres (see Folk and Lynch, 2001). As we did not find such high concentrations of carbon in other parts of the eggshell equally exposed to prospective contamination by recent organic carbon, we assume that the high carbon fraction in the alvarezsaurid eggshell refers to a contemporaneous fossil organic source. This may not be true for the amorphous mineralized matrix the EDX spectrum and SEM imaging, which indicates that the high allotment of carbon could refer to an accumulation and permineralization of a secondary organic carbon after fossilization of the eggshell.

Fig. 10. Energy dispersive X-ray (EDX) analysis of the Arriagadoolithus patagoniensis samples from the Allen Formation, Río Negro, Argentina. Numbered asterisks indicate locations where the EDX spectrum was collected from. Note that the gold peak (Au) present in all collected spectra is due to coating applied prior to SEM imaging and EDX analysis. A, E, F, mammillary layer within the mammillary cone; A, SEM micrograph, black asterisk marks spot 1 within the mammillary cone: measured spectrum E, elemental composition is consistent with calcite; white asterisk marks spot 2 within the secondary matrix that replaced distal spherulites: measured spectrum F, note the high peak of silicium and oxygen, and significant absence of carbon and calcium suggesting that elemental composition may correspond to silica. B, G, mammillary layer; B, SEM micrograph, white asterisk marks spot 3 within the secondary matrix that replaced calcite at the external/prismatic interface: measured spectrum G, elemental composition is identical to that of spectrum F. C, H, vertical pneumatic canal (with a funnel shaped outer opening); C, SEM micrograph, white asterisk marks spot 4 within the secondary filling matrix transported from outside: measured spectrum H: note significantly high silicium and bromine mixed with lower kalium, calcium and oxygen, and missing carbon. This suggests that eggshell calcite did not erode to contribute to the filling matrix. D, I, oblique pneumatic canal; D, SEM micrograph of the oblique pneumatic canal, white asterisk marks spot 5 within the secondary filling matrix: measured spectrum I: note the wide range of elements, which may indicate the presence of calcium, dolomite, hematite, aluminate, silica and/or silicate. This suggests that majority of the filling came from outside, whereas the calcite component may be partly derived from the eggshell. Abbreviations: EL, external layer; MC, mammillary cone; ML, mammillary layer; PC, pneumatic canal; PL, prismatic layer.


12




In addition, two small fungal assemblages have been found on the inner surface of the expanded part of pneumatic canal in A. patagoniensis (Fig. 15A). Both assemblages include permineralized linear and branching villose hyphae, globular to ovoid objects of different size (500 nme4 mm) referred here to conidia, and putative echinulate conidia with attachment points (Fig. 15BeD). The fossilized fungi probably represent only a small fraction of real population that contaminated an egg of Bonapartenykus ultimus, as can be seen in fossil turtle eggs from Lower Cretaceous of China (Jackson et al., 2009), and in the recent ostrich egg containing an embryo at a late stage of development (Fig. 15E, F). We suggest that the fossilized fungi were contemporaneous organisms with the Bonapartenykus ultimus and contaminated its eggs while containing organic components. 5. Discussion 5.1. Phylogenetic position and affinities of Bonapartenykus ultimus The phylogenetic analysis here performed (Fig. 16) indicates that the new taxon could be assigned to Coelurosauria on the basis of the slender, elongated scapular blade, the cranially truncate coracoid, and the flat cranial surface of the distal end of the tibia (Gauthier, 1986; Rauhut, 2003; Xu and Wang, 2003; Supplementary Information part 2). Its referral to Alvarezsauridae is based on the following derived features: (1) fossa cuppedicus of ilium reduced (Novas, 1996); (2) pubic apron absent or reduced to a tiny ridge (Novas, 1997; Hutchinson and Chiappe, 1998); (3) strongly laterally compressed proximal end of the pubis (Chiappe et al., 2002); (4) coracoid without bicipital tubercle (Chiappe et al., 2002); and (5) glenoid cavity laterocaudally oriented (Chiappe et al., 2002; Supplementary Information part 2). Within Alvarezsauridae, we infer sister-group relationships between Bonapartenykus and Patagonykus on the basis of two unambiguous synapomorphies: the presence of a strongly vermiculated ventral half of the coracoid, which is also medially tilted (ch. 422-1, 423-1; Supplementary Information part 2). Nevertheless, Bonapartenykus shows some plesiomorphic features that appears to be absent in Patagonykus and Parvicursorinae, such as the presence of a strongly concave cranial articular surface of the middorsal vertebra. In addition, Bonapartenykus and Patagonykus retained several plesiomorphies that are absent from Parvicursorinae, including: subvertical pubis with extensive distal pubic boot, pubic shaft with pubic apron reduced but still present, pubic shaft subtriangular in cross-section, caudal margin of proximal extreme of pubis devoid of a longitudinal sulcus for the ischium, and hypospheneehypantrum additional articulations which are well developed on dorsal vertebrae. Additionally, Bonapartenykus shows a plesiomorphic proximal end of femur, with both trochanters separated by a deep cleft, a condition also documented in other South American alvarezsaurids (i.e., Alvarezsaurus, Achillesaurus, Patagonykus), but which is absent in the Mononykini, in which both

13

trochanters are firmly fused to form a trochanteric crest (Xu et al., 2010). In this way, we conclude that Bonapartenykus represents the sister group of Patagonykus, both taxa being basal members of non-Parvicursorinae Alvarezsauridae. 5.2. Alvarezsaurian nomenclature and phylogeny The present analysis allows us to propose some nomenclatorial changes regarding alvarezsaurid taxonomy. Choiniere et al. (2010) suggested that the name of the superfamily rank Alvarezsauroidea Livezey and Zusi (2007) was originally defined as the clade containing Patagonykus, Alvarezsaurus and Mononykus. In their usage, Alvarezsauroidea is synonymous with Alvarezsauridae Bonaparte, 1991 as defined by Novas (1996); thus, Choiniere et al. (2010) re-defined Alvarezsauroidea as the most inclusive clade sharing a more recent common ancestor with Alvarezsaurus calvoi than with Passer domesticus. However, such a phylogenetic group would be better called Alvarezsauria, as originally proposed by Bonaparte, 1991, in order to emphasize this morphologically distinctive theropod group. As a result, it is considered here that the clade name Alvarezsauroidea Livezey and Zusi, 2007 is a junior synonym of Alvarezsauria. Within Alvarezsauria, the Alvarezsauridae consists of two main clades: Patagonykinae and (Alvarezsaurus þ Parvicursorinae). Patagonykinae nov. is coined here in order to include the genera Patagonykus and Bonapartenykus, both large and plesiomorphic genera that are restricted to the Upper Cretaceous of Patagonia. Achillesaurus manazzonei Martinelli and Vera (2007) from the Santonian of North Patagonia was not included in the present analysis because of its fragmentary condition. However, Achillesaurus resembles Patagonykinae in the general morphology of the proximal femur, the presence of a subcircular lateral depression on cranial half of the centrum in proximal caudals (shared with Patagonykus), and a transversely compressed and cranially protruding medial condyle of the astragalus (Martinelli and Vera, 2007). Although these features are not considered here as synapomorphic of Patagonykinae, their combination suggests that Achillesaurus may belong to the latter clade. The clade Alvarezsaurus þ Parvicursorinae is sustained on the basis of two synapomorphies: cuppedicus fossa on the ilium absent (318-2), and pedal phalanges of digit IV shortened (420-0). However, both features are variable among alvarezsaurids and may not be as phylogenetically informative as indicated by the present analysis. As a result, it is probable that Alvarezsaurus may be positioned as a very basal alvarezsaurid, more basal than Patagonykus (or Patagonykinae), as proposed by previous authors (Novas, 1996, 1997; Chiappe et al., 1998, 2002; Martinelli and Vera, 2007; Longrich and Currie, 2009; Xu et al., 2010, 2011). Parvicursorinae is the clade containing Parvicursor, Mononykus and their most common ancestor, following the definition employed by Choiniere et al. (2010; see also Xu et al., 2010). The Parvicursorinae Karhu and Rautian, 1996 has been regarded as the senior synonym of Mononykinae Chiappe, Norell, and Clark, 1998 by some authors (e.g., Choiniere et al., 2010; Xu et al., 2010). On

