The oldest record of Saurosphargiformes (Diapsida) from South China could fill an ecological gap in the Early Triassic biotic recovery

Materials

The new taxon is described from a single specimen (WGSC V 1701) in two parts housed at WGSC. The part specimen (WGSC V 1701-1) preserves the articulated trunk portion of the body, prepared in dorsal view, whereas the counterpart (WGSC V 1701-2) mainly shows skeletal impressions and some bone fragments posteriorly. This specimen was collected from the Lower Triassic Member II of the Jialingjiang Formation at Songshugou Quarry near Xuanjianzhen (Xuanjian Village), Nanzhang County, Hubei Province (Figs. 1A, 1D); WGSC V 1701 was found lower in the sequence than other layers that yield fossil marine reptiles at Songshugou Quarry (Fig. 1D).

Methods

We added WGSC V 1701 as a new operational taxonomic unit (OTU) to the cladistic matrix of Li et al. (2014) (Analysis 1) that focused on the phylogenetic relationships of Saurosphargidae to Sauropterygia and other diapsids, and to the matrix of Chen et al. (2014c) as modified most recently by Scheyer et al. (2017) used to assess the relationships of early Mesozoic marine tetrapods. Following Chen et al. (2014c), we run two analyses using this second matrix: (Analysis 2) incorporating all characters, and (Analysis 3) modifying marine-related characters to uncertainty (see Supplemental Information). We also added OTUs representing Hupehsuchia and Hanosaurus to the matrix of Li et al. (2014) and modified two characters (see Supplemental Information). These three analyses provide complementary results for detailed relationships of saurosphargids (Li et al., 2014) and for broader diapsid and marine tetrapod relationships using a recent data set (Chen et al., 2014c; Scheyer et al., 2017). All analyses were implemented using maximum parsimony in TNT version 1.5 (Goloboff & Catalano, 2016), and Bayesian inference in MrBayes version 3.2.7a (Ronquist et al., 2012) using gamma- and log-normal-distributed rates models (see Supplemental Material). Convergence of the analyses in MrBayes was checked using estimated sample size (ESS) >200 and plotting traces of the MCMC output in R version 4.1.0 (R Core Team, 2021) and package CODA version 0.19.4 (Plummer et al., 2006). Model comparison used a stepping-stone analysis implemented in MrBayes (Xie et al., 2011) and comparisons of Bayes factors (Kass & Raftery, 1995).

The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved, and the associated information viewed through any standard web browser, by appending the LSID to the prefix http://zoobank.org/. The LSID for this publication is: urn:lsid:zoobank.org:pub:2EF3BA4D-B401-4B86-88C9-9320466A1ACD. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central SCIE and CLOCKSS.

Saurosphargiformes tax. nov., new clade name

Phylogenetic definition: The maximum clade including Saurosphargis volzi von Huene, 1936, but excluding Placodus gigas Agassiz, 1839, Plesiosaurus dolichodeirus Conybeare, 1824, and Hupehsuchus nanchangensis Young & Dong, 1972. Abbreviated definition: max ∇ (Saurosphargis volzi von Huene, 1936) | ~ (Placodus gigas Agassiz, 1839 & Plesiosaurus dolichodeirus Conybeare, 1824 & Hupehsuchus nanchangensis Young & Dong, 1972).

Discussion: Diagnostic characters for this new clade are taken from the phylogenetic analyses presented below as well as comparing shared (non-phylogenetic) morphology with the diagnosis of Saurosphargidae presented by Li et al. (2014); this is amended below.

Diagnosis: Aquatic diapsids characterized by the following combination of characters: (1) low neural spine of dorsal vertebrae with table-like top; (2) presence of dorsal osteoderms; (3) transverse processes of dorsal vertebrae distinctly long; (4) anterior ribs developing facets for ossicles dorsally; (5) gastralia elongate and flattened; (6) lateralmost elements of gastral ribs broadened and contacting each other; (7) humerus not expanded at both ends.

Saurosphargidae Li et al., 2011

Phylogenetic definition: The minimum clade including Saurosphargis volzi von Huene, 1936, Largocephalosaurus polycarpon Cheng et al., 2012, and Sinosaurosphargis yunguiensis Li et al., 2011, and all its descendants. Abbreviated definition: min ∇ (Saurosphargis volzi von Huene, 1936 & Largocephalosaurus polycarpon Cheng et al., 2012 & Sinosaurosphargis yunguiensis Li et al., 2011).

