Diapsida: Choristodera) from the Lower Cretaceous of Liaoning, China

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Osteology and taxonomic revision of Hyphalosaurus (Diapsida: Choristodera) from the Lower Cretaceous of Liaoning, China

Article in Journal of Anatomy · July 2008 Impact Factor: 2.1 · DOI: 10.1111/j.1469-7580.2008.00907.x · Source: PubMed

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J. Anat. (2008) 212, pp747–768 doi: 10.1111/j.1469-7580.2008.00907.x

OsteologyBlackwell Publishing Ltd and taxonomic revision of Hyphalosaurus (Diapsida: Choristodera) from the Lower Cretaceous of Liaoning, China Ke-Qin Gao1,2 and Daniel T. Ksepka2 1School of Earth and Space Sciences, Peking University, Beijing, China 2Division of Paleontology, American Museum of Natural History, New York, New York, USA

Abstract

Although the long-necked choristodere Hyphalosaurus is the most abundant tetrapod fossil in the renowned Yixian Formation fossil beds of Liaoning Province, China, the genus has only been briefly described from largely unprepared specimens. This paper provides a thorough osteological description of the type species Hyphalosaurus lingyuanensis and the con-generic species Hyphalosaurus baitaigouensis based on the study of fossils from several research institutions in China. The diagnoses for these two species are revised based on comparison of a large sample of specimens from the type area and horizon of each of the two species. The skull, better known in H. baitaigouensis, exhibits key choristodere synapomorphies including an elongate contact between the prefrontals and posteriorly expanded supratemporal fenestrae that strongly support the placement of the highly derived hyphalosaurids within Choristodera. Both species of Hyphalosaurus share a proportionally small head, an elongate neck, a relatively unspecialized appendicular skeleton and a long, dorsoventrally heightened tail. Soft tissue preservation in several specimens provides rare insight into the integument of an extinct group. The integument of Hyphalosaurus is made up of small polygonal scales with several parasagittal rows of large, keeled, ovoid scutes. These possibly ornamental scutes bear a strong resemblance to the rows of large scutes in the monjurosuchid choristodere Monjurosuchus splendens. Observations from a variety of growth stages reveal that significant ontogenetic change in the proportions of the body and limb bones occurred in both species of Hyphalosaurus. Key words anatomy and taxonomy; Choristodera; Early Cretaceous; Hyphalosauridae; western Liaoning of China.

and eutherian mammals (Hu & Wang, 2002; Ji et al. Introduction 2002). The second species, Hyphalosaurus baitaigouensis, The genus Hyphalosaurus includes two species of highly is known from far more abundant material from the specialized aquatic choristoderan reptiles with unusually Yizhou area (Fig. 1), where multiple localities exposing long necks. Fossils of this genus are known only from the strata from the upper part of the Yixian Formation (Wang Early Cretaceous Yixian Formation of western Liaoning et al. 2004; but see also Ji et al. 2004a) have yielded at least Province, China. The type species, Hyphalosaurus ling- several thousand specimens of this species, including soft- yuanensis, is known from multiple specimens from a single shelled fossil eggs (Ji et al. 2004b). These two species, locality in the Lingyuan area (Fig. 1), where the fossil beds along with Shokawa ikoi from the Early Cretaceous Okuro- of the lower Yixian Formation have yielded a radiometric dani Formation of Japan (Evans & Manabe, 1999), form the date of 123–126 Ma (Smith et al. 1995; Ji et al. 2004a). The family Hyphalosauridae (Gao & Fox, 2005). In addition to fossil beds exposed at the Lingyuan area are also known features such as dorsally positioned orbits and pachyostotic for producing superbly preserved fossils including feathered ribs that are widely distributed within Choristodera, hypha- dromaeosaurs (Ji et al. 2001), a juvenile enantiornithine bird losaurids are characterized by a small head, a long neck (Hou & Chen, 1999; Zhang et al. 2003), and multituberculate consisting of more than 16 cervical vertebrae, and a greatly elongated and heightened tail. This combination of traits suggests that hyphalosaurids were the most completely aquatic choristodere clade. Taphonomy also supports this Correspondence inference, as Hyphalosaurus is common in deep-water Dr K.-Q. Gao, School of Earth and Space Sciences, Peking University, lacustrine facies bearing the large chondrostean fish Pro- Beijing 100871, China. E: [email protected] topsephurus in the Lingyuan area and co-occurs with the Accepted for publication 12 February 2008 abundant large shrimp Liaoningogriphus in the Yizhou

748 Cretaceous reptile Hyphalosaurus from China, K.-Q. Gao and D. T. Ksepka

Fig. 1 Map showing distribution pattern of Hyphalosaurus fossils in western Liaoning. Note the absence of Hyphalosaurus from the Chaoyang area (satellite image of the area from TAGEO.com).

area (Shen, 2003). Interestingly, Hyphalosaurus is absent V11075) was incompletely exposed when the original descrip- from the Chiufotang Formation exposed near the city of tion of the species was completed. Further preparation Chaoyang (Fig. 1). These deposits appear to represent a of the holotype and examination of additional previously shallow-water swampy environment and contain the undescribed specimens of H. lingyuanensis allow us to blunt-snouted monjurosuchid choristodere Philydro- provide new observations on the osteology of the type saurus proseilus (Gao & Fox, 2005; Gao et al. 2007) and species, including previously unknown information on gavialiform neochoristoderes (unpublished specimens LPMC the skull roof and integument of this species. Based on R00070, 00071), as well as birds and non-avian dinosaurs. examination of a large number of well-preserved speci- Thousands of Hyphalosaurus specimens are currently mens in several institutions, we also provide a revision of deposited in research collections or in private hands. Despite H. baitaigouensis, including an emendation of the diagno- the surfeit of material, the anatomical details of these sis and clarification of its cranial and postcranial anatomy. animals have scarcely been touched upon. The first account This study provides essential information for understanding of Hyphalosaurus briefly described the type species H. the evolution of Hyphalosauridae in Asia as a highly lingyuanensis, at that time considered Diapsida incertae specialized family of aquatic diapsids, and the phylogeny sedis (Gao et al. 1999). Following the recognition of the of the Choristodera, now recognized as an important choristoderan affinities of the genus (Gao et al. 2000), a clade in Mesozoic terrestrial ecosystems throughout the second species, H. baitaigouensis, was described (Ji et al. Northern Hemisphere. 2004b). However, the original publication of the second species lacks essential anatomical treatment of the skull, and, more unfortunately, several skull elements are misidentified Abbreviations and mislabeled in the published figure (see discussion Institutional: AMNH – American Museum of Natural History, below). The two species are most easily distinguished by New York, NY, USA; BMNHC – Beijing Museum of Natural the number of cervical vertebrae, but several other features History, Beijing, China; CAGS – Chinese Academy of Geo- (listed below) are also diagnostic, as recognized in this logical Sciences, Beijing, China; GMC – Geological Museum study. In this paper, we present a detailed description of of China, Beijing, China; IVPP – Institute of Vertebrate the osteology of Hyphalosaurus, primarily from newly Paleontology and Paleoanthropology, Beijing, China; prepared specimens from several institutions including the LPMC – Liaoning Paleontological Museum of China, BMNHC, IVPP, LPMC, and Peking University Paleontological Shenyang, China; PKUP – Peking University Paleontological Collections. The holotype specimen of H. lingyuanensis (IVPP Collections, Beijing, China.

Cretaceous reptile Hyphalosaurus from China, K.-Q. Gao and D. T. Ksepka 749

Anatomical: ar, articular; as, astragalus; bo, basioccipital; Genus Hyphalosaurus Gao et al. 1999 ca, calcaneum; ch, choana; cl, clavicle; co, coronoid; cor, coracoid; cv, cervical vertebra; den, dentary; dc, distal Type species: Hyphalosaurus lingyuanensis Gao et al. 1999. carpal; dt, distal tarsal; dv, dorsal vertebra; ect, ectopterygoid; Constituent species: The type species and H. baitai- ectf, ectepicondylar foramen; fem, femur; fi, fibula; fr, gouensis (see discussion below). frontal; hu, humerus; icl, interclavicle; il, ilium; intv, interp- Generic diagnosis: The genus is diagnosed by derived terygoid vacuity; isc, ischium; j, jugal; lac, lacrimal; m, character states including an elongated neck consisting of maxilla; mc, metacarpal; mt, metatarsal; na, nasal; neo, 19–24 cervical vertebrae and subequal length of the third neomorph; pa, parietal; pal, palatine; palf, palatal and fourth metatarsals. Because the skull of Shokawa foramen; par, parasphenoid; pm, premaxilla; porf, post- remains almost entirely unknown, it is uncertain which orbitofrontal; prf, prefrontal; ptg, pterygoid; pub, pubis; features of the skull diagnose Hyphalosaurus and which qj, quadratojugal; qu, quadrate; rad, radius; sa, surangular; are shared between the two taxa. sc, scapula; sv, sacral vertebra; sq, squamosal; ti, tibia; ul, Known distribution: Known only from the Early Cretaceous ulna; vo, vomer. Yixian Formation, western Liaoning Province, China.

