THE OSTEOLOGY OF HAYA GRIVA (DINOSAURIA: ORNITHISCHIA) FROM THE LATE CRETACEOUS OF MONGOLIA

DANIEL E. BARTA AND MARK A. NORELL

BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY

THE OSTEOLOGY OF HAYA GRIVA (DINOSAURIA: ORNITHISCHIA) FROM THE LATE CRETACEOUS

OF MONGOLIA

DANIEL E. BARTA Department of Anatomy and Cell Biology Oklahoma State University College of Osteopathic Medicine at the Cherokee Nation, Tahlequah, OK; and Richard Gilder Graduate School and Division of Paleontology, American Museum of Natural History, New York

MARK A. NORELL Division of Paleontology American Museum of Natural History, New York

BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY Number 445, 111 pp., 58 figures, 1 table Issued February 26, 2021

Copyright © American Museum of Natural History 2021 ISSN 0003-0090

CONTENTS

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ABSTRACT

Haya griva is an early-diverging neornithischian (“hypsilophodontid”) dinosaur known from several well-preserved skulls and articulated postcranial skeletons, in addition to dozens of partial or isolated finds from the Upper Cretaceous Khugenetslavkant and Zos Canyon localities Javkhlant Formation and equivalent beds) in the Gobi Desert of Mongolia. Collectively, nearly the entire skeletal anatomy of Haya is known, including partial growth series of skulls and femora. Detailed description and comparisons with other ornithischians, including novel anatomical information about the palate and braincase gleaned through high-resolution x-ray microcomputed tomography, reveals a wealth of osteological data for understanding the growth and relationships of this key taxon. Though the Haya specimens span a wide size range, bone histology reveals that all are likely perinatal to subadult individuals, with specimens of intermediate age the most common, and skel- etally mature specimens absent. Phylogenetic analyses place Haya as one of the few Asian members of Thescelosauridae, an important noncerapodan neornithischian group of the Late Cretaceous.

INTRODUCTION

The ornithischian dinosaur Haya griva holds great evolutionary, systematic, biostratigraphic, and paleoecological significance. It is the only representative of an early-diverging ornithis- chian dinosaur currently known among the vast diversity of Mesozoic vertebrates from Mongo- lias Gobi Desert. Despite previous expeditions to the Upper Cretaceous (Santonian-Campan- ian) eastern Gobi exposures of the Javkhlant Formation (Shine Us Khudag redbeds) at the Khugenetslavkant locality (Eberth et al., 2009; fig. 1) by Russian, Mongolian, and American paleontologists, the presence of a primitive neornithischian dinosaur at this site was not revealed until the first discovery of its fossils in 2002 by the joint Mongolian Academy of Sci- ences-American Museum of Natural History expedition (Makovicky et al., 2011). Makovicky et al. (2011) named and described Haya griva on the basis of an articulated holotype skull and several referred specimens consisting of articu- lated and partially articulated cranial and post- cranial remains. We extensively describe these materials and another specimen (IGM 100/3181) first presented by Norell and Barta (2016). We also describe six new nearly com- plete or partial specimens of Haya griva, and compare them to other ornithischian dinosaurs, particularly those for which excellent material also exists. Such comparisons enhance com-

parative anatomical knowledge of early-diverg- ing neornithischians. The combination of character states described in Haya provides fur- ther information for attempts to resolve the unstable relationships and complex, mosaic dis- tribution of characters within clades along this grade (Boyd, 2015). In order to provide a thor- ough account of the morphology, growth, sys- tematics, and probable life habits of Haya griva, we apply high-resolution X-ray microcomputed tomography (uCT) scanning and bone histol- ogy to a partial growth series of this taxon for the first time, reassess its phylogenetic affinities, and further evaluate the implications of gastro- liths associated with three specimens.

MATERIAL AND METHODS

The holotype and referred specimens col- lected by the Mongolian Academy of Sciences- American Museum of Natural History (MAE) expeditions listed below form the basis of this description.

Four Haya griva skulls (IGM 100/2016, IGM 100/2017, IGM 100/3178, IGM 100/3181) were scanned using high resolution X-ray micro- computed tomography (CT) at the American Museum of Natural History Microscopy and Imaging Facility (MIF) with a GE v|tome|x CT scanner at 160 kv, with a 0.5 mm copper filter, a current of 200 yA, and a voxel dimension of 0.04 mm to produce 1800 images. All of these

4 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY

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except IGM 100/3181, which was not processed for this study, were reconstructed using Phoe- nix Datos X (GE Inspection Technologies, LP, Lewistown PA) and FIJI (ImageJ, Schindelin et al., 2012) software, and features of interest were segmented with VGStudio Max (Volume Graphics, Inc. Charlotte, NC). Key specimens (IGM 100/1324, IGM 100/2014, IGM 100/2015, IGM 100/2016, IGM 100/2017, IGM 100/2019, IGM 100/2020, IGM 100/3137, IGM 100/3178, IGM 100/3181, and IGM 100/3661) were sur- face scanned with a Space Spider surface scan- ner (Artec, Luxemborg). Stereolithography (STL) files of these specimens are provided as supplementary information available online (https://doi.org/10.5531/sd.sp.47). Bone histol- ogy and phylogenetic analysis methods are described in the relevant sections below.