Fig. 11. A, C, E, G, pneumatic patterns of the eggshell in the Arriagadoolithus patagoniensis samples from the Allen Formation, Río Negro, Argentina. B, D, F, H, eggshell samples of the recent ostrich, Struthio camelus, for comparative purposes. A, SEM micrograph showing a pore opening exposed at the outer surface of the fossil eggshell; note the opening is situated between the top and base of the surface ridge. B, SEM micrograph showing high density in distribution of pore openings at the outer surface of the ostrich eggshell; note individual pores and slit-like openings that consist of several coalescent pores. C, SEM micrograph showing detailed view of the pore opening of the fossil eggshell exposed on side of the surface node; note the large size of the pore, which reaches 256 mm in diameter. D, SEM micrograph showing detailed view of the single pore opening of the ostrich eggshell; note the funnel shaped opening that gives the pore an uppermost diameter of 31 mm, whereas it is only 17 mm wide at the base of the funnel; note also the presence of pinholes on the outer surface surrounding the pore owing to natural weathering or/and bacterial activity. E, SEM micrograph showing a micro-canal traversing the external layer at the surface node; note that the canal is only 7 mm wide. We interpret it as a pneumatic canal rather than a burrowing trace due to the funnel-like appearance of the pore (white arrow) and rugose relief of the lumen. F, SEM micrograph of the cluster of pneumatic canals that exit together into a slit-like pore opening of the ostrich eggshell (see Fig. 11 B); note that the canals are vertical, having a variable diameter (here from 13 to 57 mm), and may divide (black arrow) or fuse (white arrow). G, SEM micrograph showing pore openings (black arrows) exposed between mammillary cones at the inner surface of the fossil eggshell. H, SEM micrograph showing pore openings (black arrows) exposed at the inner surface of the ostrich eggshell; note the rosette arrangement of mammillary cones around each opening. Abbreviations: EL, external layer; MC, mammillary cone; pc, pneumatic canal; sn, surficial node; sr, surficial ridge.


14




the basis of its original designation, Chiappe et al. (1998) phylogenetically defined Mononykinae as the clade including the common ancestor of Mononykus, Shuvvuia, and Parvicursor plus all of its descendants. Under this definition, Mononykinae is a junior synonym of Parvicursorinae. However, in the present paper we opt to re-define Mononykinae in order to retain this widely employed name for Mononykus and its kin (e.g., Chiappe et al., 1998, 2002; Suzuki et al., 2002; Naish and Dyke, 2004; Kessler et al., 2005; Longrich and Currie, 2009). As a consequence, we rename Mononykinae as Mononykini comb. nov., and phylogenetically define it as the theropod group that includes taxa more nearly related to Mononykus than to Parvicursor, Patagonykus and Alvarezsaurus. Hence, the Mononykini exhibit a single synapomorphy: the presence of a medial cnemial crest on the proximal tibia (ch 383-1), a condition unknown in more basal taxa, including Xixianykus and Patagonykus. The Mononykini is currently composed of the genera Shuvuuia, Mononykus and Albertonykus (Longrich and Currie, 2009; Choiniere et al., 2010; Xu et al., 2010). Recently, Xu et al. (2011) described the parvicursorine alvarezsaurid Linhenykus monodactylus as the basalmost member of the Parvicursorinae. However, in the present analysis this taxon is recovered as a derived member of the group. In fact, it is considered to be more derived than Ceratonykus and Xixianykus in having metatarsal IV subequal in length with metatarsal II (ch 415-0). Moreover, it may be included within Mononykini because it shows a medial cnemial crest on tibia (ch 383-1). Finally, Linhenykus was recovered as the sister group of Shuvuuia on the basis of the presence of relatively long pedal phalanges on digit IV (ch 420-0). As a result, Linehnykus is here considered to be a derived member of Parvicursorinae, in contrast with the more basal position proposed by Xu et al. (2011). Within Parvicursorinae, the present analysis yielded a monophyletic group formed of Ceratonykus oculatus Alifanov and Barsbold, 2009, Albinykus baatar Nesbitt et al., 2011, and Xixianykus zhangi Xu et al., 2010, from early Late Cretaceous deposits in Mongolia and China (Alifanov and Barsbold, 2009; Xu et al., 2010; Nesbitt et al., 2011). These taxa share an extensive fusion of metatarsals and distal tarsals (ch. 404-1, 405-1; see Supplementary Information part 2), in spite of its minute body size. This clade is here termed as Ceratonykini nov., and is coined to include Xixianykus, Ceratonykus, its more recent common ancestor, and all of its descendants. This new clade includes small and gracile taxa basal to other Parvicursorinae, being the sister group of Mononykini. Choiniere et al. (2010) suggested that the Alvarezsauria suffered a pattern of miniaturization in its evolution, as also occurred in the clade Paraves. The present phylogeny reinforces this hypothesis. In fact, Haplocheirus, is recovered as the basalmost Alvarezsauria, being followed by the large alvarezsaurid clade Patagonykinae, which includes very large alvarezsaurids, ca. 2.5 m long (Novas,

15

1997). By contrast, the more derived alvarezsaurid clade Alvarezsaurus þ Parvicursorinae includes very small to minute forms that are not more than 1 m long (Choiniere et al., 2010). More recently, the putative alvarezsaurid Kol ghuva Turner et al., 2009 was described on the basis of a complete foot from the Upper Cretaceous of Mongolia (Turner et al., 2009). These authors proposed alvarezsaurid affinities for this taxon, although their assumption was only based on the following putative alvarezsaurid apomorphy: development of deep and proximally expanded extensor pits on the phalanges of digit 4 (ch. 421-1; Turner et al., 2009; see also Nesbitt et al., 2011). However, this morphology is also present in the Oviraptoridae, for example, in Ingenia (Barsbold, 1981). Moreover, Turner et al. (2009) considered that Kol was very similar to the basal oviraptorosaurian Avimimus, although they distinguished both taxa because the latter lacks the proximal fusion of metatarsals seen in Kol. However, the presence or absence of proximal fusion of metatarsals is highly variable among different genera within Oviraptorosauria, including some basal taxa in which metatarsals are proximally fused, and more derived forms in which the proximal extremity of metatarsals is unfused (Osmólska et al., 2004). Another presumable alvarezsaurid trait present in Kol is that metatarsal III does not reach the ankle (Turner et al., 2009). However, this condition may also be corroborated in the basal oviraptorosaurians Elmisaurus and Avimimus (Kurzanov, 1981; Osmólska, 1981). Hence, the alvarezsaurid affinities for Kol may be regarded as lacking strong morphological evidence. Nevertheless, Kol is more reminiscent of oviraptorosaurians than alvarezsaurids in having a prominently developed flexor tubercle on pedal unguals, a metatarsal II that is shorter than metatarsals II and IV, and lacks a dorsomedial flange on the medial side, and a metatarsal III that extends more proximally than one-half of the total metatarsal length (see Turner et al., 2009). Moreover, Kol resembles taxa of the Oviraptorosauria clade Caenagnathoidea in having an arctometatarsalian metatarsus (Osmólska et al., 2004). As a result, we consider that the phylogenetic position of Kol is still uncertain; further research is required in order to elucidate its phylogenetic affinities. The inclusion of Kol in our data matrix results in an unresolved phylogenetic position for the taxon, and the collapse of most maniraptoran lineages. Hence, the incomplete nature of the only known specimen of Kol does not allow inclusion of this taxon within the present phylogenetic analysis, and its phylogenetic position within Coelurosauria may be regarded as uncertain. 5.3. Pectoral girdle reconstruction of Bonapartenykus Bonapartenykus exhibits very peculiar scapulocoracoid morphology. In fact, as occurs in Patagonykus, the coracoid shows its ventral half to be medially deflected, and with an extremely thin