Systematic palaeontology Species Hyphalosaurus lingyuanensis Gao et al. 1999 Class Reptilia Laurenti, 1768 Synonym: Sinohydrosaurus lingyuanensis Li et al. 1999 (see Subclass Diapsida Osborn, 1903 Smith & Harris, 2001 for discussion). Order Choristodera Cope, 1876 Holotype: IVPP V11075, nearly complete skull, mandibles, Family Hyphalosauridae Gao and Fox, 2005 and well-preserved postcranial skeleton; BMNHC V398 (BPV-398), counterpart impressions of IVPP V11075. The Type genus: Hyphalosaurus Gao et al. 1999 part and counterpart of the same specimen were acquired Family diagnosis (revised from Gao & Fox, 2005): Distinct independently by the two institutions; however, both choristoderan family characterized by having proportionally parts are here treated as the holotype, as they are of the small skull, infratemporal fenestra closed in adult individuals, same individual. greatly elongated neck consisting of 16–24 cervical vertebrae, Type locality and horizon: Fanzhangzi, approximately and development of triangular and spike-like neural spine 20 km southwest of the city of Lingyuan, Liaoning Province, of the caudal vertebrae. China; Early Cretaceous Yixian Formation, radiometrically Constituent genera: The family is currently known dated to 123–126 Ma (Smith et al. 1995; Ji et al. 2004a). from two genera, including the type genus Hyphalosaurus Referred specimens: PKUP V1052, GMC juvenile (Fig. 3); from western Liaoning Province of China and the closely both topotypic specimens from the type locality near related genus Shokawa from Japan (see remarks below). Lingyuan as described above. Known distribution: Early Cretaceous lacustrine deposits Known distribution: Known only from the type locality in East Asia, including western Liaoning Province of China and horizon. and central Japan. Diagnosis (revised from Gao et al. 1999): Hyphalosaurid Remarks: Although highly specialized for an aquatic choristodere differing from the congeneric species H. ecology, Hyphalosauridae share many character states baitaigouensis by possession of the following autapomor- that support the inclusion of the family group in the order phies: postorbital part of skull substantially shorter than Choristodera (Evans & Manabe, 1999; Gao & Fox, 2005). anterior part including snout and orbit; frontal-parietal Within the Choristodera, the family occupies a position suture located at level slightly posterior to the anterior outside the Neochoristodera and may represent the sister border of supratemporal fenestrae; postorbitofrontal not group of the Monjurosuchidae or a more basal clade (Gao contacting parietal; elongated neck consisting of 19 cervical & Fox, 2005). New evidence revealed in this study will help vertebrae; dorsal vertebrae 16 in number; interclavicle to resolve the relationships of the group within the essentially T-shaped, with great reduction of anteromedial Choristodera in future cladistic analyses. process; iliac blade oriented horizontally. The Early Cretaceous Shokawa ikoi from Japan shares Remarks: Hyphalosaurus lingyuanensis is known from many postcranial features with Hyphalosaurus. Because several specimens (Figs 2, 3) from the type Lingyuan area. the skull is almost completely unknown and important Since the original publication by Gao et al. (1999), little postcranial characters such as the cervical vertebral progress has been made towards understanding the count also remain uncertain for the Japanese taxon, it is anatomical details of this morphologically peculiar animal. not possible to provide a coherent diagnosis separating the With further preparation of the holotype and the discovery two genera at present. We retain the name Shokawa here, of new specimens, it is now possible to provide a thorough pending the discovery of additional materials that can help anatomical description of the species. A comparison with clarify the anatomy and taxonomic status of this genus. the congeneric species H. baitaigouensis in this study

750 Cretaceous reptile Hyphalosaurus from China, K.-Q. Gao and D. T. Ksepka

Fig. 2 Hyphalosaurus lingyuanensis: A) IVPP V11075 (holotype), nearly complete skeleton preserved in volcanic shale slab; B) PKUP V1052, topotypic specimen from Lingyuan (Early Cretaceous Yixian Formation). Both specimens with posterior tail omitted.

reveals new information to distinguish the two species from one another, leading to the revision of the diagnosis Osteology of Hyphalosaurus lingyuanensis of the type species presented above. As a result of this Gao et al. 1999 revision, two features have been removed from the Cranial skeleton species diagnosis. One feature was ‘pachyostotic dorsal ribs strongly sigmoid, imbricated distally with posteroventral Comparative study of several specimens (IVPP V11075, extension’, but it is now clear that the ventral imbrication uncataloged juvenile specimen from the GMC, PKUP of the ribs is preservational. Similar distortion is seen in a V1052) consistently shows a roughly pear-shaped skull few specimens of H. baitaigouensis (e.g. LPMC R-00065 configuration, with a pointed snout, laterally bulging and R-00066). The second feature, ‘third and fourth orbital region and short posterior expansion of the metatarsals subequal in length’ (Gao et al. 1999), is now supratemporal fenestra. This skull configuration is con- also known from specimens of H. baitaigouensis (e.g. sistent through ontogenetic development, as both the BMNHC V050) and thus no longer diagnostic at the species smallest specimen examined (GMC-juvenile specimen) level. and the largest specimen (IVPP V11075) show essentially

Cretaceous reptile Hyphalosaurus from China, K.-Q. Gao and D. T. Ksepka 751

interorbital bar as seen in H. baitaigouensis. The frontals, however, are posterolaterally widened with an extensive, slanted sutural contact with the fused postorbitofrontal. Posteriorly, the frontal has a transverse suture with the parietal at a level slightly posterior to the anterior border of the supratemporal fenestra, and in this aspect it is different from H. baitaigouensis (see below). The parietals are paired, forming a roughly squared table with very short supratemporal processes. The lateral border of the parietal is slightly concave, forming the medial border of the small supratemporal fenestra. A parietal foramen is absent as in other choristoderes. The maxilla (best shown on the right side of GMC juvenile) lacks a clearly defined dorsal process, and instead the medial portion takes the form of a low, inwardly scrolled flange. The anterior margin of the flange forms the posterior border of the external narial opening, and the posterodorsal margin of the flange meets the prefrontal and lacrimal. The jugal has an anterior process that forms a large part of the lateral rim of the orbit, and a well-defined dorsal process that contacts the fused postorbitofrontal. Fig. 3 Hyphalosaurus lingyuanensis: part and counterpart of an The extent of the posterior process cannot be ascertained. unnumbered juvenile specimen in GMC vertebrate fossil collections from The postorbital and postfrontal are fused into a postor- Lingyuan; Early Cretaceous Yixian Formation. bitofrontal. The postorbitofrontal forms the anterior border of the small supratemporal fenestra, but appears not the same configuration (Figs 2–4). The external narial to have a contact with the parietal. This condition differs openings are small, paired and anteriorly placed. The from that in H. baitaigouensis, which has a small contact orbits are proportionally large, and dorsally oriented. between the postorbitofrontal and parietal. The supratemporal openings are small (less than one-half Palate: The holotype of H. lingyuanensis (IVPP 11075) size of the orbit), while the infratemporal opening is exposes the palate, but this region was unprepared at the closed. The postorbital portion of the skull is significantly time the species was named and described. The holotype shorter than the anterior part of the skull, including the has since been further prepared (Fig. 4) and restudy of this snout plus the orbit. Such proportions of the skull are specimen together with observations from PKUP V1052 different from those in H. baitaigouensis, in which the (a topotypic specimen of the same species) provide a postorbital skull accounts for roughly one-half of the skull better understanding of the palate of hyphalosaurids. length (see below). The paired vomers share a long midline contact. The Skull roof: The morphology of the skull roof was hitherto vomer forms the entire medial and anterior border of the unknown for H. lingyuanensis, as the holotype skull is choana, and sends out a short process to form a portion of exposed in palatal view (Fig. 4A) and the skull of one other the lateral border as well. In PKUP V1052, a single row specimen (PKUP V1052) was split along the horizontal of small palatal teeth is preserved on the right vomer. The plane as the slab encasing it was excavated. Fortunately, a choanae are only slightly posteriorly displaced relative to new GMC juvenile specimen from the type locality shows the nares. Although the contact between the vomer and the relationships of the many elements of the skull roof pterygoid cannot be deciphered with absolute certainty, it with clarity (Fig. 4B). appears to occur at the posterior border of the choana. The premaxillae and nasals are not well exposed in any The palatines form the major portion of the lateral and of the three available specimens, and thus the detailed posterior borders of the choanae and meet the pterygoids morphologies of these skull elements cannot be ascertained in a long, straight sutural contact medially. The right palatine at this stage. However, the nasals were necessarily short preserves a few palatal teeth near its anterior tip in IVPP and narrow in keeping with the short and pointed snout. 11075 (Fig. 4A). Some parts of the palatal dentition have The paired prefrontals are elongated with an extensive clearly been lost to damage, so the scarcity of palatal teeth midline sutural contact. This feature is considered a key in this specimen and in PKUP V1052 is most likely due to synapomorphy of Choristodera (Gao & Fox, 1998). The preservational effects. Damage caused by the splitting of prefrontal-frontal suture is located slightly posterior to the slab makes it difficult to discern whether a nasopalatal the anterior borders of the orbits. The frontals are also trough was present, and also precludes identifying the paired, and strongly narrowed anteriorly to form a narrow palatine foramen.