INSTITUTIONAL ACRONYMS

AMNH FARB American Museum of Natural History Fossil Amphibians, Rep- tiles, and Birds Collection

BYU Earth Sciences Museum, Brigham Young University, Provo, Utah

IGM Institute of Geology, Mongolian Academy of Sciences, Ulaan Baatar, Mongolia

ROM Royal Ontario Museum, Toronto, Ontario, Canada

MOR Museum of the Rockies, Boze- man, Montana

YPM Yale Peabody Museum of Natu-

ral History, New Haven, Con- necticut

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA 5

SYSTEMATIC PALEONTOLOGY Dinosauria Owen, 1842 Ornithischia Seeley, 1887

Neornithischia Cooper, 1985 (sensu Sereno, 1998)

Haya Makovicky et al., 2011 Haya griva Makovicky et al., 2011

EtyMo.ocy: “Haya griva, from the Sanskrit for the Hindu deity Hayagriva, an avatar of Vishnu characterized by a horse head, in refer- ence to the elongate and faintly horselike skull of this dinosaur, and the common depiction of this deity in the Buddhist art of Mongolia” (fig. 2) (Makovicky et al., 2011: 626).

Ho.otype: IGM 100/2017 (figs. 3-5, 17A, 18A, 21-26A, 30), complete articulated skull (CT scanned) and anterior cervical vertebrae.

REFERRED SPECIMENS:

IGM 100/1324 (figs. 41, 51, 52), large isolated femur (the largest in the studied sample). IGM 100/2013 (figs. 44, 47), “dorsal rib and series of chevrons, an articulated right crus and pes, part of left pes” (Makovicky et al.,

2011: 626) and right femur.

IGM 100/2014 (figs. 9, 17B, 26B, 20), Largely complete crushed skull articulated with cervi- cal vertebrae.

IGM 100/2015 (figs. 27, 31, 35, 37, 38, 42, 49, 51, 52), Articulated postcranial skeleton; a cast is catalogued as AMNH FARB 30635.

IGM 100/2016 (fig. 10), largely complete articu- lated skull (CT scanned).

IGM 100/2018 (fig. 11), anterior portion of small skull.

IGM 100/2019 (figs. 6, 18B, 19, 28, 33, 34), largely complete skull and articulated postcra- nia.

IGM 100/2020 (figs. 43, 51, 52), postcranial frag- ments including ribs, femur, tibia, and pedal phalanges (Makovicky et al., 2011: 626). This specimen includes the smallest femur in the studied sample.

IGM 100/3137 (fig. 29), articulated postcrania lacking skull.

IGM 100/3178 (figs. 7, 32, 36, 39, 40, 45, 46, 48), skull (CT scanned) and partially articulated postcrania.

IGM 100/3181 (fig. 8), skull (CT scanned) and articulated dorsal series with ribs, manual phalanges, radius and ulna (Norell and Barta, 2016).

IGM 100/3182 (fig. 50), partial postcrania, including a largely complete left leg, some dorsal vertebrae, and associated gastroliths.

IGM 100/3557 (fig. 12), crushed partial skull.

IGM 100/3661 (fig. 14), disarticulated partial skull and skeleton.

IGM 100/3672 (fig. 15), partial pelvic region and articulated legs and feet from two individuals in close proximity, centra of the axis and third cervical vertebra, a jaw fragment and other surface collected fragments, including a pos- sible atlantal neurapophysis. An isolated troodontid tooth was found in the matrix inside the jacket during preparation (fig. 16).

MAE 15-84, isolated femur.

Many additional specimens (IGM 100/3561,

100/3632, 100/3633, 100/3634, 100/1322, 100/1873, 100/3558, 100/3559, 100/3560, 100/3562, 100/3563, 100/3564, 100/3565, 100/3566, 100/3567, 100/3568, 100/3569,

100/3570, 100/3571, 100/3604, 100/3605, MAE 03-21) (fig. 13) comprise surface-collected cra- nial and postcranial fragments, including an iso- lated frontal (IGM 100/3567) and abundant partial maxillae and dentaries. These are all from very small, apparently juvenile (or even perinate- sized) individuals. IGM 100/3561 is from the Red Rum sublocality at Zos Canyon (Norell and Barta, 2016).

LOCALITY AND GEOLOGIC SETTING: All speci- mens other than IGM 100/3181 (Norell and Barta, 2016), IGM 100/3661, and IGM 100/3561 are from the Upper Cretaceous (Santonian-Cam- panian) Javkhlant Formation at the Khugenet- slavkant locality within the Shine Us Khudag badlands in the southeastern Gobi Desert of

6 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY

FIG. 2. A Buddhist depiction of the deity Hayagriva.