Fig. 12. AeC, E, F, microstructure patterns of the mammillary and prismatic layers of Arriagadoolithus patagoniensis and D, G, H, the ostrich eggshell for comparative purposes. A, SEM micrograph showing broken surface of mammillary cone that represents the basic unit of the mammillary layer in the fossil eggshell. Fine radiating calcite crystals emanate from a central core (white asterisk), and broaden distally to form blade-like crystals of the spherulite, which grade into the long and splayed wedges of the mammillae (white arrow); note that crystallites of adjacent cones interlace (black arrow). The radiating spherulites extend deeper into prismatic zone than others (black arrowhead). The contact between the mammillary and prismatic layers is defined here by the presence of tabular prisms (white arrowhead), and is evidently gradual. B, SEM micrograph showing the closely spaced mammillary cones of the fossil eggshell with the cratered apex (white arrow). C, SEM micrograph of the eroded inner surface of the fossil eggshell showing the cratered apex of the mammillae (white arrow) in tangential view; visible margins of the mammillae suggest that the cone may reach 150 mm in diameter. Note the internal pore openings, indicated by black arrows, partly filled with sediment. D, SEM micrograph of the inner surface of the ostrich eggshell showing closely packed slender mammillae and inner pore openings (black arrows) in tangential view. Note the cratered apex (white arrow) due to resorption of calcium for ossification of embryonic skeleton: the eggshell sample was collected from the ostrich egg with a 40-day-old embryo (close to hatching) inside it. E, SEM micrograph showing broken surface that represents the prismatic layer of the fossil eggshell; outer eggshell surface is at the top of the image. Black arrows indicate borders between prismatic columns indicated by the black arrows; note that the interface between the columns is not always perfectly vertical and can either converge (white arrowheads) or even fuse (black arrowhead) to each other. Note the squamatic texture (white arrows) that occurs in the upper part of prismatic layer. F, enlargement of the prismatic column of the fossil eggshell showing tabular structure (white arrow) including very fine horizontal lamination (black arrow); note the presence of vesicles (within black circle) in the prism. G, SEM micrograph showing broken surface of mammillary cones in the ostrich eggshell. Note cratering of the cone apex (white asterisk) and advanced degradation of basal part of radiating spherulites owing to calcium uptake by developing embryo: the eggshell sample was collected from the ostrich egg with a 35-day-old embryo inside it. H, SEM micrograph showing the irregular contact between the mammillary layer and overlying prismatic layer in the ostrich eggshell; note the irregular transition between the two layers (black arrowheads). Black arrows indicated the margins of a prismatic eggshell unit. The mammillary cones are slender and closely spaced. Abbreviations: MC, mammillary cone; ML, mammillary layer; PL, prismatic layer.


16




medial rear that is slightly wrapping dorsally. The ventral half of the coracoid, in both Patagonykus and Bonapartenykus shows a deeply vermiculate sculpture, a condition more developed in the latter genus. This peculiar ornamentation probably correlates with some skin structures, as noted in other tetrapods. In living vertebrates, skin coupled with soft keratinization and non-specialized dermal architecture lacks any bony correlation. By contrast, cornified specialized structures show clear correlatations with bone surface ornament and texture. In Bonapartenykus (and to a lesser degree in Patagonykus) the ventral surface of the coracoid is decorated by anastomosing and dichotomous grooves and rugosities. This pattern of grooves and rugosities has been interpreted to be related to highly cornified skin (Hieronymus et al., 2009). However, in Bonapartenykus the absence of oblique neurovascular foramina, and a “lip” at the transition with smooth bone areas, precludes its assignation to a cornified sheath (Hieronymus et al., 2009). It also differs from cornified pads owing to the absence of profuse neurovascular foramina and a pitted surface (Hieronymus et al., 2009). In addition, cornified scales are also rejected, because of the lack of the hummocky rugosity on the bone surface that is diagnostic of such structures (Hieronymus et al., 2009). As a result, although the rugosities and grooves present in the ventral half of the coracoid of Bonapartenykus and Patagonykus appear to be related to some kind of skin cornification, its correlation with any particular epidermal structure is not possible at present. Sternal morphology and relationships of this bone with the pectoral girdle are poorly known in non-avian theropod dinosaurs. In coelurosaurs, the presence of large and ossified sternal plates has often been regarded as diagnostic of the clade Paraves þ Oviraptorosauria (Maryánska et al., 2002). In addition, an ossified sternum has also been reported in Alvarezsauridae (Perle et al., 1994). In the remaining coelurosaurs the presence of ossified sterni is so far uncertain. These structures were mentioned or briefly described for some puntual taxa (e.g., Barsbold and Osmólska, 1990; Pérez Moreno et al., 1994; Dal Sasso and Signore, 1998), but most of these previous reports have been dismissed recently (Holtz et al., 2004). Plesiomorphically, in theropods the coracoids articulate along the lateral margin of the sternum (Paul, 2002). In Maniraptorans, including Oviraptorosauria and Paraves, the sternum apomorphically articulates with the coracoids on its craniolateral margin (Paul, 2002; Lü et al., 2005). In alvarezsaurids the sternum is only properly known in Mononykus (Perle et al., 1994) and Linhenykus (Xu et al., 2011), whereas in Shuvuuia it is known only from the dorsally exposed sternal plate (Sereno, 2001). The sternum in Mononykus is an elongate, narrow bone with a deep median carina (Perle et al., 1994). This bone has not preserved any sign of coracoidal articular surfaces, the articulation of the sternum with the coracoids in Mononykus being still unknown (Perle et al., 1994). Chiappe et al. (2002) indicated that the long sternal margin of the coracoid articulated with the craniolateral portion of the sternum in Shuvuuia. However, Chiappe et al. (2002) based their observation on a single specimen (MGI

17

100/977) in which the coracoids are displaced, and not articulated with the sternum; hence, the articulation between the two bones in Shuvuuia is still uncertain (Sereno, 2001). In Linhenykus the sternum was not found articulated with the scapular girdle; thus, its articulation with the coracoid is unknown (Xu et al., 2011). Based on this evidence it is clear that the actual articulation between the sternum and coracoid in alvarezsaurids remains unknown. In Bonapartenykus both scapulocoracoids are nearly complete, and allow reconstruction of some details regarding pectoral girdle articulation and relationships between its bones within alvarezsaurids. In Bonapartenykus the coracoid is extremely elongate. It becomes progressively narrower caudally, ending in a caudally acute rod. This acute end is unlikely to have allowed an articulation with the sternum, lacking the flat, stepped caudal articular margin seen in most maniraptorans (Lü et al., 2005). Contrasting with most other theropods, in Bonapartenykus and Patagonykus the coracoid shows a medially deflected ventral half, a condition considered here as diagnostic of Patagonykinae (see above). This medial deflection ends medially in a thin, slightly dorsally curled margin, which shows a nearly smooth surface, contrasting with the rugose texture exhibited by the rest of the bone. Based on this morphology and texture, this narrow, smooth area is here considered to be the articular surface for the sternum. Hence, it is highly probable that the coracoids of alvarezsaurids articulated the sternum along its lateral margin, as suggested by Chiappe et al. (2002) for Shuvuuia, thus retaining the plesiomorphic condition of Dinosauria (Paul, 2002). In patagonykines, especially Bonapartenykus, the medial deflection of the coracoid forms a subhorizontal shelf. If the coracoids and sternum articulated along its longitudinal margin, as proposed here, then the medial deflection of the coracoids formed a continuous subhorizontal surface with the sternal plate. This combination of characters suggests that alvarezsaurids possessed a flat and wide breast, a morphology that appears to be unique to alvarezsaurids, yet unreported in other theropod dinosaurs. 5.4. Glenoid and forelimb morphology and its implications in alvarezsaurid ecology The morphology of the glenoid of the pectoral girdle appears to be nearly correlated with theropod forelimb function and range of mobility (Senter, 2008). Owing to its highly modified nature, the capability of movement of the alvarezsaurid forelimb is still a matter of debate. Some authors (Bonaparte, 1991; Sereno, 2001) proposed that alvarezsaurid forelimbs were highly reduced, and forelimb movements were severely restricted. On the other hand, other authorities (Senter, 2008; Longrich and Currie, 2009) proposed that alvarezsaurid forelimbs were capable of a large array of movements. Bonapartenykus possess a very well-preserved pectoral girdle that will possibly shed some light on this debated topic. Originally, the glenoid of Alvarezsauridae was considered by Bonaparte (1991) as proportionally small and poorly developed,

Fig. 13. Microstructure patterns of the external layer of Arriagadoolithus patagoniensis. A, SEM micrograph showing tri-laminate structure of the fossil eggshell, which includes the well-defined external layer. B, SEM micrograph showing a detailed view of the external layer (93 mm), which consists of minute blocky crystals; white arrows indicate borders between individual units. The broken surface indicates the presence of two structural sub-layers, being equal in thickness: upper sub-layer (EL/1) with more vertical aspect of crystalline texture expressed, and lower sub-layer (EL/2) with crystalline texture of more horizontal aspect. Note that the upper part of the blocky crystals consists of well-defined laminae (black arrows). C, SEM micrograph showing two sub-layers of the external layer with a well- laminated (black arrows) lower sub-layer (62 mm) being twice as thick as the overlying upper sub-layer (31 mm). Note the basal extension of borders between individual units owing to partial diagenetic alteration. D, SEM micrograph showing another sample of two equally thick sub-layers of the external layer; note a sharp interface (white arrowhead) between the two sub-layers. The blocky crystals show well-preserved laminae (black arrows) in the upper sub-layer. Although this pattern becomes obscure in the underlying sub-layer, extensions of the crystal borders can be followed (white arrows). E, enlargement of the interface region between the two sub-layers indicated by the white arrowhead in Fig. 5 D; note the presence of micropores (white arrows) going through the calcium substrate of the external layer (white asterisk, 1), and two different objects, smaller squamous (black arrowhead, 2) and larger rounded (black asterisk, 3) inside the micropores. FeH, EDX analysis of the external layer. F, EDX analysis consistent with calcite. G, EDX analysis indicates that the squamous objects are secondary infiltration owing to the presence of silica, aluminium, and arsenic. H, EDX analysis differs from others in having peaks of iron and nitrogen, which might indicate that the rounded objects represent fossilized biological structures. Note that the gold peak (Au) present in all collected spectra is a result of coating applied prior to SEM imaging and EDX analysis. Abbreviations: EL, external layer; EL/1, upper part of external layer; EL/2, lower part of external layer; ML, mammillary layer; PL, prismatic layer.