752 Cretaceous reptile Hyphalosaurus from China, K.-Q. Gao and D. T. Ksepka

Fig. 4 Skull of Hyphalosaurus lingyuanensis: A) palatal view of the holotype skull IVPP V11075; B) dorsal view of the skull of a juvenile specimen in GMC collections.

The pterygoids are identifiable in the holotype and the Mandible and dentition: The holotype and all other left element is exposed in dorsal view in one slab of PKUP available specimens of the species have the mandibles V1052. In the holotype, the pterygoids are separated from preserved in articulation with the skull, making it difficult one another over most of their lengths, and show only a to discriminate the structural details of the jaw. The lower limited anterior contact. However, the asymmetry of the jaw is slenderly built, in accordance with the lightly built opening between the pterygoids suggests the two elements skull. The dentary and splenial can be identified, but the were displaced from one another by deformation. If so, boundaries of the more posterior elements of the lower the pterygoids may have shared a more extensive midline jaw are difficult to discern. The mandibular symphysis contact as in H. baitaigouensis. It is unclear from either is limited to the anterior extremity (IVPP V11075). The specimen whether the pterygoids or the parasphenoid retroarticular process is weakly developed but clearly complete the posterior border of the vacuity. defined. Monjurosuchidae and some neochoristoderes The suborbital fenestra is roughly subtriangular and lack a definite retroarticular process, although other slightly elongated. Location of the craniomandibular joint neochoristoderes possess a short, broad retroarticular is roughly at the same level as the occipital condyle, as seen process (Gao & Fox, 1998, 2005). in both the holotype and PKUP V1052 as well as in the In the original publication, the marginal teeth of the congeneric species H. baitaigouensis (LPMC unnumbered species were described as likely ‘slender, simple, and specimen). Unfortunately, much of the posterior half of needle-like’ (Gao et al. 1999) based on the exposed tips of the skull remains obscured by damage caused by the the maxillary teeth. Further preparation of the holotype splitting of the slabs in these specimens. has shown that the upper teeth of this animal are generally

peg-like. Posterior teeth are substantially smaller than V1052, GMC juvenile) confirms that all specimens possess those anterior ones, and the tooth crowns are weakly three sacral vertebrae. This agrees with other choristoderes, wrinkled with vertical ridges on the medial surface. All though Lazarussuchus inexpectens was described as having teeth are unicuspid, and broken tooth bases show no four sacral vertebrae (Hecht, 1992). The sacral vertebrae indication of developing plicidentine infoldings. are partially exposed in ventral view in the holotype, revealing that the robust sacral ribs are unfused to the vertebrae. The strongly expanded lateral ends of the sacral Postcranial skeleton ribs do contact one another (Fig. 6). Vertebral column and ribs: The vertebral column in the As described by Gao et al. (1999), the holotype preserves holotype consists of a total of 35 presacral, three sacral, 55 caudal vertebrae (PKUP V1052 shows a similar number). and more than 55 caudal vertebrae. All vertebrae have All but the first caudal have a shallow groove on the platycoelous centra, with essentially flat anterior and ventral surface of the centrum, and the groove is laterally posterior articular surfaces. flanked by well-developed longitudinal ridges (Fig. 6). The As described in the original publication, the elongate holotype also shows that at least the anterior caudal ribs neck of H. lingyuanensis consists of 19 cervical vertebrae are unfused to the centrum, though the rest seem tightly (Gao et al. 1999). This number is confirmed by observation articulated if not fused. Starting from the 4th caudal, of another adult specimen (PKUP V1052; Fig. 2B) and the the centra become more or less hour-glass-shaped with GMC juvenile specimen (Fig. 3) from the same locality a constricted middle portion and expanded anterior and and horizon. This number of the cervical vertebrae clearly posterior ends (Fig. 6). The caudal ribs are laterally distinguishes the type species from H. baitaigouensis, directed and become progressively shorter toward the end which possesses 24 cervical vertebrae. The holotype shows of the tail. that the cervical vertebrae are narrow and elongate, with Gastralia: As in other choristoderes, a mass of gastralia the 3rd through the 19th vertebrae varying between 10 is developed ventrally at the abdominal region (Figs 2, 5). and 12 mm in length. Most of the cervical centra in the The gastral elements are arranged in longitudinal and holotype were damaged by the splitting from a horizontal transverse rows to form a sheet of bony protection plane, but the last two cervical vertebrae are well preserved between the pectoral and pelvic girdles. The extensive and reveal a well-defined ventral crest. All but the first two gastral sheet starts anteriorly at the level of the 7th dorsal cervical vertebrae bear ribs. These ribs are double-headed vertebra, and posteriorly ends at a level below the 15th or and become progressively longer and more spatulate the 16th dorsal vertebra. Individual elements are stout and posteriorly (Fig. 5). spindle-like, with a cylindrical shaft and pointed ends. The dorsal series of the type species was described as Each body segment is associated with two to three hori- having 16–17 vertebrae (Gao et al. 1999). Re-examination zontal rows. Thus, there are more than 20 horizontal rows of the newly prepared holotype and other topotypic of the gastralia, each consisting of a central element in specimens (PKUP V1052, GMC juvenile specimen) shows articulation with two lateral elements. a count of 16 dorsal vertebrae is correct. This number Pectoral girdle and forelimb: The pectoral girdle and the indicates that the trunk of the H. lingyuanensis is forelimbs are well preserved in the holotype (Fig. 5) and all shorter than that of H. baitaigouensis by three vertebrae the referred specimens. The interclavicle was mistakenly (see description below). The dorsal vertebrae are equal listed as unpreserved in the original publication (Gao et al. in length or slightly shorter than the cervical vertebrae. 1999). Additional preparation of the holotype revealed The first four anterior dorsal vertebrae are completely that the interclavicle was in fact embedded in the shale preserved and have a smooth ventral surface with no matrix. Sharply distinguished from that in the congeneric clearly defined crest. The next six dorsal vertebrae exhibit species H. baitaigouensis, the interclavicle of the type slight damage to the centrum, leaving the morphology of species is essentially T-shaped and has a poorly defined their ventral surface uncertain. The posteriormost six anteromedial process (Fig. 5). The anterior two-thirds of dorsal vertebrae are completely preserved, but are the stem is slightly widened giving it a sword-like shape, largely obscured by a thick sheath of gastralia. All dorsal while the posterior one-third tapers to a point. vertebrae are preserved in articulation with their ribs, As shown on the left side in the holotype, the scapula although the distal ends of the ribs have been displaced has a short blade with a strongly expanded dorsal end. posteriorly by compression of the specimen. The dorsal This expansion creates a well-developed neck at the lower ribs are unicapitate and strongly expanded distally. The part of the blade near the glenoid cavity. An acromion high degree of pachyostosis seen in the ribs is similar to process is absent. The dorsal border of the scapular blade that in Neochoristodera. is convex dorsally, with a thickened rim for muscle attach- The original description of H. lingyuanensis estimated ment. The lower part of the scapula is a greatly widened the number of sacral vertebrae as either three or four. plate, which has its curved ventral border in articulation Comparison of the holotype with other specimens (PKUP with the coracoid plate. At the posterior border, the

Fig. 5 Hyphalosaurus lingyuanensis (holotype IVPP V11075): photograph and line drawings of the pectoral girdle and fore limbs.

scapula contributes slightly over half of the glenoid cavity, absent, a derived condition within Diapsida (Evans, 1988). with the remaining portion contributed by the coracoid. There is also no trace of ossified sternal plates. No supraglenoid foramen is identified on the scapula, and The coracoid is a large suboval plate, with a rounded thus such a foramen is probably absent in Hyphalosaurus medial border. At the dorsomedial border, the coracoid is as in Monjurosuchidae (Gao & Fox, 2005). A cleithrum is thickened and projects dorsally to form part of the glenoid

Fig. 6 Hyphalosaurus lingyuanensis (Holotype IVPP V11075): photograph and line drawings of the pelvic girdle and hind limbs. cavity, but the actual shape of the cavity is hard to below the scapula-coracoid suture. Such a foramen is determine due to slight disarticulation on both sides of the commonly seen in other diapsids and serves as the passage specimen. Anteroventral to the glenoid cavity, a coracoid of the supracoracoid nerve and its associated blood vessels (supracoracoid) foramen penetrates the coracoid plate (Romer, 1956).