Mongolia (Eberth et al., 2009; fig. 1). They were found primarily within a 90 m thick section of the middle Javkhlant beds (Eberth et al., 2009). IGM 100/3181 is from the Zos Canyon locality in the western Gobi, and illustrates the wide- spread geographic distribution of Haya griva during the Late Cretaceous. The presence of this specimen also provides important evidence for correlating the Javkhlant Formation and Zos Canyon beds, and by extension illustrating the conformable nature of the stratigraphic sequence spanning the base of the Bayn Shire Formation to the top of the Djadokhta Formation (Norell and Barta, 2016).

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EMENDED DiaGnosis: Makovicky et al. (2011: 627) identified a combination of seven characters diagnostic of Haya griva in their differential diagnosis:

(1) “five homodont, bulbous, unserrated pre- maxillary teeth’; (2) “premaxilla without rugose ramphothecal pad”; (3) “triangular accessory maxillary fenestra’; (4) “jugal with bifid caudal ramus’; (5) “quadratojugal foramen present”; (6) “midline depression along internasal suture”; and (7) “predentary with bifid ventral ramus.’

To these we add an eighth: a bifid anterior process of the jugal (only present in Haya and Heterodontosaurus). Autapomorphies of Haya

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA

griva resulting directly from a new phylogenetic analysis are discussed in the Phylogeny section below.

TAPHONOMY

Both the Shine Us Khudag and Zos Canyon localities preserve Haya specimens as articulated, partially articulated, associated, and isolated ele- ments. One of the Zos Canyon specimens, IGM 100/3661 (fig. 14), is unusual in that the skull and postcranial bones are all fairly widely sepa- rated from one another, possibly dispersed by scavengers or running water. Articulated speci- mens (e.g., IGM 100/2015) are contorted in a death pose typical of small ornithischians (Santa Luca, 1980; Zheng et al., 2012), in which the back is strongly flexed, the neck curled back, and the knees bent slightly forward (figs. 27-29). Articulated postcranial specimens often lack the hands, distal half of the tail, and sometimes the skull. When information from all specimens is combined, however, only some of the manual elements, distalmost tail, and a few braincase ele- ments remain unknown or too poorly preserved to describe.

IGM 100/3672 is unusual in that it con- tains the remains of two individuals, the pel- vic region and both legs of one, and a foot from a third that points opposite to the other two feet (fig. 15). This is the only specimen that preserves definitive evidence of two Haya buried in close proximity to one another. A troodontid tooth also was recovered from matrix within the same jacket as IGM 100/3672 (fig. 16). To our knowledge, this is the first published indication of troodontids from the Javkhlant Formation. Many Haya bones contain holes, likely made by insects feeding on the bones postmortem, as in many other Gobi specimens (Norell and Makovicky, 1997; Fanti et al., 2012; Norell et al., 2018). None of the Haya specimens have been recov- ered from any kind of burrow structure, in contrast to the related Oryctodromeus (Varric- chio et al., 2007).

DESCRIPTION SKULL AND MANDIBLE

The following description is based primarily on elements as preserved in the Haya griva holo- type, IGM 100/2017 (figs. 3-5, 17A, 18A, 21-26). Elements not preserved or readily visible in IGM 100/2017 are described from other specimens in which they are visible. Morphological differences between IGM 100/2017 and other specimens also are emphasized to comprehensively docu- ment variation within Haya griva. Definitions of clade names follow those provided by Madzia et al. (2018).

PREMAXILLA AND PREMAXILLARY DENTITION: The anterior margin of the premaxilla overhangs the anteriormost premaxillary tooth, though it is not developed into a hooked projection to the extent seen in Thescelosaurus, Changchunsaurus, and Hypsilophodon (Huxley, 1870; Galton, 1974a; Jin et al., 2010; Boyd, 2014). The two nutrient foramina on the anteriormost portion of the pre- maxilla form a “figure 8” configuration, as noted by Makovicky et al. (2011). Just posterior to the nutrient foramina, at the position of the first tooth, the premaxilla bulges laterally. The poste- rior portion of the premaxilla laterally flares and thins dorsally along the subnarial process, form- ing a flat articular surface with the lateral side of the nasal (fig. 3, 5). The premaxilla of Haya griva is proportionally dorsoventrally taller and antero- posteriorly shorter than that of Thescelosaurus (Boyd, 2014) and has a more dorsally directed subnarial process. As in Hypsilophodon, Isaber- rysaura, and possibly Orodromeus, the subnarial process of Haya gently curves posteriorly, but does not contact the lacrimal (Galton, 1974a; Scheetz, 1999; Makovicky et al., 2011; Salgado et al., 2017). The process is taller, narrower, and less anteroposteriorly expanded than the condition seen in Jeholosaurus (Barrett and Han, 2009). The supranarial (ascending) process of the premaxilla is incompletely preserved in all Haya specimens, with only a short process remaining (figs. 3, 4, 5, 7, 8, 11). The anteriormost points of the nasals opposite the external nares from the ascending

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FIG. 3. Skull of the holotype specimen of Haya griva, IGM 100/2017, in A, C, right lateral and B, D, left lateral views. Abbreviations in appendix 1.