18




which was indicative of highly reduced forelimbs, an assumption based on the incomplete information available from the single known skeleton of Alvarezsaurus. Moreover, the posteroventrally oriented glenoid suggested to Bonaparte (1991) that Alvarezsaurus possessed a reduced forelimb with limited movement (Bonaparte, 1991). Posteriorly, Perle et al. (1994) described in detail the skeleton of Mononykus olecranus. In this genus the forelimb bones are extremely thick, short and robust, the carpometacarpus is extremely short, massive, and subquadrangular, without an intermetacarpal space. The non-ungual phalanges of digit II are very stout and show robust proximal processes, as well as very deeply excavated and sharply defined distal and proximal articular surfaces. Perle et al. (1994) suggested that the enlarged deltopectoral crest of the humerus, the huge olecranon of the ulna, the short and massive forelimb elements, and robust II digit were indicative of strong movements of the forelimb. Nevertheless, as noticed by Perle et al. (1994), the relationships between the articular surfaces of the different forelimb elements strongly restricted movements of the arm in alvarezsaurids. More recently, Senter (2008) analyzed in detail the function of forelimbs in alvarezsaurids. Based on anatomical grounds, he concluded that the movements of alvarezsaurid forelimbs were mainly restricted to the parasagittal plane. In this way, Senter (2008) stated that in Mononykus the humerus has a limited anteroposterior movement of an arc of 23 , the antebrachium functioned as a single unit, flexing only 21, and that the carpals possessed highly restricted movement. In addition, he indicated that in Mononykus, the glenoid has switched to the plesiomorphic saurischian orientation (this is a posteroventrally facing glenoid), but the modification of the humeral head enabled the humerus to move through the transverse plane. However, as pointed out by Novas (1996), the humerus in alvarezsaurids exhibits the humeral head with its major axis ventrolaterally inclined with respect to the main axis of the bone, and an olecranal fossa on its distal end is lacking (Novas, 1996; Chiappe et al., 2002). This peculiar morphology may not have allowed the humerus to have important fore-aft movements, as recognized by Senter (2008). In addition, Senter (2008) indicated that the distal forelimb of alvarezsaurids reoriented its proximal elements, so that the palm faced down; thus, the movements of distal forelimb were parasagittal. By contrast, in other theropods the palm of the manus is oriented medially (Sereno, 1999). Senter (2008) suggested that although most forelimb elements were of restricted mobility, the first digit was able of swing in a large arc. By contrast, a detailed analysis by Sereno (2001) has indicated that owing to their articular morphology, metacarpal-phalangeal joints showed a restricted arc, with a maximum extension of less than 15 . This condition was considered by Suzuki et al. (2002) as probably comparable to birds, in which the carpus-metacarpus severely limited phalangeal mobility. Longrich and Currie (2009) proposed that the cup-shaped humeral articular surface of ulna, which articulated with the distal and enlarged ball-like condyle of the humerus (Perle et al., 1994) may have allowed great mobility to the alvarezsaurids

19

forelimbs. However, the same condition is also recognized for living flightless ratite birds, in which the hand are extremely reduced and nearly lack any function (Lowe, 1928; McGowan, 1982). Some authors (Perle et al., 1994; Longrich and Currie, 2009) have indicated that the presence of an enlarged olecranon may be also considered as evidence of powerful movements in alvarezsaurid forelimbs (Longrich and Currie, 2009). However, most flightless living birds with useless forelimbs show a very large olecranon in the ulna (Olson, 1973); moreover, the extinct flightless phororhacoid bird Paraphysornis had a very large olecranon, comparable in some respects to the alvarezsaurid olecranon (Alvarenga, 1982). As a result, the anatomical evidence indicative of powerful movements in alvarezsaurid forelimbs is here considered to be dubious at least. On the contrary, based on the articular morphology of the forelimb elements, the mobility of the forearms in alvarezsaurids, including the fore-aft movements, was severely restricted. Mainly on the basis of forelimb anatomy, Senter (2008) concluded that Mononykus was capable both of scratch-digging to make depressions and of hook and pull behaviour consistent with a diet of insects that make tough earthen nests or live inside palms (Senter, 2008). In this way, he and later Longrich and Currie (2009) reported several traits present in alvarezsaurids that suggest that this theropod clade was mainly myrmecophagous. These characters include (1) an anterior diastema in front of the jaws, (2) reduced and simplified teeth, (3) long and narrow jaws, (4) weak mandibles, and (5) reduced jaw articulations; all these features were regarded as present in mostly myrmecophagous taxa as, for example, in the mammalian clade Xenarthra. The features 1, 2 and 5 are characters that are widely distributed among xenarthrans, being usually regarded as synapomorphies of the entire clade (Engelmann, 1985; see Gaudin and McDonald, 2006); moreover, traits 3 and 4 are also found in all known Dasypodidae xenarthrans (Gaudin and McDonald, 2006), as recognized by Longrich and Currie (2009). It is worth mentioning that the only strictly myrmecophagous xenarthrans known hitherto are the living species of the clade Myrmecophagidae (Nowak, 1991). As a result, owing to its widespread condition, all the features employed by Longrich and Currie (2009) in order to suggest myrmecophagous diet in alvarezsaurids are highly ambiguous. These characters are not exclusive to anteaters; they are present among different groups of xenarthrans, including the follivorous tree sloths (characters 1, 2 and 5; Nowak, 1991), and the omnivorous (mainly carnivorous) dasypodids (characters 1e5; McDonough and Loughry, 2006). Hence, since all these traits are present in clades that show a great disparity in dietary habits, we conclude that there is no unambiguous evidence to demonstrate myrmecophagous habits for Alvarezsauridae.

5.5. Alvarezsaurid egg morphology and phylogenetic implications The eggs described here are clearly distinct from the spherical eggs with a distinct shell units and granular surface produced by

Fig. 14. AeD, shell membrane of Arriagadoolithus patagoniensis and EeG, ostrich eggshell for comparative purposes. A, H, I, fossilized remnants of the shell membrane that underlies the mammillary layer. A, SEM micrograph showing position of fossilized remnants of the shell membrane. H, I, EDX spectra of the shell membrane, note the almost consistent elemental composition dominated by carbon (1 and 2). The gold peak (Au) present in all collected spectra is a result of coating applied prior to SEM imaging and EDX analysis. B, Enlargement of the B-boxed region in Fig. 14 A showing the interface between crystalline matrix of the mammillary cone and a thin layer of randomly oriented fibre-like structures (black arrows). C, enlargement of the C-boxed region in Fig. 14 A showing the base of mammillary cones coated by a layer of fibrous consistency (black arrows) that is reminiscent of the shell membrane in modern birds. D, J, amorphous matrix (white arrow) underlying the mammillary cone (compare with Fig. 14 G); the white cross indicates the location from which the EDX spectrum J was collected. D, SEM micrograph of the amorphous matrix underlying the mammillary cone. J, EDX spectrum J; note the significantly high peak of carbon in comparison with those of calcium, oxygen and aluminuim. E, detailed view of protein fibers arranged in a network of overlying layers of the shell membrane in ostrich eggshell. F, SEM micrograph showing the interface between the base of mammillary cones, the inner opening of pneumatic canals and the shell membrane in ostrich eggshell. G, SEM micrograph showing the amorphous matrix of albumen (black arrow) that underlies the shell membrane in ostrich eggshell. Abbreviations: MC, mammillary cone; ML, mammillary layer; SM, shell membrane; PC, pneumatic canal; PL, prismatic layer.