The clavicles are preserved in tight articulation with the has a phalangeal formula of 2–3–4–4–3 as shown on the scapulae and the interclavicle. The clavicles are only weakly left and right side of the holotype. angled at midpoint, giving the bone a boomerang-like Pelvic girdle and hind limb: All three pelvic elements in shape. The dorsal half of the clavicle is attached to the the holotype are well ossified and preserved in articula- anteromedial border of the scapula. The ventral half of tion on the left side (Fig. 6), but on the right side these the bone extends more or less horizontally and interlocks elements are slightly damaged by splitting and incomplete. with a groove on the anterior border of the interclavicle On both sides of the specimen the ilium is exposed in crossbar. Medially, the two clavicles may contact one lateral view, with weakly developed surface rugosities along another at the ventral midline (Fig. 5). the dorsal border of the iliac blade for attachment of axial The holotype includes all the forelimb elements, well- muscles (Romer, 1956). The iliac blade lacks an anterior preserved and in articulation, except for the probable loss extension but has a short and deep posterior elongation of a few carpals. The humerus has a short shaft and moder- beyond the acetabulum, a morphology that is primitive ately expanded proximal and distal ends. The distal end is within Diapsida. The iliac blade is oriented horizontally. As expanded and twisted at an approximately 45° angle in consistently shown in both juvenile and adult specimens, relation to the proximal expansion. The better-preserved this orientation of the blade is a taxonomically significant right humerus shows that the proximal articular surface is difference from the more vertical orientation in H. well ossified, indicating the maturity of the individual at baitaigouensis (see below). Between the iliac blade and death. The proximal ventral surface is concave, with a well- the acetabulum is a constricted neck. Constriction is variable defined subtriangular depression tapering toward the among different taxa of choristoderes and also shows shaft. The anterior border of this depression marks the ontogenetic variation in Champsosaurus (Erickson, 1972). presumably well-developed deltopectoral crest, which is Ventrally, a large part of the base of the ilium is occupied broken off on both humeri as a result of splitting the slab. by the acetabulum, the dorsal rim of which is formed by The dorsal surface of the distal end is smoothly convex the weakly developed supra-acetabular buttress. as preserved on the right element. The status of the The puboischiadic plate is formed by a large pubis and ectepicondylar and entepicondylar foramina is indetermi- a slightly smaller but more stoutly built ischium. The two nate due to breakage. elements share a tight sutural articulation, leaving no The epipodial elements and the forefoot were largely space for a thyroid fenestra. The pubis bears a well- unknown at the time of the original publication as they developed pectineal tubercle, the thickness of which is were embedded in the matrix. Subsequent preparation of proportionally comparable to the expanded condition in the holotype thereafter shows that the epipodial elements Champsosaurus (Romer, 1956). An obturator foramen are preserved crossing one another on both sides of the perforates the thickened pubic plate near the distolateral specimen. The radius is slightly longer than the more margin as in other choristoderes. The ischium contributes stoutly built ulna. The proximal end is expanded and a small part of the acetabulum, while the pubis forms only slightly wider than the distal end in both elements. As in the anteroventral border of the pelvic cavity. A marked other choristoderes, no olecranon process or sigmoid rugose angle projects from the posterior border of the notch is developed proximally on the ulna. Loss of the ole- ischium. This tubercle is similar to that seen in most cranon process and its associated sigmoid notch has been neochoristoderes, but sharply different from the spike-like recognized as a derived morphology at the neodiapsid process in monjurosuchids (Gao & Fox, 2005; Gao & Li, 2007). level (de Braga & Rieppel, 1997; Evans, 1988). The femur in the holotype is nearly completely preserved At least nine carpal elements can be identified in the left on the left side, but is damaged by breakage on the right. manus of the holotype (Fig. 5). The same number and pat- The femur is roughly 136% of the length of the tibia in the tern are also seen in PKUP V1052. The two large proximal holotype individual, the largest studied here (see Table 1). elements are evidently the radiale and ulnare. A much However, the proportions of the limb bones change smaller element distal to the radiale and ulnare can be markedly over ontogeny. In a juvenile individual (Fig. 3) identified as the intermedium. Two or three smaller ele- the femur is relatively longer at 168% the length of the ments positioned near metacarpals I–II are tentatively tibia, and in another specimen (PKUP V1052, slightly smaller identified as the medial centrale and lateral centrale. than the holotype), the femur is 158% of the length of the There are four distal carpals. Distal carpal 5 is absent. No tibia. The femur is basically a straight rod with weakly known member of the neodiapsid Choristodera has shown expanded proximal and distal ends. The expanded distal the presence of distal carpal 5, regardless of whether the end is twisted at a 40–45° angle with respect to the absence is interpreted as the result of fusion with meta- expanded proximal end. As shown on the left element, the carpal IV or a simple loss of the element (see Romer, 1956). intertrochanteric fossa on the ventral aspect of the femur Of the five metacarpals, metacarpal I is the shortest but is greatly reduced to a shallow and short depression, the most stoutly built, and metacarpal III is the longest, in extending just slightly more than one-fifth of the femoral keeping with the relative length of the digits. The forefoot length. There is neither any sign of the development of a

Table 1 Lengths of major elements from Hyphalosaurus lingyuanensis and Hyphalosaurus baitaigouensis in millimeters. Measurements for LPMC specimens were taken with dial calipers and rounded to the nearest 1 mm, other measurements were taken with digital calipers and rounded to the nearest 0.1 mm

Hyphalosaurus lingyuanensis Hyphalosaurus baitaigouensis

PKUP IVPP PKUP PKUP BMNHC PKUP LPMC BMNHC BMNHC LPMC LPM C Specimen V1052 V11075 V1057 V1058 V050 V1056 R00052 V053 V060 R00066 R00065

Skull 54.1 57.8 13.6 16.1 27.0 33.0 35.0 36.0 33.0 66.0 65.0 Humerus 39.6 40.0 4.5 4.7 13.5 24.0 20.0 27.3 27.6 45.0 46.0 Ulna 25.5 26.0 3.1 3.5 9.0 15.8 13.0 15.3 17.9 – 28.0 Radius 25.5 27.0 2.9 3.1 9.5 15.9 13.0 15.3 19.3 – 28.0 Femur 50.5 43.0 4.9 5.1 16.5 27.6 21.0 29.6 31.6 52.0 52.0 Tibia 31.9 31.5 3.2 3.7 11.0 17.0 14.0 18.1 19.1 30.0 31.0 Fibula 30.5 31.0 3.0 3.3 10.0 16.4 13.0 17.5 18.9 28.0 29.0

fourth trochanter near the distal end of the intertrochanteric the removal of the anterior portion of the slab precludes fossa, nor any evidence of the adductor ridge that is identification of species by vertebral formula. Close normally associated with the fourth trochanter. examination confirms that the remaining portion of the The shafts of both the fibula and the tibia have a skeleton, including the integument, is authentic. straight external border, but a concave internal border, A parasagittal row of large, oval scutes topped with creating a spindle-shaped gap between the articulated low midline keels runs along the flank of both specimens bones. The slenderly built fibula is distally expanded, in and is best preserved in GMC V351 (Fig. 7B). The row contrast to the proximally expanded tibia (Fig. 6). The continues onto the base of the tail without significant distal end of the fibula articulates with both the astragalus decrease in size in PKUP V1052. These large keeled scutes (tibiale) and calcaneum (fibulare), while the tibia articu- are evenly spaced, with smaller, irregularly arranged, lates only with the astragalus. At the proximal end of the smooth polygonal scales occupying the area in between tibia, a weakly developed cnemial crest can be identified them. Smooth polygonal scales overlap the last preserved extending from the head toward the middle portion of large keeled scutes, indicating the patch of integument the shaft. bearing smaller keeled scutes has been folded over this The tarsus of the holotype includes six ossified elements. part of the flank integument. A single small keeled oval Six tarsals have also been reported for adults of Mon- scute with an area about one-fourth that of the others is jurosuchus (Gao et al. 2000) and for simoedosaurids (Liu, preserved anterior of the femur in GMC V351. This keeled 2004). The astragalus and calcaneum remain separate scute appears to represent another parasagittal row and form the proximal portion of the tarsus. Four smaller located either ventral or dorsal to the flank row. The small elements represent distal tarsals 1–4, and distal tarsal 5 is scales of the tail are quadrilateral and are more regularly absent. The same number and pattern are also present in arranged than those of the flank. In PKUP V1052, the tail PKUP 1052. Metatarsals III and IV are subequal in length is twisted at a level between the14th and 15th caudal and are substantially longer than the remaining metatarsals. vertebra, so that a lateral view of the tail and integument Metatarsal V is best preserved in the left hind foot, where is exposed posterior to this point. Integument impressions it shows a strong proximal expansion but no development of extend for a significant distance from both the dorsal and plantar tubercles. The phalangeal formula for the hind foot ventral margins of the caudal vertebrae, suggesting the is 2–3–4–4–3, as clearly shown on the right side (Fig. 6). height of the tail may have been increased by soft-tissue projections. The polygonal scales surrounding the hind- limb skeleton are irregular and smaller than the polygonal Integument scales separating the keeled scutes. Impressions of soft tissue are preserved in two specimens Integumentary impressions have previously been reported of Hyphalosaurus examined in this study. PKUP V1052 in Champsosaurus (Brown, 1905; Erickson, 1985) and (Fig. 7C–E) is a specimen of H. lingyuanensis. The other Monjurosuchus splendens (Gao et al. 2000). The integument specimen, GMC V351 (Fig. 7A–B), cannot be identified to of Champsosaurus gigas is made up of fine scales. Scales of the species level because autapomorphy-bearing areas of the upper back are small and rhomboid with sharp crests, the anatomy are obscured by artificial modification of the scales on the lateral surface of the tail are low, smooth and specimen. The skull and part of the neck are clearly part of pustulate, and scales on the lower flank are large and a separate individual and were joined to the specimen to circular (Erickson, 1985). There is no evidence of large keeled form a composite. This is particularly unfortunate because scutes in Champsosaurus, but patches of integument are