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BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA

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FIG. 4. Skull of the holotype specimen of Haya griva, IGM 100/2017, in A, C, dorsal and B, D, ventral views. Abbreviations in appendix 1.

processes of the premaxillae appear damaged, providing no evidence about the morphology of the internarial bar. The apparently confluent nature of the external nares of Haya (fig. 5) is best considered a taphonomic artifact because conflu- ent external nares (i.e., with loss of a complete internarial bar) are unknown among dinosaurs except for some diplodocoid and titanosaur sau- ropods (Upchurch, 1995; Wilson et al., 2016). In Haya, the surface of the premaxilla is smooth, in contrast to the rugose anterior premaxillary sur- faces of Lesothosaurus, Jeholosaurus, Changchun- saurus, Oryctodromeus, Zephyrosaurus, Thescelosaurus, and Hypsilophodon (Galton,

1974a; Sues, 1980; Sereno, 1991; Varricchio et al., 2007; Barrett and Han, 2009; Jin et al., 2010; Boyd, 2014). Such rugose surfaces have been interpreted as evidence of a ramphotheca (Gal- ton, 1974a), but the extent and attachment of a ramphotheca in Haya, if present, is unclear. The general morphology of the premaxilla anterior to the first premaxillary tooth is similar to Lesotho- saurus (Sereno, 1991; Knoll, 2008), except Haya lacks even the limited pitting inferred to corre- spond to a short ramphotheca anterior to the first premaxillary tooth in Lesothosaurus (Sereno, 1991; Knoll, 2008). Future discoveries of morpho- logically mature skulls may reveal whether pitting

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA 11

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and, by inference, a ramphotheca, developed on the premaxilla of Haya griva through ontogeny, as in Jeholosaurus (Barrett and Han, 2009). In IGM 100/2017, the premaxillae are unfused along their midline contact. Many other primitive ornithischian taxa, including Oryctodromeus, Changchunsaurus, and Thescelosaurus, possess fused or partially fused premaxillae (Norman et al., 2004; Varricchio et al., 2007; Jin et al., 2010; Boyd, 2014). The premaxilla contains five teeth, as is typical for most early-diverging ornithischi- ans (Norman et al., 2004), though six are present in Lesothosaurus, Isaberrysaura, Jeholosaurus, and Thescelosaurus (Sereno, 1991; Barrett and Han, 2009; Boyd, 2014; Salgado et al., 2017). Boyd (2014) noted that the number of premaxillary teeth may have increased through ontogeny in

D

Jeholosaurus and Thescelosaurus, based on his personal observations of multiple specimens of the two taxa. So far, there is no evidence for an increase in premaxillary tooth count through ontogeny in Haya, but future discoveries of onto- genetically more mature specimens are needed to test this. The teeth lack serrations (Makovicky et al., 2011) but bear very faint longitudinal stria- tions. As in Lesothosaurus, the premaxillary teeth lack wear facets, suggesting that during feeding they worked in opposition to the softer kerati- nous beak inferred to be present on the preden- tary (Knoll, 2008; but Norman et al., 2004, notes the presence of premaxillary tooth wear facets in other taxa). The apicalmost portion of each tooth is slightly recurved (figs. 3, 7, 8). In IGM 100/2017, the first and third right premaxillary

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FIG. 5. Skull of the holotype specimen of Haya griva, IGM 100/2017, in anterior view. Abbreviations in appendix 1.

teeth are somewhat bulbous, unlike the more pointed second, fourth, and fifth teeth. This is also true of the left premaxillary teeth, though the tips of the second and fifth teeth are broken on this side. The first and third left premaxillary teeth of IGM 100/3178 (fig. 7) are also somewhat bulbous, but the other premaxillary teeth are largely obscured. IGM 100/2018 (fig. 11) is not well preserved, but the left premaxilla is more complete than the right. The suture between the two premaxillae is visible at the anteriormost end of the rostrum, and the quality of preservation

makes it difficult to tell whether or not the two bones are fused. The premaxillary toothrow is in line with the maxillary toothrow, in contrast to Hypsilophodon, where they are offset (Galton, 1974a; Makovicky et al, 2011). These two toothrows are separated by a diastema, as is pres- ent in most basal neornithischians (Norman et al., 2004; Makovicky et al., 2011). It is unclear whether the diastema present in these taxa is homologous to that of theropods or the possible sauropodomorph Eoraptor (Langer and Benton, 2006; Sereno et al., 2012).

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FIG. 6. Skull and cervical vertebrae of Haya griva, IGM 100/2019, in right lateral view (skull) and dorsolateral view (vertebrae). Abbreviations in appendix 1.