20


Fig. 15. AeD, fungi present in the eggshell of Arriagadoolithus patagoniensis and E, F the ostrich eggshell for comparative purposes. A, SEM micrograph showing location of fossilized fungi (circled region) found on the inner surface of the pneumatic canal. B, C, detailed view of the fossilized fungal mass; note permineralized conidia and villose hyphae dispersed within two different areas the circled region in Fig. 15A. D, enlargement of the boxed region in Fig. 15C showing a small, young conidium connected to a larger semi-mature conidium by a fibre-like hypha; note another large conidium with a structured surface that may represent an echinulate conidium (white arrow) with attachment point (black arrow). E, SEM micrograph showing invasion of fungi distributed within the pneumatic canal of the eggshell in ostrich. F, detailed view of young conidia arranged in chains found inside the pneumatic canal of the eggshell in ostrich. Abbreviations: cd, conidium; EL, external layer; hy, hypha; PC, pneumatic canal; PL, prismatic layer; smcd, semi-mature conidium; sn, surficial node; ycd, young conidium.



Fig. 16. Strict consensus cladogram showing the phylogenetic interrelationships of alvarezsaurid theropods. Abbreviations: Alvarez., Alvarezsauria; Pat., Patagonykinae; Cer., Ceratonykini.

titanosaurian sauropods, and abundantly represented in the same stratigraphic unit (see Carpenter, 1999; Coria et al., 2010). The eggs of Arriagadoolithus have been considered previously by other authors as elongathoolithid eggs, mainly on the basis on their external ornament. It may be pointed out, that based on its relative abundance; Salgado et al. (2009) speculated that some of these Elongatoolithus-type eggs pertained to alvarezsaurid species, a hypothesis that is corroborated here on the basis of associated skeletaleegg material. The ornamentation patterns expressed on the outer shell surface of A. patagoniensis are most reminiscent of those seen in Elongatoolithus and Macroelongatoolithus oospecies (Zhao, 1975; Mikhailov, 1994; Li et al., 1995; Zelenitsky et al., 2000; Jin et al., 2007), Continuoolithus canadensis (Zelenitsky et al., 1996), and Triprismatoolithus stephensi (Jackson and Varricchio, 2010). However, A. patagoniensis substantially differs from all Elongathoolithidae and C. canadensis by the presence of three structural layers of calcite, deferring the surface ornament and other characters (e.g., shell thickness mammillary/prismatic layer thickness ratio of 1:5 in Elongatoolithus; Zhao, 1975; see also Wang et al., 2010) to secondary importance. Moreover C. canadensis, unlike A. patagoniensis, displays evenly distributed squamatic texture in the prismatic layer. Arriagadoolithus patagoniensis shares three structural layers of calcite with Prismatoolithus levis (Varricchio and Jackson, 2004; Jackson et al., 2010), T. stephensi, the Lourinhanosaurus eggs (see Varricchio and Jackson, 2004), the?avian theropod from the Willow Tank Formation, USA (Bonde et al., 2008), and basal birds from Gobi (Grellet-Tinner and Norell, 2002) and Patagonia (Schweitzer et al., 2002). Arriagadoolithus patagoniensis is also similar to P. levis, T. stephensi and the Lourinhanosaurus eggs on account of the irregular squamatic texture in the prismatic layer, prismatic columns that comprise the prismatic layer, and gradual transition from the mammillary to the prismatic layer. The Lourinhanosaurus eggs, like those of Bonapartenykus, possess markedly wide pneumatic canals that are oblique to the shell surface (Hirsch, 1994; Mateus et al.,1997). Unlike P. levis (Varricchio et al., 2002; Varricchio and Jackson, 2004), A. patagoniensis and T. stephensi are similar in having low, tubercle-type ornamentation of the other shell surface, a laminated external layer with two different textures, an abrupt rather than a gradual contact between the external and prismatic layers, prismatic columns with a tabular structure, a mammillary/prismatic layer thickness ratio of about 1:5, and large pore openings up to 140 mm; finally, the both oospecies display cracking patterns on the outer shell surface that resemble cuticle in eggs of modern birds. The two taxa differ in such minor characters as reticulation of the surface ornamentation, specific textures of the two units

21

recognized in the external layer, and the range in size of pore openings. The eggs of T. stephensi are symmetrical whereas the overall shape is unknown for A. patagoniensis. Apparently, based on the above comparisons, Arriagadoolithus patagoniensis shares numerous characters with Triprismatoolithus stephensi. The unique combination of characters found in the two oospecies is quite derived from other known ootaxa. Therefore, we suggest that both oogenera be included in their own ooparafamily, the Arriagadoolithidae. Arriagadoolithus patagoniensis, which has large eggs (? 70 mm) and a thick eggshell (1000 mm), would therefore represent the robust arraigadoolithid type in comparison to T. stephensi, which has considerably smaller eggs (30 75 mm) with a thinner eggshell (525 mm). Having established a direct link between Arriagadoolithus patagoniensis and Bonapartenykus ultimus, it is possible to speculate that the oospecies Triprismatoolithus stephensi may tentatively belong to an unknown alvarezsaurid or to a closely related taxon, currently represented by the four eggs from the lowermost section of Two Medicine Formation in Montana, USA (Jackson and Varricchio, 2010). Paired arrangements of eggs in the nest (e.g., Zelenitsky and Hills, 1996; Zhao et al., 1999) of some theropods have been interpreted as evidence for two functional oviducts in Troodon and oviraptorids (Sabath, 1991; Varricchio et al., 1997). Preservation of the two eggs in the Patagonian alvarezasaurid implies that Bonapartenykus might have evolved a bilateral oviductal function as well. Remarkably, this may also be true for T. stephensi, known from two pairs of eggs discovered in situ (Jackson and Varricchio, 2010). Egg fossils have been hitherto been ascribed to five groups of non-avian theropods: oviraptorids (Norell et al., 1994, 1995, 2001; Grellet-Tinner et al., 2006), troodontids (Varricchio et al., 1997, 2002; Bever and Norell, 2009; Weishampel et al., 2008), dromaeosaurids (Makovicky and Grellet-Tinner, 2000), allosauroids (Hirsch, 1994; Antunes et al., 1998) and therizinosauroids (Kundrát et al., 2008). Alvarezsaurids thus represent another taxon to be added to this growing list. 5.6. Palaeobiogeographical implications Bonapartenykus represents the youngest record for the Alvarezsauridae in South America. Previously reported South American alvarezsaurids came from pre-Santonian beds (see Novas, 1996). This indicates the survival of this clade up to the latest Cretaceous on this continent. In spite of its young age, Bonapartenykus shows a combination of plesiomorphic traits absent from latest Cretaceous Parvicursorinae, but present in older alvarezsaurids; curiously, basal Alvarezsauridae were reported hitherto only from South America. This, together with the older age of Argentinean specimens led Novas (1996, 1997) to propose a South American origin of the group. However, the recent finding of a Jurassic basal Alvarezsauria indicates that the clade probably had its centre of origin in Asia (Choiniere et al., 2010; Xu et al., 2011). Novas (1996) also proposed that alvarezsaurids probably migrated from South to North America and then to Eurasia (Novas, 1996; Kessler et al., 2005; Choiniere et al., 2010). Martinelli and Vera (2007) suggested that the exclusively South American genera Alvarezsaurus, Patagonykus, and Achillesaurus constituted a ConiacianeSantonian basal radiation of Alvarezsauridae, and that the derived Parvicursorinae were absent from South America, a fact also corroborated by the finding of the basal alvarezsaurid Bonapartenykus. Curiously, in South America there appears to have been a Late Cretaceous survival of stem Alvarezsauridae, whereas they became extinct in northern continents, probably being replaced by derived Parvicursorinae. In fact, in Eurasia, in contrast to the conservative Gondwanan forms, alvarezsaurids suffered a large array of