Fig. 7 Integument of Hyphalosaurus: A) Hyphalosaurus sp. (GMC V351) in dorsal view. Arrow indicates the area where cervical vertebrae and a skull from a separate individual have been artificially attached; box indicates area shown in (B). B) Close-up of integument impressions showing large, ovoid, keeled scutes surrounded by small irregular polygonal scales. C. Hyphalosaurus lingyuanensis (PKUP V1052) in ventral view; boxes indicate areas featured in (D) and (E). D) Skin impressions adjacent to dorsal ribs, including large keeled scutes (arrows) and small irregular polygonal scales. E) Skin impressions adjacent to caudal vertebrae, showing quadrilateral scales.

currently known from only a few regions of the body. The Type locality and horizon: Baitaigou village near Toutai, integument of Monjurosuchus consists largely of small Yixian County, Jinzhou City of Liaoning Province; Early overlapping scales, which are largest on the dorsal surface Cretaceous Yixian Formation (see remarks below). of the body, at least at the hind limb (Gao et al. 2000). Referred specimens: PKUP V1056-1058, BMNHC V014- 053, Monjurosuchus also possesses large ovoid, keeled scutes, LPMC R-00052, LPMC R-00065-00066, and many unnumbered arranged in parasagittal rows and surrounded with specimens in BMNHC, IVPP, LPMC and PKUP collections. smaller papilloid scales. The striking similarity between Diagnosis (revised from Ji et al. 2004b): Hyphalosaurid these scales in Monjurosuchus and Hyphalosaurus provides choristodere differing from the congeneric species H. additional evidence that the apomorphic hyphalosaurids lingyuanensis in having the frontal/parietal suture located belong within Choristodera. Integument impressions at the midlevel between the orbit and the supratemporal indicate that Monjurosuchus possessed webbed feet (Gao fenestra; fused postorbitofrontal medially having exten- et al. 2000). The integument is incompletely preserved sive sutural contact with both the frontal and the parietal; around the manus and pes in both specimens of Hyphalo- possessing greater elongation of the neck, consisting of 24 saurus, but a patch of scales visible between the proximal cervical vertebrae; 19 dorsal vertebrae; more than 60 phalanges of the right pes in PKUP V1052 suggests some caudal vertebrae; deep and horizontal groove developed degree of webbing in Hyphalosaurus. on the lateral surface of the dorsal vertebral centra; interclavicle rhomboid in shape, lacking a well-developed cross bar; iliac blade vertically oriented. New observation and taxonomic revision on Remarks: The original designation of the holotype is Hyphalosaurus baitaigouensis problematic, as the holotype skeleton and the eggs outside the skeleton must be considered to be different Species Hyphalosaurus baitaigouensis Ji et al. 2004b individuals. Following the ICZN rules (ICZN, 1999: 73.1), the Holotype: CAGS-IG-03-7-02, incomplete skull and partial 11 leathery-shelled eggs associated with the holotype postcranial skeleton (excluding the 11 leathery-shelled skeleton must be excluded from the holotype designation; eggs from the original designation; see remarks below). therefore, the original type designation should be corrected

to include only the incomplete skull and its associated partial postcranial skeleton as a single specimen. The original description of the holotype is also problematic. The holotype skull is badly damaged and as illustrated in Ji et al. (2004b: Fig. 1) it contains at least five questionable structure identifications. Moreover, many key features (e.g. external nares) were not shown in the poorly preserved skull. A thorough description is needed to clarify the cranial morphology of the species (see below). Based on our observation of a large number of well-preserved specimens, we have extensively revised the diagnosis of the species as shown above. The single diagnostic feature mentioned in the original publication was the total of 26 cervical vertebrae (see Ji et al. 2004b). However, as described below, all the fully articulated specimens that we have examined have 24 cervical vertebrae. The miscount by the original authors was probably caused by including the two anteriormost dorsal vertebrae as cervical vertebrae. As shown in the original publication (Ji et al. 2004b: plate 1), the cervical series was distorted and the incompletely preserved pectoral girdle and right arm have been slightly displaced. Because of distortion in the holotype, the original authors miscounted the dorsal vertebrae as 17 in number, while multiple fully articulated specimens that we have observed show 19 dorsal vertebrae as described and figured below. In the original publication, the type horizon was described as the upper part of the Chiufotang Formation Fig. 8 New specimens of Hyphalosaurus baitaigouensis: A) LPMC R-00065; B) LPMC R-00066; both nearly complete skeletons from the (Ji et al. 2004b). Detailed stratigraphic study, however, has upper Yixian Formation exposed near Yizhou. shown that the fossil horizon is probably part of the Yixian Formation (Wang et al. 2004). The latter stratigraphic designation is followed in this paper. Cranial skeleton The skull is small proportional to body size, with paired Osteology of H. baitaigouensis and elongate nares, large orbits and posteriorly flared The description below is based primarily on the study of supratemporal fenestrae (Figs 8–11). The infratemporal several fully prepared specimens (BMNHC V014, BMNHC fenestrae are fully closed in adults but remain open in V050, PKUP V1056, LPMC R-00065, LPMC R-00066). These small juveniles (pers. comm. from Hou Lianhai on LPMC specimens are presumed to represent a range from specimens). The shape of the skull also shows minor medium-sized subadults to large fully-grown adults, based ontogenetic variations: the skull of small to medium sized on the range of sizes (see Table 1) and degree of limb individuals is generally lancelet shaped, with a pointed ossification observed in our study. Among these, LPMC snout and strong posterior flaring of the supratemporal R-00065 and R-00066 (Fig. 8) are the largest specimens known fenestrae, whereas large individuals tend to have a for this species. The former has a skull length of 66 mm (entire blunter snout as shown in LPMC R-00065. The skull body length of > 1050 mm), and the latter specimen of 65 mm appears to be strongly flattened, a feature seen in other (entire body length of 1100 mm). We examined approx- choristoderes. However, all fossils examined in this study imately 50 additional specimens of H. baitaigouensis in have undergone post-mortem compression in variable the BMNHC, GMC, LPMC and PKUP collections, though degrees and the true degree of flattening may have been most of these were of varying completeness, quality of somewhat less in life. preservation and stages of preparation. Study of these specimens reveals previously unknown information regard- Skull roof ing several cranial elements (premaxilla, frontal, and quadratojugal), and allows us to revise the description of The premaxillae are unknown from the holotype (Ji et al. several other elements (postorbital, postfrontal, lacrimal, 2004b: Fig. 1), but are well preserved in several specimens and squamosal) to clarify the osteology of the species. used in this study. As best shown in the fully articulated

Fig. 10 Skull roof of Hyphalosaurus baitaigouensis: photograph and line drawing of LPMC R-00065.