MAXILLA AND MAXILLARY DENTITION: The maxilla contacts the premaxilla anteriorly, a small portion of the nasal dorsally, the lacrimal and jugal posterolaterally, the palatine medially, and the ectopterygoid posteromedially. In palatal view, it forms the lateral border of the postpala- tine (suborbital) fenestra as in Heterodontosau- rus, Changchunsaurus, and Hypsilophodon (Galton, 1974a; Jin et al., 2010; Norman et al., 2011; fig. 4B, D). The ramus of the maxilla is straight in lateral view in Haya griva. In ‘Thesce- losaurus, the posterior end of the ramus curves dorsally. The maxilla of Haya becomes mediolat- erally thin dorsally where it meets the nasal and premaxilla. A narrow gap between the premax- illa and maxilla, just dorsal to the diastema between the premaxillary and maxillary toothrows, forms the anterior maxillary fossa (Boyd, 2014). The long axis of this narrow fossa is oriented dorsoventrally in Haya, in contrast to

the round fossa of Thescelosaurus. The toothrow is strongly inset from the rest of the maxilla, with a well-defined emargination (the buccal ridge) between the two. In lateral view, the buccal ridge dips ventrally and continues posteriorly to below the midpoint of the orbit (Makovicky et al. 2011). At least six nutrient foramina lie ventral and par- allel to the buccal ridge in IGM 100/2017, with the more posterior three being larger than the anterior three. The anterior three nutrient foram- ina face laterally, but the posterior three face more lateroventrally underneath the overhang- ing buccal ridge. There are five or six foramina in IGM 100/3181, four small anterior ones, one larger posterior foramen, and possibly one shal- low ventrally facing foramen near the junction with the jugal. At least four nutrient foramina pierce the incomplete right maxilla of IGM 100/2014; however, the two posteriormost foramina are smaller than the anterior two. Two

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FIG. 7. Skull of Haya griva, IGM 100/3178, in left lateral view. Abbreviations in appendix 1.

foramina are present on the anteriorly eroded maxilla of IGM 100/2016. Thus, it is clear that the relative sizes and possibly the number of these formina are variable in Haya griva. Haya lacks the row of smaller foramina on the lateral surface of the buccal ridge seen in Thescelosaurus (Boyd, 2014). A triangular maxillary fenestra lies anterior to the antorbital fenestra, and is sepa- rated from it by a narrow, posteriorly concave interfenestral strut (figs. 3, 8). In Haya, the ant- orbital fenestra is larger than the maxillary fenes- tra. Among other early-diverging neornithschians, a maxillary fenestra is present only in Kulindadromaeus, where it may be larger than the antorbital fenestra (Godefroit et al., 2014), and Hypsilophodon, where it is even smaller relative to the antorbital fenestra than in Haya (Galton, 1974a; Makovicky et al., 2011). IGM 100/3181 has a small prong dorsal to the buccal ridge that projects into the maxillary

fenestra. It is matched by a less-pronounced knob on the interfenestral strut that projects ven- trally into the maxillary fenestra (fig. 8). The interfenestral strut separating the maxillary and antorbital fenestra is also more strongly concave posteriorly at its midpoint in IGM 100/3181 (fig. 8) than in IGM 100/2017 (fig. 3). This could be an artifact of slight crushing or displacement of the strut; however, the 83 mm long skull of IGM 100/3181 is less dorsoventrally crushed overall than the 93 mm long skull of IGM 100/2017 (Makovicky et al., 2011; Norell and Barta, 2016). The antorbital fenestra is ovate, with the long axis of the oval directed anterodorsally, similar to the condition in Jeholosaurus (Barrett and Han, 2009). In comparison, the long axis of the antor- bital fenestra is oriented anteroposteriorly in Thescelosaurus, Changchunsaurus, and Gasparin- isaura (Coria and Salgado, 1996) and dorsoven- trally in Hypsilophodon. The antorbital fenestra is

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA 15

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nearly circular in Orodromeus (Scheetz, 1999), and more triangular in Agilisaurus and Hexin- lusaurus (Barrett et al., 2005). A shallow antor- bital fossa surrounds the fenestra and extends dorsally to the contact with the nasal and ven- trally to meet the buccal ridge. A row of special foramina (Edmund, 1957) linked by a groove pierces the lingual surface of the maxilla. The special foramina of the dentary are described in more detail below.

As confirmed in CT slices, the right maxilla of IGM 100/2017 contains 14 alveoli, whereas the left contains 13. In the left maxilla, replacement teeth are present at the fourth, fifth, seventh, 10th, and 13th alveoli (counted from anterior to posterior). Replacement teeth in the fourth and 13th positions are partially erupted, with just the tips of the crowns protruding. The right maxilla contains replacement teeth at the first, fourth, fifth, seventh, eighth, 10th, 11th, and 14th alveoli (four of these are visible in the CT slice in figure

17A). Those at the fourth, seventh, and 10th tooth positions have partially erupted, whereas the others are deep within the maxilla. This sug- gests the presence of at least three “generations” of teeth in the right maxilla: (1) fully erupted, worn teeth (first, second, third, fifth, sixth, eighth, ninth, 11th, 12th, 13th, and 14th alveoli), (2) partially erupted, unworn teeth (fourth sev- enth, and 10th alveoli), and (3) unerupted teeth (first, fifth, eighth, 11th, and 14th alveoli). The right maxilla contains more replacement teeth than the left, even after accounting for the pres- ence of an extra alveolus in the right maxilla. The degree of eruption of the replacement teeth also differs between right and left. This suggests that the timing of tooth replacement waves differed between the right and left maxillae, as may be the case for the right and left dentaries (see Dentary section below).