22


osteological modifications that were in parallel with bird morphology (e.g., presence of a carpometacarpus, opisthopubic pelvis and a rod-like pubis and ischium; Perle et al., 1993; Novas, 1996; Xu et al., 2011). In contrast to Novas (1996, 1997; see also Longrich and Currie, 2009; Choiniere et al., 2010), the presence of parvicursorine alvarezsaurids in North America may not be explained in terms of migration from South America (see Hutchinson and Chiappe, 1998). As a result, based on the presence of basal alvarezsaurids in South America, the occurrence of derived Parvicursorinae in North America is better explained as reflecting an arrival from Asia, where highly derived parvicursorine alvarezsaurids were rather abundant and well represented. The presence of elongatoolithid-like eggs in Europe has been considered by some authors as indicative of the possible presence of Oviraptorosauria there (Amo Sanjuán et al., 2000; Canudo, 2006). However, the present report indicates that eggs externally similar to Elongatoolithidae are not exclusive of Oviraptorosauria and appear to be more widespread among Coelurosauria. As a consequence, elongatoolithid-like ornamented eggs from Europe may belong to Therizinosauroidea, Oviraptorosauroidea, or Alvarezsauria, a fact that weakens the putative presence of oviraptorosaurians in Europe. From the same locality and horizon where the known specimens of Bonapartenykus ultimus were collected, Salgado et al. (2009) also reported several incomplete and fragmentary specimens representing a large and plesiomorphic alvarezsaurid. Some of the specimens (MGPIFD-GR 166, 177, 184) are here referred to Bonapartenykus ultimus. However, some elements differ from the latter in lacking hypospheneehypantrum accessory articulations on vertebrae (Salgado et al., 2009). Salgado et al. (2009) considered these specimens to belong to a form probably related to Patagonykus based on general resemblance, a criterion with which we agree. Hence, it is probable that at least two different large and plesiomorphic alvarezsaurids coexisted at the same time and locality, indicating that they were probably more diverse and speciose than previously thought. Acknowledgements We thank Martín Ezcurra, who made useful comments on early drafts of the manuscript; Peter Makovicky, who helped us with the interpretation of several bones of the holotype of Bonapartenykus; Agustín Scanferla and Diego Pais for their help with the figures. Martin Kundrat thanks Per Ahlberg (Uppsala University, Sweden) for his support and funding provided through a Linnaeus Framework Grant, "The Genomics of Phenotypic Diversity in Natural Populations", awarded by Vetenskapsrådet (the Swedish Research Council). We also thank the editor David Batten for his detailed review of the manuscript. Appendix. Supplementary material Supplementary data related to this article can be found online at doi:10.1016/j.cretres.2011.11.014. References Alifanov, V.R., Barsbold, R., 2009. Ceratonykus oculatus gen. et sp. nov., a new dinosaur (?Theropoda, Alvarezsauria) from the Late Cretaceous of Mongolia. Paleontological Journal 43, 94e106. Alvarenga, H., 1982. Uma gigantesca ave fóssil do Cenozoico brasileiro: Physornis brasiliensis sp. n. Anais Academia Brasileira de Ciencias 54, 697e712. Amo Sanjuán, O., Canudo, J.I., Cuenca-Bescós, G., 2000. First record of elongatoolithid eggshells from the Lower Barremian (Lower Cretaceous) of Europe (Cuesta Corrales 2, Galve Basin, Teruel, Spain). First International Symposium on Dinosaur Eggs and Babies, extended abstracts, pp. 7e14.

Antunes, M.T.P., Taquet, P., Ribeiro, V., 1998. Upper Jurassic dinosaur and crocodile eggs from Pai Mogo nesting site (Lourinha e Portugal). Memorias da Academia das Ciencias de Lisboa 37, 83e99. Barsbold, R., 1981. The toothless carnivorous dinosaurs of Mongolia. Sovmestnaya Sovetsko-Mongolskaya Paleontologichekaya Ekspeditsia Trudy 15, 28e39. Barsbold, R., Osmólska, H., 1990. Ornithomimosauria. In: Weishampel, D.B., Dodson, P., Osmólska, H. (Eds.), The Dinosauria. University of California Press, Berkeley, CA, pp. 225e244. Bever, G., Norell, M.A., 2009. The perinate skull of Byronosaurus (Troodontidae) with observations on the cranial ontogeny of paravian theropods. American Museum Novitates 3657, 1e51. Bonaparte, J.F., 1991. Los vertebrados fósiles de la Formación Río Colorado, de la ciudad de Neuquén y cercanías, Cretácico superior, Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Paleontología 6, 17e123. Bonde, J.W., Varricchio, D.J., Jackson, F.D., Loope, D.B., Shirk, A.M., 2008. Dinosaurs and dunes! Sedimentology and paleontology of the Mesozoic in the Valley of Fire State Park. In: Duebendorfer, E.M., Smith, E.I. (Eds.), Field Guide to Plutons, Volcanoes, Faults, Reefs, Dinosaurs, and Possible Glaciation in Selected Areas of Arizona, California, and Nevada. Geological Society of America, Field Guide 11, pp. 249e262. Canudo, J.I., 2006. La ambigüedad paleobiogeográfica de los dinosaurios ibéricos durante el Cretácico Inferior. III Jornadas Internacionales sobre Paleontología de Dinosaurios y su Entorno, pp. 21e54. Carrano, M.T., Hutchinson, J.R., 2002. Pelvic and hindlimb musculature of Tyrannosaurus rex (Dinosauria: Theropoda). Journal of Morphology 253, 207e228. Carpenter, K., 1999. Eggs, Nests, and Dinosaur Babies: A Look at Dinosaur Reproduction, Indiana University Press, Bloomington. Chiappe, L.M., Norell, M.A., Clark, J.M., 1998. The skull of a new relative of Mononykus. Nature 392, 275e278. Chiappe, L.M., Norell, M.A., Clark, J.M., 2002. The Cretaceous, short-armed Alvarezsauridae. Mononykus and its kin. In: Chiappe, L.M., Witmer, L.M. (Eds.), Mesozoic Birds: Above the Heads of Dinosaurs. Berkeley University Press, Berkeley, CA, pp. 87e120. Choiniere, J.N., Xu, X., Clark, J.M., Forster, C.A., Guo, Y., Han, F., 2010. A basal alvarezsauroid theropod from the early Late Jurassic of Xinjiang, China. Science 327, 571e574. Clark, J.M., Norell, M.A., Chiappe, L.M., 1999. An oviraptorid skeleton from the Late Cretaceous of Ukhaa Tolgod, Mongolia, preserved in an avian-like brooding position over an oviraptorid nest. American Museum Novitates 3265, 1e36. Coria, R.A., 2001. A new theropod from the Late Cretaceous of Patagonia. In: Tanke, D.H., Carpenter, K. (Eds.), Mesozoic Vertebrate Life. Indiana University Press, Bloomington, IN, pp. 3e9. Coria, R.A., Salgado, L., 1996. “Loncosaurus argentinus” Ameghino 1899 (Ornithischia, Ornithopoda): a revised description with comments on its phylogenetic relationships. Ameghiniana 33, 373e376. Coria, R.A., Salgado, L., 2001. South American ankylosaurs. In: Carpenter, K. (Ed.), The armoured dinosaurs. Indiana University Press, Bloomington, IN, pp. 159e168. Coria, R.A., Salgado, L., 2005. Last patagonian non-avian theropods. In: Carpenter, K. (Ed.), Carnivorous dinosaurs. Indiana University Press, Bloomington, IN, pp. 153e160. Coria, R.A., Cambiaso, A.V., Salgado, L., 2007. New records of basal ornithopod dinosaurs in the Cretaceous of North Patagonia. Ameghiniana 44, 473e477. Coria, R.A., Salgado, L., Chiappe, L.M., 2010. Multiple dinosaur egg-shell occurrence in an Upper Cretaceous nesting site from Patagonia. Ameghiniana 47, 107e110. Dal Sasso, C., Signore, M., 1998. Exceptional soft-tissue preservation in a theropod dinosaur from Italy. Nature 392, 383e387. Dong, Z.-M., Currie, P.J., 1996. On the discovery of an oviraptorid skeleton on a nest of eggs at Bayan Mandahu, Inner Mongolia, People’s Republic of China. Canadian Journal of Earth Sciences 33, 631e636. Engelmann, R.M., 1985. The phylogeny of the Xenathra. In: Montgomery, G.C. (Ed.), The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington DC, pp. 51e64. Folk, R.L., Lynch, F.L., 2001. Organic matter, putative nannobacteria and the formation of ooids and hardgrounds. Sedimentology 48, 215e229. Gaudin, T.J., McDonald, H.G., 2006. Morphology-based investigations of the phylogenetic relationships among extant and fossil xenarthrans. In: Vizcaíno, S.F., Loughry, W.J. (Eds.), The Biology of the Xenarthra. Florida University Press, Gainesville, FL, pp. 11e23. Gauthier, J., 1986. Saurischian monophyly and the origin of birds. In: Padian, K. (Ed.), The Origin of Birds and the Evolution of Flight. California Academy of Sciences, San Francisco, CA, pp. 1e55. Goloboff, P.J., Farris, J., Nixon, K., 2008. A free program for phylogenetic analysis. Cladistics 24, 774e786. Grellet-Tinner, G.L., 2005. Membrana testacea of titanosaurid dinosaur eggs from Auca Mahuevo (Argentina): implication for exceptional preservation of soft tissue in Lagerstätten. Journal of Vertebrate Paleontology 25, 99e106. Grellet-Tinner, G.L., Norell, M.A., 2002. An avian egg from the Campanian of Byan Dzak, Mongolia. Journal of Vertebrate Paleontology 22, 719e721. Grellet-Tinner, G., Chiappe, L.M., 2004. Dinosaur eggs and nestings: implications for understanding the origin of birds. In: Currie, P.J., Koppelhus, E.B., Shugar, M.A., Wright, J.L. (Eds.), Feathered Dragons: Studies on the Transition from Dinosaurs to Birds. Indiana University Press, Bloomington, IN, pp. 185e214.