skull of LPMC R-00065, the premaxilla has a blunt tooth- bearing base that carries at least four teeth. Four teeth are also observed on the right premaxilla of BMNHC V050. The dorsal process is slender and long, terminating at a point slightly posterior to the mid-level of the external narial openings. The narial openings are clearly paired, elongate and dorsally placed, as best shown in LPMC R-00065. The anterior surface of the premaxilla is penetrated by several small and rounded foramina, as seen in other choristoderes, and the posterolateral end of the premaxilla has a small notch for articulation with the maxilla (best shown in BMNHC V050 and LPMC R-00065). The maxilla, as shown on both sides in BMNHC V014, has a small anterior process that inserts into the small notch on the premaxilla. The dorsal rim of this anterior process is slightly notched for the lateral border of the external narial openings. The middle part of the maxilla lacks a dorsal process, but has a relatively straight sutural contact with the nasal. At the level of the anterior border of the orbit, the maxilla is dorsolaterally notched, accepting the anterior tongue of the jugal, which forms the entire lateral rim of the orbit (best shown on the right side in BMNHC V014; Fig. 11A). The posterior extent of the maxilla is unknown from this specimen, but can be inferred as reaching the posterior border of the orbit, where the marginal tooth row ends in the lower jaw. The nasal was identified on the right side of the holotype skull but labeled with a question mark (Ji et al. 2004b: Fig. 9 New specimen of Hyphalosaurus baitaigouensis: BMNHC V050; a Fig. 1). Several well-preserved specimens used in this study nearly complete skeleton from the upper Yixian Formation exposed near show that the nasals are paired and elongated. The nasals Yizhou. have a short midline suture anteriorly, but diverge posterolaterally between the maxilla and the prefrontal. Each

Fig. 11 Skull roof and palate of Hyphalosaurus baitaigouensis: A) skull roof in BMNHC V014; B) skull roof in BMNHC V050; C) palate in an unnumbered specimen in the LPMC collections. nasal is anteriorly notched for the posterior border of the BMNHC V050, there appears to be a small triangular bone narial opening, and each has a small process abutting the forming the anterior rim of the orbit. This bone articulates dorsal process of the premaxilla. The posterior extension medially with the prefrontal and laterally with the maxilla. of the nasal has a small process that wedges between the In BMNHC V014, the sutural patterns of the nasal with its prefrontal and the lacrimal (Fig. 10). The limited midline surrounding elements are unclear, but large specimens in contact between the nasals contrasts with the more exten- the LPMC collections (LPMC R-00065, R-00066) preserve a sive contact or fusion seen in other choristoderes. This modest-sized, triangular lacrimal, and display similar feature may be taxonomically significant at the species sutural patterns as in BMNHC V050. In LPMC R-00065, the level or a higher level, pending information on the nasals lacrimal foramen is visible. in other hyphalosaurids. The frontals are unknown from the holotype, but a The prefrontals are paired and share a long medial large number of well-preserved specimens used in this sutural contact. The prefrontals are widest anterior to the study show that they are paired, slender and elongate. The orbit between the lacrimals, tapering both anteriorly frontals narrow anteriorly to form an interorbital beam towards the contact with the nasals and posteriorly that articulates with the prefrontals and posteriorly towards the contact with the frontals. The anterior half of become slightly widened and they share an oblique suture the prefrontal shares an oblique suture with the nasal with the postorbitofrontals. The frontals form the larger laterally. The anterior process extends to the level close to half of the interorbital beam but barely contribute to the the posterior border of the nares. Posteriorly, the prefrontal/ posterior rim of the orbit. The interdigitating frontal/ frontal articulation is roughly at the midlevel of the parietal suture is roughly transverse and is located at orbit and is formed by the small posterior process of the the midlevel between the orbit and the supratemporal prefrontal overlapping the small notch of the frontal fenestra, a diagnostic feature of the species (best shown in (Figs 10, 11A,B). BMNHC V014, V050, LPMC R-00065). The status of the lacrimal was uncertain in the original The postorbital and postfrontal were misidentified as publication, where a long strip-like structure was ques- separate elements and were illustrated as disarticulated tionably identified as the lacrimal. On the left side of and far apart in the holotype specimen (Ji et al. 2004b:

Fig. 1). However, all well-preserved specimens used in this ing suture with the postorbitofrontal laterally. The pineal study clearly show that the two bones are fused into a foramen is clearly absent in all observed specimens, as in single postorbitofrontal (Figs 10, 11). In one relatively other choristoderes. The posttemporal processes are small specimen (BMNHC V014) there are differences in the slender and long, diverging posterolaterally to the posterior coloration of the two bones. On both sides, the supposed extremity of the skull, where the parietal meets the medial area of the postfrontal (the more medial element) is slightly extension of the squamosal. Along the medial border of darker than the postorbital part, although no suture can the supratemporal fenestra, the parietal develops a be identified. A similarly sized individual (BMNHC V050) downward flange to meet with several other elements and a large specimen (LPMC R-00065), however, show and complete the lateral wall of the braincase (see below). no evidence of a suture or other sign of differentiation The squamosal was incorrectly labeled in the holotype between the two parts of the postorbitofrontal. The (see Ji et al. 2004b: Fig. 1), as the structure labeled ‘squamosal’ postorbitofrontal has a slightly notched anterior margin is obviously part of the postorbitofrontal. In fact, the forming the entire posterior rim of the orbit. Medially, the squamosal is an elongate element as best shown in postorbitofrontal has a straight, posterolaterally oriented BMNHC V050. In dorsal view, the squamosal has the anterior sutural contact with both the frontal and the parietal process in contact with the posterior extension of the (different from H. lingyuanensis; see above). Laterally, the postorbitofrontal, and thus it forms a large part of the postorbitofrontal shares a straight sutural contact with the lateral border of the supratemporal fenestra. This anterior deepened posterior portion of the jugal. The posterior process may ventrally contact both the jugal and quadra- border of the fused postorbitofrontal is notched to form tojugal, but the actual sutural pattern between these the entire anterior rim of the supratemporal fenestra and elements is unclear. The posterior part of the squamosal a well-developed posterolateral process attaches to the develops a roughly triangular medial wing that meets medial side of the squamosal, forming the anterior part of the posttemporal process of the parietal. Within the the dorsal rim of the supratemporal fenestra as well. supratemporal fossa, the slightly curved anterior border of The jugal has a slender and blade-like anterior process the squamosal wing sutures with the quadrate. that forms the ventral rim of the orbit. The tongue-like Palate and braincase: The vast majority of H. baitaigouensis anterior end of the process articulates with the lacrimal specimens are exposed in dorsal view, and thus the palate and maxilla (best shown on the right side in BMNHC V014; remains incompletely known for this species. Most of our Fig. 11A). The anterior process of the jugal is well preserved information on the palate of the species is derived from an on the left side in BMNHC V050, but is slightly disarticulated unnumbered specimen in the LPMC collection (Fig. 11C), from the maxilla as a preservational artifact. On the right the only fully prepared specimen exposed in ventral view. side in BMNHC V050, the process is still in articulation with The small, subcircular internal choanae show a moderate the maxilla, though the tip of the process is broken. As degree of posterior displacement, opening at approximately shown on both specimens, the jugal lacks a dorsal process one-third of the length from the anterior to the posterior at the posterior border of the orbit; instead, the dorsal end of the marginal tooth row. A nasopalatal trough runs border of the jugal has a roughly straight sutural contact posteriorly from the choana in Neochoristodera and is with the postorbitofrontal (Fig. 11A,B). Posterior to the also present as a shallow groove in Monjurosuchidae. orbit, the jugal is deepened and is notched for articulation However, the presence or absence of this structure cannot be with the quadratojugal. confirmed in H. baitaigouensis. The suborbital fenestra is The quadratojugal was not identified in the holotype. visible on both sides of the skull and is subtriangular in shape. This bone is incompletely exposed on the right side of Due to preservation and overlying portions of the BMNHC V050, and is often obscured by dorsal elements in mandible, details of the anterior tip of the snout are other specimens. The posterior extent and the role of this unclear and it is not possible to identify the sutures element in the closing of the infratemporal fenestra in between the vomer, palatine and pterygoid with complete adult individuals are unclear, but its anterior articulation confidence. Regardless, it is clear that the vomers share with the jugal is clearly by a process fitting in the notch of a long midline contact as in H. lingyuanensis and bear at the jugal as shown on the right side of BMNHC V014 and least one row of palatal teeth. The exact relationship of the left side of BMNHC V050 (Fig. 11A,B). In the two largest the vomer to the maxilla is less certain. It appears these specimens (LPMC R-00065, R-00066), the quadratojugal is bones contact each other as in other choristoderes, but the either concealed by other bones or damaged by breakage, extent of the contact is uncertain. No clear suture between thus providing no reliable information on the morphology the pterygoid and palatine is identifiable in this specimen, of this skull element. but we presume that the region medial to the suborbital The parietals are paired elements that form the entire fenestra includes the contact between these two elements. medial border of the supratemporal fenestra. Anteriorly, If this is correct, the palatal tooth row running between the parietals form a roughly trapezoidal table that shares the suborbital fenestra and the internal choana is part of a transverse suture with the frontals anteriorly and a slant- the palatine.