IGM 100/3178 (fig. 7) has 13 teeth in its left maxilla. The right is not preserved well enough

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to obtain a complete count. Unerupted replace- ment teeth are not clearly visible within the alve- oli in CT slices for any of the tooth-bearing elements of IGM 100/3178 (there could be some that have erupted slightly, but this is difficult to discern in the CT slices).

Fourteen maxillary teeth in Haya griva is within the range of most other basal neornithis- chians, which may display one or two teeth greater or fewer than found in Haya griva. This is with the exception of the greatly enlarged maxillary tooth counts (18-30) of Hexinlusau- rus, Kulindadromaeus, Isaberrysaura, and Thes- celosaurus (Barrett et al., 2005; Boyd, 2014; Godefroit et al., 2014; Salgado et al., 2017). The number of maxillary tooth positions increases through ontogeny in Orodromeus and possibly in Kulindadromaeus (Godefroit et al., 2014). This is also likely true of Haya, given the short length of the maxilla in the specimen with juve- nile morphology (IGM 100/2016); however, maxillary alveoli are not well preserved in this specimen. The teeth are low crowned and trian- gular, with at least 10 denticles distributed evenly between the mesial and distal carinae on unworn teeth in the right maxilla of IGM 100/2017. The teeth exhibit lingual wear facets. The crowns of unworn and worn teeth appear somewhat asymmetric in buccal view, with the apical edge sloping basodistally, as in Changch- unsaurus and Hypsilophodon (Galton, 1974a; Jin et al., 2010) (fig. 17B). This asymmetry stands in contrast to the more symmetrical maxillary teeth of heterodontosaurids and Lesothosaurus (Sereno, 1991, 2012). The maxillary teeth of Thescelosaurus change from symmetrical anteri- orly being more asymmetrical posteriorly (Boyd, 2014). In Haya there is no clear change in the degree of asymmetry along the toothrow. The asymmetric maxillary teeth of Haya also differ from its symmetrical dentary teeth, as is the case for Hypsilophodon (Galton, 2007).

LACRIMAL: The straplike lacrimal is gently concave along its anterior and posterior borders, anterodorsally oriented, and contacts the dorsal process and posterodorsal corner of the maxilla

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(figs. 3, 5-8). It also contacts the prefrontal and anterior supraorbital dorsally, and the jugal pos- teroventrally. The lacrimal of Haya is relatively narrower and more elongate than the more tri- angular lacrimal of Thescelosaurus, and is straighter than the lacrimals of Agilisaurus (Peng, 1992; Barrett et al., 2005), Kulindadromaeus (Godefroit et al., 2014), Hypsilophodon (Galton, 1974a), and a probable juvenile Jeholosaurus (IVPP V12530), which all form inverted L-shapes (Barrett and Han, 2009). The dorsal end of the lacrimal flares slightly anteriorly in at least one Haya specimen (IGM 100/3181), similar to the lacrimals of Lesothosaurus and Changchunsaurus (Jin et al., 2010; Porro et al., 2015). The lacrimal of IGM 100/3181 may have contacted the sub- narial process of the premaxilla along a very small margin (fig. 8), in contrast to IGM 100/2017, in which these two bones do not meet (Makovicky et al., 2011) (fig. 3). The premaxilla and lacrimal develop an extensive contact through ontogeny in Jeholosaurus (Barrett and Han, 2009). The two bones contact each other in Kulindadromaeus (Godefroit et al., 2014), and a still more extensive contact is present among iguanodontians (Norman, 2004). The premaxilla and lacrimal do not articulate in other early- diverging neornithischians nor Hypsilophodon (Norman et al., 2004). Posteriorly, the lacrimal contains a dorsoventrally oriented groove, pos- sibly contiguous with the lacrimal foramen. In IGM 100/2019, the right lacrimal contains a small depression (possibly the lacrimal foramen), the lateral border of which forms a pronounced ridge that curves slightly medially toward the dorsal end of the lacrimal.

NasAL: The nasals are roughly triangular in dorsal view, contacting the subnarial processes of the premaxillae anterolaterally, the prefrontals posterolaterally, and the frontals posteriorly (fig. 4A, C). Unlike Thescelosaurus (Boyd, 2014), but similar to most early-diverging neornithischi- ans, the nasal of Haya does not contribute to the border of the antorbital fenestra. The nasals are mediolaterally broadest above the anteroposte- rior midpoint of the maxillae and taper posteri-

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA 17

FIG. 9. Skull and cervical vertebrae of Haya griva, IGM 100/2014, in A, left lateral and B, right lateral views. Abbreviations in appendix 1.