F.L. Agnolin et al. / Cretaceous Research xxx (2012) 1e24 Grellet-Tinner, G., Chiappe, L.M., Norell, M., Bottjer, D., 2006. Dinosaur eggs and nesting behaviours: a paleobiological investigation. Palaeogeography, Palaeoclimatology, Palaeoecology 232, 294e321. Hieronymus, T.L., Witmer, L.M., Tanke, D.H., Currie, P.J., 2009. The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record 292, 1370e1396. Hirsch, K.F., 1994. Jurassic eggshell from the Western Interior. In: Carpenter, K., Hirsch, K.F., Horner, J. (Eds.), Dinosaur Eggs and Babies. Cambridge University Press, Cambridge, pp. 137e150. Holtz, T.R., Jr., Molnar, R.E., Currie, R.E., 2004. Basal Tetanurae. In: Weishampel, D.B., Dodson, P., Osmólska, H. (Eds.), The Dinosauria. University of California Press, Berkley, CA, pp. 98e135. Huene, F.V., 1920. Bemerkungen zur Systematik und Stammesgeschichte einiger Reptilien. Zeitschrift für induktive Abstammungslehre Vererbungslehre Lehre 24, 162e166. Hutchinson, J.R., Chiappe, L.M., 1998. The first known Alvarezsaurid (Theropoda: Aves) from North America. Journal of Vertebrate Paleontology 18, 447e450. Jackson, F.D., Varricchio, D.J., 2010. Fossil eggs and eggshell from the lowermost Two Medicine Formation of Western Montana, Sevenmile Hill locality. Journal of Vertebrate Paleontology 30, 1142e1156. Jackson, F.D., Horner, J.R., Varricchio, D.J., 2010. A study of a Troodon egg containing embryonic remains using epifluorescence microscopy and other techniques. Cretaceous Research 31, 255e262. Jackson, F.D., Jin, X., Schmidt, J.G., 2009. Fungi in a Lower Cretaceous turtle egg from China: evidence of ecological interactions. Palaios 24, 840e845. Jasinoski, S.C., Russell, A.P., Currie, P.J., 2006. An integrative phylogenetic and extrapolatory approach to the reconstruction of dromaeosaur (Theropoda: Eumaniraptora) shoulder musculature. Zoological Journal of the Linnean Society 146, 301e344. Jin, X., Azuma, Y., Jackson, F.D., Varricchio, D.J., 2007. Giant dinosaur eggs from the Tiantai basin, Zhejiang Province, China. Canadian Journal of Earth Sciences 44, 81e88. Karhu, A.A., Rautian, A.S., 1996. A new family of Maniraptora (Dinosauria: Saurischia) from the Late Cretaceous of Mongolia. Paleontological Journal 30, 583e592. Kessler, E., Grigorescu, D., Csiki, Z., 2005. Elopteryx revisited e a new bird-like specimen from the Maastrichtian of the Hat¸eg Basin (Romania). Acta Palaeontologica Romaniae 5, 249e258. Kohring, R.R., 1999. Calcified shell membranes in fossil vertebrates eggshell: evidence for preburial diagenesis. Journal of Vertebrate Paleontology 19, 723e727. Kolesnikov, C.M., Sochava, A.V., 1972. A paleobiochemical study of the Cretaceous dinosaur eggshell from the Gobi. Paleontological Journal 2, 235e245. Kundrát, M., Cruickshank, A.R.I., Manning, T.W., Nudds, J., 2008. Embryos of therizinosauroid theropods from the Upper Cretaceous of China: diagnosis and analysis of ossification patterns. Acta Zoologica 89, 231e251. Kurzanov, S.M., 1981. On the unusual theropods from the Upper Cretaceous of Mongolia. Sovmestnaya Sovetsko-Mongolskaya Paleontologichekaya Ekspeditsia Trudy 15, 39e50. Li, Y., Yin, Z., Liu, Y., 1995. The discovery of a new genus of dinosaur egg from Xixia, Henan, China. Journal of the Wuhan Institute of Chemical Technology 17, 38e41. Livezey, B.C., Zusi, R.L., 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnean Society 149, 1e95. Longrich, N.R., Currie, P.J., 2009. Albertonykus borealis, a new alvarezsaur (Dinosauria: Theropoda) from the Early Maastrichtian of Alberta, Canada: implications for the systematics and ecology of the Alvarezsauridae. Cretaceous Research 30, 239e252. Lowe, P.R., 1928. Studies and observations bearing on the phylogeny of the ostrich and its allies. Proceedings of the Zoological Society of London 1928, 185e247. Lü, J., Huang, D., Qiu, L., 2005. The pectoral girdle and the forelimb of Heyuannia (Dinosauria: Oviraptorosauria). In: Carpenter, K. (Ed.), The Carnivorous Dinosaurs. Indiana University Press, Bloomington, IN, pp. 256e273. Makovicky, P.J., Grellet-Tinner, G., 2000. Association between theropod eggshell and a specimen of Deinonychus antirrhopus. In: Bravo, A.M., Reyes, T. (Eds.), Symposium of Dinosaur Eggs and Babies, Isona, Spain. Isona i Conca Della, Catalonia, pp. 61e76. Makovicky, P.J., Apesteguía, S., Agnolín, F.L., 2005. The earliest dromaeosaurid theropod from South America. Nature 437, 1007e1011. Marsh, O.C., 1881. Principal characters of American Jurassic dinosaurs. Part V. The American Journal of Science and Arts 21, 417e423. Martinelli, A.G., Forasiepi, A.M., 2004. Late Cretaceous vertebrates from Bajo de Santa Rosa (Allen Formation), Río Negro province, Argentina, with the description of a new sauropod dinosaur (Titanosauridae). Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia 6, 257e305. Martinelli, A.G., Vera, E., 2007. Achillesaurus manazzonei, a new alvarezsaurid theropod (Dinosauria) from the Late Cretaceous Bajo de la Carpa Formation, Río Negro Province, Argentina. Zootaxa 1582, 1e17. Maryánska, T., Osmolska, H., Wolsam, M., 2002. Avialian status for Oviraptorosauria. Acta Palaeontologica Polonica 47 (1): pp. 97e116. Mateus, I., Mateus, H., Antunes, M.T., Mateus, O., Taquet, P., Ribeiro, V., Manuppella, G., 1997. Couvée, oeufs et embryos d’un dinosaure théropode du Jurassique supérieur de Lourinha (Portugal). Comptes Rendus de l’Academie des Sciences, Paris 325, 71e78.