There is a significant gap between the pterygoids (Fig. 11C), unlike the condition in Monjurosuchidae and Neochoristodera, in which the pterygoids share a long midline suture. Two rows of small palatal teeth stud each pterygoid, beginning at the suture with the parasphenoid and continuing to the level of the suborbital fenestra. Each row appears to be a single tooth position wide. Whether the transverse flange of the pterygoid is also toothed cannot be determined with certainty. As in other choristoderes, the palate is akinetic, with the pterygoid and parasphenoid sharing a tight sutural contact. The interpterygoid vacuity is enclosed by the parasphenoid rostrum posteriorly and the pterygoids anteriorly. In size, the interpterygoid vacuity is proportionally larger than that of Champsosaurus or Simoedosaurus, but smaller than that of Philydrosaurus or Tchoiria. The interpterygoid vacuity does not extend as far as the posterior edge of the suborbital fenestra. The ectopterygoid is exposed in dorsal view through the orbit in several specimens (BMNHC V014, V050). The bone is triradiate with short anterior and posterior processes and a well-developed pterygoid process. The pterygoid process is slightly constricted at its lateral end, as in Cteniogenys (Evans, 1990). The ventral surface of the braincase is well exposed in the unnumbered specimen from the LPMC collections (Fig. 11C). The basisphenoid is unexpanded posteriorly and the parasphenoid rostrum is short and broad. This gives the ventral surface of the braincase a flask-like Fig. 12 Vertebral column of Hyphalosaurus baitaigouensis (LPMC shape, with the basisphenoid forming the base and the R-00065). Note the sharp distinction of the neural spines between the cervical and dorsal series. parasphenoid forming the thick neck. Projection of the basal tubera is very weak. The craniomandibular joint is located at roughly the same level with the occipital process), which approaches the anterior interior border of condyle as in the type species (see above). Fine details of the supratemporal fossa. The anterior margin of the the occipital condyle itself are not observable. quadrate shares sutures with the element identified as the The lateral wall of the braincase is best observed on the possible neomorph and the ventral flange of the parietal right side of BMNHC V050. The parietal table projects a (Fig. 11A). At this suture a small foramen opens. If the ventral flange. The squamosal sends a triangular medial tentative identification of the neomorph proves correct, process to contact the posttemporal process of the parietal. this opening is the quadratojugal foramen. The posterior end of this triangular plate forms the posterior extremity of the skull and the anterior border of this triangular process sutures with the quadrate. Anterior Axial skeleton to the quadrate, an inverted triangular bone forms part of All the specimens used in this study consistently show that the lateral wall of the braincase. This bone may represent the cervical vertebrae are 24 in number, contrary to the the neomorph present in Neochoristodera, but better counting of 26 in the original description by Ji et al. (2004b). specimens are desirable for confirmation of this important Large specimens (LPMC R-00065, R-00066) also display a feature. Anterior to the inverted triangular bone is a robust sharp distinction between the cervical and dorsal series: in ventral extension from the parietal table. The left side of the the cervical vertebrae the neural spine is a low and simple skull in BMNHC V050 shows that a major portion of the crest, but starting from the first dorsal vertebra the neural lateral braincase wall has been crushed into small pieces spine becomes expanded with a rugose dorsal surface within the supratemporal fossa, though the triangular plate- (Fig. 12). The centrum of each cervical is slightly longer like medial extension of the squamosal is well preserved. than tall. BMNHC V050 shows breakage of the 21st cervical In BMNHC V014, the braincase is well exposed on both vertebra, but the number of cervical vertebrae has not sides of the skull. Examination of the squamosal confirms been artificially altered in any manner. The 17th through observations made in BMNHC V050. The quadrate shows the 24th cervicals of this specimen show slight shifting of a well-defined anterolateral extension (quadratojugal the neural arches towards the right, but the arches are

The tail is greatly elongated, accounting for more than half of overall body length. There are more than 60 caudal vertebrae preserved in BMNHC V050. This caudal count is consistent with other well-preserved and prepared specimens we observed, including LPMC R-00066. The anterior and middle caudal vertebrae are slender, elongate and laterally compressed, bearing a tall and spike-like neural spine. The neural arch of the first caudal is disarticulated from the centrum, but in all posterior caudal vertebrae the neural arch is fused to the centrum. The spike-like neural spines remain well developed through- Fig. 13 Vertebral column of Hyphalosaurus baitaigouensis (PKUP out almost the entire caudal series, but the last few vertebrae V1056). Arrows pointing to deep horizontal grooves developed in the are reduced to tiny cylinders lacking recognizable spines. lateral surface of the centrum in the dorsal series. The tips of the transverse processes of the first few vertebrae are posteriorly deflected, but for the rest of the still partly in articulation with the centra. This slight dis- caudal series the transverse processes are oriented per- articulation indicates that the neural arches and centra are pendicular to the centrum. unfused as typical in choristoderes. The dorsal vertebrae are well exposed in BMNHC V050 and many other specimens. There are 19 dorsal vertebrae, Appendicular skeleton along with the cervicals providing a total of 43 presacral The interclavicle is exposed in dorsal view on the left side vertebrae for H. baitaigouensis. The dorsal vertebrae are of the vertebral column in BMNHC V050 (Fig. 14). shortened anterior-posteriorly and are slightly taller than long. In many of the dorsal vertebrae in BMNHC V050, the neural arch is disarticulated from the centrum, leaving the articular surface of the centrum exposed in dorsal view. The centrum is platycoelous, typical for choristoderes. The centrum of the 13th dorsal vertebra is exposed in lateral view on the left side, and the lateral surface of the centrum has a deep and horizontal groove, also clearly visible in PKUP V1056 (Fig. 13), collected from the same formation and horizon as the holotype of the species. This feature is absent in H. lingyuanensis and is recognized in this study as diagnostic for H. baitaigouensis. In marked contrast to the cervical series, the neural spines of the dorsal vertebrae have a laterally expanded and rugose dorsal surface (best shown in LPMC R-00065, R-00066). Erickson (1987) hypothesized that the rugose neural spine apices of Simoedosaurus dakotensis provided attachment surfaces for a sagittal row of large scutes. We posit a similar function for the dorsal neural spines of H. baitaigouensis. The distinct expansion of the neural spine ends at the third sacral vertebrae, and the following caudal vertebral neural spines have a markedly different tall and triangular spike-like shape. The dorsal ribs are greatly expanded and terminate abruptly at their distal ends. Three sacral vertebrae are identified in BMNHC V050 and other specimens used in this study. In all three sacral vertebrae the neural arch is disarticulated from the centrum and the neural spine is strongly expanded, as in the dorsal vertebrae. As exposed on the left side of the specimen, the sacral ribs are also unfused to the centrum, and have been slightly disarticulated from their associated Fig. 14 Photograph and line drawings of BMNHC V050, showing the sacral vertebra. The first sacral rib is the longest, the pectoral girdle and the forelimbs of Hyphalosaurus baitaigouensis. Note second the most robust, and the third is shortest. the interclavicle lacks a crossbar.