orly near their contact with the frontals. The posterior end flares somewhat laterally, forming a ridge along the contacts with the maxilla and prefrontal that borders the antorbital fossa dor- sally. In Haya, the nasals are not as extensively exposed in lateral view as those of some other early-diverging neornithischians (e.g., Isaber- rysaura, Jeholosaurus, Thescelosaurus), though the nasal region is not often preserved among taxa of this grade (Norman et al., 2004). The nasals are unfused along the internasal suture. They dip toward one another, forming a shallow midline depression along the length of their suture (fig. 4A), as in Heterodontosaurus, Agilis- aurus, Hexinlusaurus, Kulindadromaeus, Jeholo- saurus, and Changchunsaurus (He and Cai, 1984; Peng, 1992; Barrett and Han, 2009; Jin et al., 2010; Makovicky et al., 2011; Norman et al., 2011; Godefroit et al., 2014; Norell and Barta, 2016). This depression deepens anteriorly. The nasals are mostly flat except near the midline depression and at their anterior ends, which arch above the naris. The anterior ends of the frontals wedge between the posterior ends of the nasals (Makovicky et al., 2011). The prefrontals overlap the posterior half of the nasals along an extensive flat contact. A single nutrient foramen

is present near the broadest portion of each nasal (Makovicky et al., 2011; fig. 4A). Multiple such foramina are present in Jeholosaurus and Thescelosaurus (Barrett and Han, 2009; Boyd, 2014). As noted by Makovicky et al. (2011), the internarial bar is not preserved, but the anterior ends of the nasals leave little space for the pre- maxillae to wedge between them, in contrast to the nasal-premaxilla articulation of Hypsiloph- odon (Galton, 1974a).

JUGAL: The jugal is mediolaterally compressed and forms the ventral borders of the orbit and lateral temporal fenestra (figs. 3, 5-8, 10). The anterior (maxillary) ramus is dorsoventrally nar- rower than the posterior (quadratojugal) ramus. Overall, the jugals of Haya and most other early- diverging neornithischians are dorsoventrally narrow and anteroposteriorly long, compared to the dorsoventrally wider jugal of Hypsilophodon (Galton, 1974a). The jugal thickens mediolater- ally at the level of the dorsal (postorbital) pro- cess. The postorbital overlaps the dorsal process of the jugal dorsally along an anterolaterally fac- ing scarf joint. The dorsal process of IGM 100/2017 is more posteriorly directed than in other specimens, but this likely is a consequence of the slight crushing and shearing of the holo-

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type skull. In IGM 100/3181, the dorsal process exhibits a well-defined dorsoventrally directed ridge on its lateral surface (fig. 8). Unique to Haya and Heterodontosaurus among noncerapo- dan ornithischians is a bifid anterior process of the jugal (figs. 3, 6, 8). In IGM 100/2017 and IGM 100/2019, the dorsal prong of this bifurca- tion appears to reach the lacrimal (as in Heter- odontosaurus), and the ventral prong articulates solely with the jugal process of the maxilla. It is difficult to determine whether the dorsal prong would have reached the lacrimal in IGM 100/3181 because of poor preservation. In Heter- odontosaurus the anterior jugal bifurcation forms the entrance to a deep lateral channel connecting to the antorbital fossa (Norman et al., 2011; Sereno, 2012). Haya lacks such a deep channel; instead, the lateral surface of the anterior process contains a shallower suborbital sulcus in all spec- imens. In IGM 100/3181 and IGM 100/2016 this sulcus houses at least five small foramina that are not present in other Haya specimens or other taxa (Norell and Barta, 2016). The slight degree of curvature of the anterior process is similar to that of Thescelosaurus (Boyd, 2014) and Changc- hunsaurus (Jin et al., 2010). It lacks the extreme dorsal curvature seen in Agilisaurus (Peng, 1992; Barrett et al., 2005). The anterior process does not taper as sharply as in Hexinlusaurus, Agilis- aurus, and Jeholosaurus. Instead, the dorsal and ventral borders of the process are largely parallel to one another for their entire lengths. Posteri- orly, the jugal is bifid, with both prongs overlap- ping the quadratojugal. IGM 100/2016 best illustrates the bifid nature of the jugal (Makov- icky et al., 2011), with two nearly equal-length prongs forming a V-shape where they overlap the quadratojugal (fig. 10). As noted by Makov- icky et al. (2011), the appearance of this V-shape may be exaggerated by bone loss between the prongs. However, the angle between the prongs is a much shallower U-shape in many other spec- imens (IGM 100/2017, IGM 100/2019, IGM 100/3178 and IGM 100/3181), and it seems likely that this shape difference in jugal prongs com- pared to IGM 100/2016 is at least partially bio-

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logic. The prongs are roughly equal in size in IGM 100/3181 (fig. 8), whereas the dorsal prong is narrower and more pointed than the ventral prong in IGM 100/2017, IGM 100/3178, and IGM 100/2019 (figs. 3, 6, 7). The prongs both overlap the quadratojugal, in contrast to Thesce- losaurus, Tenontosaurus, and Zalmoxes, where the dorsal prong overlaps the lateral surface of the quadratojugal and the ventral prong the medial surface (Weishampel et al., 2003; Makov- icky et al., 2011; Boyd, 2014). The surface of the jugal in all examined Haya specimens is smooth, with no trace of the jugal rugosities seen in some Jeholosaurus and Changchunsaurus specimens (Barrett and Han, 2009; Jin et al., 2010). It fur- ther lacks the jugal bosses present in Heterodon- tosaurus, Manidens, Zephyrosaurus, and Orodromeus (Sues, 1980; Scheetz, 1999; Norman ettal., 201 I; Pol-et-al;, 2011).