23

McDonough, C.M., Loughry, W.J., 2006. Behavioral ecology of the armadillos. In: Vizcaíno, S.F., Loughry, W.J. (Eds.), The Biology of the Xenarthra. Florida University Press, Gainesville, FL, pp. 281e293. McGowan, C., 1982. The wing musculature of the brown kiwi Apteryx australis mantelli and its bearing on ratite affinities. Journal of Zoology 1982, 173e217. Mikhailov, K.E., 1994. Theropod and protoceratopsian dinosaur eggs from the Cretaceous of Mongolia and Kazakhstan. Paleontological Journal 28, 101e120. Naish, D., Dyke, G.D., 2004. Heptasteornis was no ornithomimid, troodontid, dromaeosaurid or owl: the first alvarezsaurid (Dinosauria: Theropoda) from Europe. Neues Jahrbuch für Geologie und Paläontologie 7, 385e401. Nesbitt, S.J., Clarke, J.A., Turner, A.H., Norell, M.A., 2011. A small alvarezsaurid from the eastern Gobi Desert offers insight into evolutionary patterns in the Alvarezsauroidea. Journal of Vertebrate Paleontology 31, 144e153. Norell, M.A., Clark, J.M., Chiappe, L.M., 2001a. An embryonic oviraptorid (Dinosauria: Theropoda) from the Upper Cretaceous of Mongolia. American Museum Novitates 3315, 1e17. Norell, M.A., Clark, J.M., Makovicky, P., 2001b. Phylogenetic relationships among coelurosaurian theropods. In: Gauthier, J., Gall, L.F. (Eds.), New Perspectives on the Origin and Early Evolution of Birds. Proceedings of the International Symposium in Honor of John H. Ostrom. Peabody Museum of Natural History, New Haven, CT, pp. 69e98. Norell, M.A., Clark, J.M., Chiappe, L.M., Dashzeveg, D., 1995. A nesting dinosaur. Nature 378, 774e776. Norell, M.A., Clark, J.M., Dashzeveg, D., Barsbold, R., Chiappe, L.M., Davidson, A.R., McKenna, M.C., Novacek, M.J., 1994. A theropod dinosaur embryo, and the affinities of the Flaming Cliffs dinosaur eggs. Science 266, 779e782. Novas, F.E., 1996. Alvarezsauridae, Cretaceous maniraptorans from Patagonia and Mongolia. Memoirs of the Queensland Museum 39, 675e702. Novas, F.E., 1997. Anatomy of Patagonykus puertai (Theropoda, Maniraptora, Alvarezsauridae) from the Late Cretaceous of Patagonia. Journal of Vertebrate Paleontology 17, 137e166. Novas, F.E., Pol, D., Canale, J.I., Porfiri, J.D., Calvo, J.O., 2009. A bizarre Cretaceous theropod dinosaur from Patagonia and the evolution of Gondwanan dromaeosaurids. Proceedings of the Royal Society B 276, 1101e1107. Nowak, R.M., 1991. Walker’s Mammals of the world, Vol. 2. Johns Hopkins University Press, Baltimore, MD, 526 pp. Olson, S.L., 1973. Evolution of the rails of the South Atlantic Islands (Aves: Rallidae). Smithsonian Contributions to Zoology 152, 1e53. Osmólska, H.,1981. Coossified tarsometatarsi in theropod dinosaurs and their bearing on the problem of bird origins. Acta Palaeontologica Polonica 42, 79e95. Osmólska, H., Currie, P.J., Barsbold, R., 2004. Oviraptorosauria. In: Weishampel, D.B., Dodson, P., Osmólska, H. (Eds.), The Dinosauria. University of California Press, Berkeley, CA, pp. 165e183. Paul, G.S., 2002. Dinosaurs of the air. John Hopkins University Press, Baltimore, MD, 432 pp. Pérez Moreno, B.P., Sanz, J.L., Buscalioni, A.D., Mortalla, J.J., Ortega, F., RasskinGutman, D., 1994. A unique multitoothed ornithomimosaur dinosaur from the Lower Cretaceous of Spain. Nature 370, 363e367. Perle, A., Norell, M.A., Chiappe, L.M., Clark, J.M., 1993. Flightless bird from the Cretaceous of Mongolia. Nature 362, 623e626. Perle, A., Chiappe, L.M., Barsbold, R., Clark, J.M., Norell, M.A., 1994. Skeletal morphology of Mononykus olecranus (Theropoda: Avialae) from the Late Cretaceous of Patagonia. American Museum Novitates 310, 1e29. Powell, J.E., 1987. Hallazgo de un dinosaurio hadrosáurido (Ornithischia, Ornithopoda) en la Formación Allen (Cretácico superior) de Salitral Moreno, Provincia de Río Negro, Argentina. X Congreso Geológico Argentino, Vol. 3, pp. 149e152. Rauhut, O.W.M., 2003. The interrelationships and evolution of basal theropod dinosaurs. Special Papers in Palaeontology 69, 1e213. Sabath, K., 1991. Upper Cretaceous amniotic eggs from the Gobi Desert. Acta Palaeontologica Polonica 36, 151e192. Salgado, L., Coria, R.A., Arcucci, A.B., Chiappe, L.M., 2009. Restos de Alvarezsauridae (Theropoda, Coelurosauria) en la Formación Allen (CampanianoeMaastrichtiano), en Salitral Ojo de Agua, Provincia de Río Negro, Argentina. Andean Geology 36, 67e80. Sato, T., Cheng, Y.-N., Wu, X.-C., Zelenitsky, D.K., Hsiao, Y.-F., 2005. A pair of shelled eggs inside a female dinosaur. Science 308, 375. Schweitzer, M.H., Jackson, F.D., Chiappe, L.M., Schmitt, J.G., Calvo, J.O., Rubilar, D.E., 2002. Late Cretaceous avian eggs with embryos from Argentina. Journal of Vertebrate Paleontology 22, 191e195. Senter, P., 2008. Function in the stunted forelimbs of Mononykus olecranus (Theropoda) a dinosaurian anteater. Paleobiology 31, 373e381. Sereno, P., 1999. The evolution of dinosaurs. Science 284, 2137e2147. Sereno, P., 2001. Alvarezsaurids: birds or ornithomimosaurs? In: Gauthier, J., Gall, L.F. (Eds.), New Perspectives on the Origin and Early Evolution of Birds Proceedings of the International Symposium in Honor of John H. Ostrom. Peabody Museum of Natural History, New Haven, CT, pp. 29e98. Sochava, A.V., 1969. Dinosaur eggs from the Upper Cretaceous of the Gobi Desert. Paleontological Journal 3, 517e527. Suzuki, S., Chiappe, L.M., Dyke, G.J., Watabe, M., Barsbold, R., Tsogtbaatar, K., 2002. A new specimen of Shuvuuia deserti Chiappe et al. 1998 from the Mongolian Late Cretaceous with a discussion of the relationships of alvarezsaurids to other theropod dinosaurs. Los Angeles County Museum, Contributions in Science 494, 1e18.


24


Turner, A.H., Nesbitt, S.J., Norell, M.A., 2009. A large alvarezsaurid from the Late Cretaceous of Mongolia. American Museum Novitates 3648, 1e14. Varricchio, D.J., Jackson, F.D., 2004. A phylogenetic assessment of prismatic dinosaur eggs from the Cretaceous Two Medicine Formation of Montana. Journal of Vertebrate Paleontology 24, 931e937. Varricchio, D.J., Jackson, F.D., Borkowski, J.J., Horner, J.R., 1997. Nest and egg clutches of the dinosaur Troodon formosus and the evolution of avian reproductive traits. Nature 385, 247e250. Varricchio, D.J., Jackson, F., Trueman, C.N., 1999. A nesting trace with eggs for the Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 19, 91e100. Varricchio, D.J., Horner, J.R., Jackson, F.D., 2002. Embryos and eggs for the Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 22, 564e576. Wang, Q., Wang, X.-L., Zhao, Z.-K., Jiang, Y.-G., 2010. A new oogenus of Elongatoolithidae from the Upper Cretaceous Chichengshan Formation of Tiantai Basin, Zhejiang Province. Vertebrata PalAsiatica 48, 111e118. Weishampel, D.B., Fastovsky, D.E., Watabe, M., Varricchio, D., Jackson, F., Tsogtbataar, K., Barsbold, R., 2008. New oviraptorid embryos from Bugin.Tsav, Nemegt Formation (Upper Cretaceous), Mongolia, with insights into their habitat and growth. Journal of Vertebrate Paleontology 28, 1110e1119. Xu, X., Wang, X.L., 2003. A new maniraptoran theropod from the Early Cretaceous Yixian Formation of Western Liaoning. Vertebrata Palasiatica 41, 195e202.

Xu, X., Wang, D.Y., Sullivan, C., Hone, D.W.E., Han, F.L., Yan, R.H., Du, F.M., 2010. A basal parvicursorine (Theropoda: Alvarezsauridae) from the Upper Cretaceous of China. Zootaxa 2413, 1e19. Xu, X., Sullivan, C., Pittman, M., Choiniere, J.N., Hone, D., Upchurch, P., Tan, Q., Xiao, D., Tan, L., Han, F., 2011. A monodactyl nonavian dinosaur and the complex evolution of alvarezsauroid hand. Proceedings of the National Academy of Sciences. doi:10.1073/pnas.1011052108. Zelenitsky, D.K., Hills, L.V., 1996. An egg clutch of Prismatoolithus levis oosp. nov. from the Oldman Formation (Upper Cretaceous), Devil’s Coulee, southern Alberta. Canadian Journal of Earth Sciences 33, 1127e1131. Zelenitsky, D.K., Carpenter, K., Currie, P.J., 2000. First record of elongatoolithid theropod eggshell from North America: the Asian oogenus Macroelongatoolithus from the Lower Cretaceous of Utah. Journal of Vertebrate Paleontology 20, 130e138. Zelenitsky, D.K., Hills, L.V., Currie, P.J., 1996. Parataxonomic classification of ornithoid eggshell fragments from the Oldman Formation (Judith River Group, Upper Cretaceous), southern Alberta. Canadian Journal of Earth Sciences 33, 1655e1667. Zhao, Z., 1975. Microstructure of the dinosaurian eggshells of Nanxiong, Guangdong, and the problems in dinosaur egg classification. Vertebrata PalAsiatica 13, 105e117. Zhao, Z.K., Li, Z., Feng, Z., Wang, D., 1999. Oolithia of dinosaurs distributed in Xixia Basin of Henan Province and its buried features. Geoscience Journal of the Graduate School, China University of Geosciences 13, 298e300.