Although partly obscured by the scapula blade, clavicle and several ribs, the base of the interclavicle is clearly rhomboid in shape with a well-developed triangular anterior process. However, the interclavicle lacks a well- developed crossbar. This configuration of the interclavicle is different from the T-shaped condition in the type species H. lingyuanensis (Gao et al. 1999) and is another diagnostic feature of the species recognized in this study. The interclavicle has a long and slender stem, which is partly obscured by several ribs and the scapula. The left clavicle is a curved bone, and is disarticulated from but closely associated with the interclavicle. The right clavicle is also partly exposed in close association with the right scapula. The left scapula is well exposed in association with the interclavicle and the coracoid. The scapular blade is narrow and tapering. The coracoid is a roughly rounded plate. The coracoid foramen is located close to the anterior border of the coracoid plate as shown in several other specimens of the same species. The left humerus is completely preserved in BMNHC V050. The humerus is slightly sigmoid with widened proximal and distal ends, but the shaft is greatly constricted. The left humerus is exposed in dorsal view. A small groove is observable close to the anterior border of the distal part of the bone, though an ectepicondylar foramen cannot be identified. In BMNHC V014 the well-preserved left humerus clearly preserves a well-defined ectepicondylar Fig. 15 Photograph and line drawing of BMNHC V050, showing pelvis foramen. The right humerus of BMNHC V050 is completely and hind limbs of Hyphalosaurus baitaigouensis. preserved, but the distal part of the forelimb has been added artificially from a different specimen. The distal part of the left forelimb is authentic, and the ulna is surface of the ulnare. The centrale and distal carpals 2, 3 slightly shorter than the radius. The radius exhibits slight and 4 are also ossified. Distal carpal 1 and 5 were appar- curvature. The proximal end of the ulna is thicker than the ently unossified or absent, at least at the ontogenetic distal end, but no olecranon process is present. Based on stage represented by PKUP V1056. Distal carpal 5 is present comparisons of specimens from a variety of size classes, in Monjurosuchus (Gao et al. 2000), but has not been there is a clear ontogenetic trend in reduction of the reported in neochoristoderes. A pisiform has been identi- epipodial length relative to propodial length as growth fied in Monjurosuchus, but is not present in an articulated progresses. In BMNHC V050, a smaller individual, the forelimb of the neochoristodere Ikechosaurus pijiagouensis humerus is approximately 150% the length of the ulna, (Liu, 2004). The third and the fourth metacarpals of H. whereas in the large individual LMPC R-00066 the baitaigouensis are equal in length and are the longest in humerus is about 170% the length of the ulna. comparison with other elements. The first metacarpal is At the distal end of the ulna in BMNHC V050, three ossified the shortest and most robust. The phalangeal formula of mesopodial elements are identified. The ossification of the manus is 2–3–4–4–3 based on multiple specimens. only three carpal elements indicates subadult status, as larger The ilium is best exposed in medial view on the right side of individuals show several additional elements. A slightly BMNHC V050 (Fig. 15). The iliac blade is roughly rectangular larger specimen (PKUP V1056) shows better ossification in with a blunt dorsal end, and meets the acetabular base at this part of the limb and includes seven carpal elements. an angle greater than 45°. The iliac neck is poorly defined. The ulna contacts three elements, which we identify as the The medial surface of the ilium is smooth and slightly pisiform, ulnare and intermedium based on position. The concave. The left ilium is well-exposed in lateral view in pisiform is suboval and positioned postaxially at the ulna/ the same specimen. This view indicates the lower part of the ulnare contact. The ulnare is a large square bone, capping ilium is expanded and concave, forming a large part of the distal end of the ulna. As preserved, the ulnare directly the acetabulum. The blade is slightly ridged for attachment contacts metacarpal V distally without intervention of a of pelvic muscles. The blade is nearly vertically oriented distal carpal. The intermedium is an elongate element that in examined specimens, differing from the horizontal contacts the ulna proximally and lies against the preaxial orientation in the type species H. lingyuanensis. The pubis

has a concave anterior border, and shares a sutural contact with the ischium posteriorly. The ischium is a roughly Paleoecology of the family Hyphalosauridae triangular plate, with a well-developed tubercle projecting The Hyphalosauridae exhibit extensive skeletal modifica- from the posterior border. This tubercle is similar to that tions that suggest they were the most exclusively aquatic seen in most neochoristoderes, but is sharply different choristoderes. One such modification is the great elongation from the spike-like process in monjurosuchids (Gao & Fox, of the neck. The number of cervical vertebrae in hyphalo- 2005; Gao & Li, 2007). saurids varies from at least 16 to 24, and the number of The hind limbs are well preserved on both sides in dorsal vertebrae varies from 16 to 19. Amongst other BMNHC V050. The femur is essentially straight, lacking clades of choristoderes, the presacral vertebral series significant sigmoid curvature. A large specimen (LMPC includes eight cervical vertebrae and 16 dorsal vertebrae R-00065), however, shows some sigmoid curvature of in the Monjurosuchidae (Gao et al. 2000; Gao & Fox, 2005; the femur. This feature is also ontogenetically variable in Gao & Li, 2007), eight cervical vertebrae and 16 dorsal M. splendens (Gao et al. 2000). The tibia is slightly stouter vertebrae in the neochoristodere Simoedosaurus lemoinei and slightly longer than the fibula. The fibula is a simple (Sigogneau-Russell, 1981), and nine cervical vertebrae and straight bone with an expanded distal end. The femur is 17 dorsal vertebrae in the neochoristodere Champsosaurus roughly 150% of the length of the tibia in BMNHC V050, (Champsosaurus ambulator: AMNH 981; C. gigas, Erickson, but large specimens (LPMC R-00065, R-00066) display 1972). Thus, the elongation of the neck of Hyphalosaurus different proportions, with the femur being approxi- appears to have been achieved through addition of cervical mately 165–170% of the length of the tibia. The hind foot vertebrae rather than incorporation of dorsal vertebrae into is completely preserved on both sides in BMNHC V050, the cervical series. The addition of dorsal vertebrae has also but a slightly larger specimen (PKUP V1056) is more occurred in H. baitaigouensis, with three additional vertebrae completely ossified. added to the reconstructed plesiomorphic count of 16. In the articulated tarsus of PKUP V1056, at least five The expanded pachyostotic ribs and gastralia of Hyphalo- discrete elements can be identified. The astragalus is the saurus would provide negative buoyancy and also restrict largest tarsal element and takes the shape of an irregular the flexion of the trunk. The appendicular skeleton is rel- hexagon in dorsal view. Proximally, this bone bears two atively unspecialized, but the tail is deepened throughout articular surfaces for the tibia and fibula. A non-articulatory most of its length by the high neural spines. Based on surface is directed medially. Two distal surfaces serve as these features, the most likely means of underwater pro- articulations with a moderate-sized element we identify as pulsion was undulation of the tail, with little involvement distal tarsal 4 and with the first metatarsal. The remaining of the limbs. The well-ossified carpus and tarsus suggest lateral surface is for the articulation with the calcaneum. that hyphalosaurids retained some capacity for terrestrial The calcaneum is the second largest element, and articulates locomotion, though the great elongation of the neck and with the fibula but not the tibia. It possesses a strong tail relative to the rest of the body would have made lateral projection and appears to be largely or completely movement on land cumbersome. Based on anatomical separated from the 5th metatarsal. The distal surfaces of details (including integument pattern) from a large the astragalus and calcaneum together form a smooth number of specimens, an accurate life reconstruction of concave articulation for distal tarsal 4. These three tarsal the animal can be presented (Fig. 16). elements are tightly articulated in PKUP V1056. Distal The super-abundance of hyphalosaurids throughout the tarsal 4 clearly articulates with the fourth and fifth Yixian Formation indicates that they played a particularly metatarsals. Adjacent to distal tarsal 4, a square element, important role in the aquatic food chain of the Early presumably distal tarsal 3, articulates with the 3rd Cretaceous ecosystem in the area. Our understanding of metacarpal. Distal tarsal 3 is clearly exposed on the left the jaw musculature of Hyphalosaurus remains poor due side of this specimen, but obscured on the right. At least to the two-dimensional preservation in available specimens. one small tarsal element is present medial to distal tarsal However, the simple peg-like dentition, small skull size, 3. The possibility that larger individuals had additional and greatly elongated neck suggest pursuit of small prey ossified tarsals remains, but in the largest specimens items. As in other choristoderes, both species of Hyphalo- examined in this study the tarsus is not as well preserved saurus have a flattened skull. A flattened skull has been as in PKUP V1056. associated with prey capture through a sideways strike in The pes is longer and more asymmetrical than the aquatic reptiles (Taylor, 1987). Peg-like teeth in both manus. Metatarsals III and IV are subequal in length as in upper and lower jaws seem to be designed for grasping the type species, and these significantly exceed metatarsals prey with a quick sweeping bite, as seen in the extant fish I, II and V in length. Digit IV is the longest, followed by the Lepisosteus. The small and pointed palatal teeth are not digit III, II, V and I. The claws are short and weakly curved, suited for crushing, but may have been employed in holding with poorly developed plantar tubercles. The digital formula small prey. The great range of neck orientation in arti- of the pes is 2–3–4–4–3, as in other choristoderes. culated skeletons includes animals with the head oriented

These associations provide only circumstantial evidence for a predator–prey relationship, but Hyphalosaurus likely consumed Lycoptera fish at least on occasion. Gut contents are preserved only in one specimen, LPMC R-00066. Small, disarticulated ribs are visible enclosed between the ribs and gastralia of this individual. This indicates Hyphalosaurus consumed vertebrate prey at least occasionally. It is uncertain whether the dearth of gut contents in other specimens reflects a diet composed mainly of soft-bodied prey or is due to gut contents being lost and/or remaining uncovered during preparation.

Acknowledgements

This study is primarily a collection-based research. For access to the fossil collections under their care, we thank Zhou Zhonghe and Zheng Fang (IVPP), Li Quanguo (Beijing Museum of Natural History of China), and Cheng Shaoli and Hou Lianhai (Shenyang Normal University). We thank Ji Shu’an for providing a quality photograph of a juvenile in the collections of the Geological Museum of China. The research was supported by the National Natural Science Foundation of China (NSFC grants #40532008 and 40772009). Ksepka’s travel was supported by the Carter Fund of the AMNH and an NSF/Palaeontological Society grant for travel to the 2006 IPC meeting in Beijing. We thank Mick Ellison for photography of IVPP V11075 and PKUP V1052, and thank Kristin Lamm for her skillful reconstruction of Hyphalosaurus lingyuanensis.

References

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