QUADRATOJUGAL: The quadratojugal is a small, flat element situated between the jugal lat- erally and the quadrate medially (figs. 3, 6-8, 10). It is trapezoidal in overall shape, with a dor- sal border that is shorter than its ventral border (Makovicky et al., 2011), whereas the exposed portion of the quadratojugal is more triangular in Orodromeus and somewhat teardrop shaped in Zalmoxes and some Dryomorpha (Scheetz, 1999; Norman, 2004). It has a pointed dorsal extension as in Agilisaurus, Thescelosaurus, and many other early-diverging neornithischians (Norman et al., 2004; Barrett et al., 2005; Boyd, 2014). The quadratojugal is relatively dorsoven- trally tall and contributes more extensively to the posterior border of the lateral temporal fenestra than to the ventral border. This dorsal process of the quadratojugal is splintlike and appressed to the anterior margin of the quadrate (fig. 6). Its dorsalmost point reaches the anteriormost pro- jection of the quadrate in lateral view as in Agil- isaurus, Jeholosaurus, Changchunsaurus, Thescelosaurus, and Hypsilophodon (Galton, 1974a; Peng, 1992; Barrett and Han, 2009; Jin et al., 2010; Boyd, 2014). This process does not reach the squamosal, unlike in Heterodontosau- rus and possibly Lesothosaurus and Gasparin-

2021 BARTA AND NORELL: OSTEOLOGY OF HAYA GRIVA 19

FIG. 10. Skull of Haya griva, IGM 100/2016 in A, ventral, B, dorsal, C, right lateral, D, left lateral, E, posterior, and F, anterior views. Abbreviations in appendix 1.

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isaura (Coria and Salgado, 1996; Norman et al., 2011; Porro et al., 2015). The quadratojugal of Haya lacks any significant anterior process, in contrast to the L-shaped quadratojugals of Park- sosaurus and especially Gasparinisaura (Galton, 1973; Coria and Salgado, 1996). In lateral view, it overlaps and obscures most of the quadratojugal wing of the quadrate. Dorsally, the quadratojugal contributes to the posteroventral border of the lateral temporal fenestra. Ventrally, the border of the quadratojugal is straight and parallels the anteroposterior axis of the skull. The posteroven- tral corner projects ventrally to the same level as the ventral edge of the jugal in lateral view. It lacks the extremely long posteroventral process of heterodontosaurids (Norman et al., 2011; Pol et al., 2011; Sereno, 2012), and the lesser postero- ventral expansions present in Changchunsaurus, Parksosaurus, and Thescelosaurus (Galton, 1973; Jin et al., 2010; Boyd, 2014). Centrally, a large quadratojugal foramen pierces the quadratojugal, as in Hypsilophodon and Jeholosaurus (Galton, 1974a; Barrett and Han, 2009). The long axis of this ovate foramen is oriented anteroposteriorly. Much smaller foramina are present in the qua- dratojugals of Thescelosaurus and Gasparinisaura (Coria and Salgado, 1996; Boyd, 2014). There may be a small notch present in the posteroven- tral corner of the quadratojugals of IGM 100/2017 and IGM 100/2016 (figs. 3, 10). In IGM 100/3181, the quadratojugal foramen appears to pierce the suture between the jugal and quadra- tojugal (Norell and Barta, 2016; fig. 8), somewhat similar to the condition in Tenontosaurus (Nor- man, 2004); however, this could be an artifact of displacement or erosion in this specimen. PosToORBITAL: As in most basal neornithischi- ans, the postorbital is a triradiate bone, with pro- cesses that contact the frontal, parietal, jugal, and squamosal (figs. 3, 6-10). There does not appear to be any contact with the laterosphenoid, as occurs in Hypsilophodon (Galton, 1974a). The anteroventrally directed ventral process exten- sively overlaps the dorsal (postorbital) process of the jugal along a scarf joint to form the posterior border of the orbit. The posterior process articu-

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lates with the squamosal, with the posterior pro- cess forming a simple triangular prong on IGM 100/3178 (fig. 7) and a possibly bifid prong on IGM 100/2017 and IGM 100/2019 (figs. 3, 6). The anterior process contacts the frontal and parietal near where those two bones meet. The anterior process of Haya is straight and straplike, being less anteroposteriorly expanded than the postorbital of Orodromeus (Scheetz, 1999). A deep sulcus extends dorsoventrally across the lat- eral side of the postorbital in IGM 100/318] (fig. 8), but it is less evident in the other Haya speci- mens, being nearly absent or forming a shallow, U-shaped trough (IGM 100/2016). This differs from the more extensive postorbital fossa in Het- erodontosaurus (Sereno, 2012). Viewed anteri- orly, the orbital margin of the ventral process possesses a shallow dorsoventrally oriented trough. The posterior edge