Discussion: A phylogenetic definition for Saurosphargidae has not previously been set down; the name is based on inclusion of the type species Saurosphargis volzi (Li et al., 2011), and diagnosed based on Largocephalosaurus and Sinosaurosphargis (Li et al., 2014). We propose a minimum (node-based) clade definition matching the indications of Saurosphargidae in previous phylogenetic hypotheses, differentiating Middle Triassic Saurosphargidae from more plesiomorphic Saurosphargiformes. The diagnosis below is modified from Li et al. (2014) based on our phylogenetic analyses and comparing shared characters with the more inclusive Saurosphargiformes.

Diagnosis: Modified from Li et al. (2014): (1) dorsal ribs forming a closed basket; (2) presence of large dorsal osteoderms [modified]; (3) external naris retracted; (4) median elements of gastral ribs with a two-pronged lateral process on one side; (5) supratemporal extensively contacting quadrate shaft; (6) posterior margin of skull roof deeply emarginated; (7) jugal-squamosal contact; (8) presence of ectopterygoid; (9) presence of interpterygoid vacuity and open braincase-palatal articulation; (10) leaf-shaped tooth crown with convex labial surface and concave lingual surface; (11) tip of neural spines covered by osteoderms [modified]; (12) large interclavicle boomerang-like or atypical T-shaped, with a small and sharp posterior process; (13) nine carpals; (14) four tarsals; (15) pachyostosis of dorsal ribs [new]; (16) distal end of transverse process distinctly thickened [new]; (17) deltopectoral crest absent [new]; (18) median gastral rib element two-pronged with lateral process on one side [new].

Pomolispondylus biani gen. et. sp. nov.

LSID: zoobank.org:act:42A625CB-EE27-4432-8606-7DD0ADC760D4

Etymology: The generic name Pomolispondylus is from the Greek ‘πόμολα σπόνδυλο’ (pómola spóndylo) meaning ‘knobbly vertebra’, referencing the morphology of the neural spines; the specific name biani honors Bian He, a famous Chinese historical figure from the locality.

Holotype: Part and counterparts: WGSC V 1701-1 and V 1701-2 (Figs. 2, 3). When WGSC V 1701 was removed from the matrix the rock split into two parts along the fossil layer and some elements were broken. Most elements are present on the part specimen (WGSC V 1701-1; Fig. 2A), while four posterior dorsal and two sacral vertebrae are on the counterpart with impressions of the neural spines, ribs, and fore and hind limbs of the right side (WGSC V 1701-2; Fig. 2B). The length of WGSC V 1701-1 is 128.54 mm, and the counterpart WGSC V 1701-2 is 200.8 mm long.

Locality and Horizon: Member II of the Jialingjiang Formation, Spathian (Olenekian), Early Triassic; Songshugou Quarry, Xuanjianzhen, Nanzhang County, Hubei Province, China. The definition of the Jialingjiang Formation was revised and three members were recognized based on geological mapping in Nanzhang and Yuan’an counties recently (Yan et al., 2021). The NYF is found in the top layers of Member II in the Jialingjiang Formation (Fig. 1).

Diagnosis: Saurosphargiformes with the following unique combination of characters: at least 18 dorsal vertebrae, two sacral vertebrae; neural spine heavily rugose dorsally; vertebral centrum with parallel lateral surfaces; proximal end of dorsal ribs slightly pachyostotic; lateral margin of distal part of dorsal rib developing oval facet; dense, sheet-like gastralia, with four grouped elements corresponding to one centrum; a small ossicle attaching the distal end of the lateral element of gastralia; humerus curved more strongly than straight femur; medial margin of pubis rounded.

Size

As preserved the specimen WGSC V 1701 measures 200.8 mm on the counterpart specimen (WGSC V 1701-2), while the dorsal portion is around 150 mm long. This size is comparable to that of Keichousaurus yuananensis from the same formation (dorsal length 145 mm in IVPP V2799; Young, 1965), and to small Middle Triassic pachypleurosaurs like Dianopachysaurus dingi (Liu et al., 2011) and Dianmeisaurus gracilis (trunk length 98 mm in IVPP V 18630; Shang & Li, 2015). The humerus impression indicates that it was 31.5 mm in WGSC V 1701. This is notably smaller than the humerus of Lariosaurus sanxiaensis (58.02 mm in HFUT YZS-16-01; Li & Liu, 2020) and Hanosaurus hupehensis (by way of comparison: the femur is 43.2 mm in IVPP V3231; Young & Dong, 1972; Rieppel, 1998). WGSC V 1701 is also smaller than Hupehsuchia from the same locality: the smallest Eretmorhipis carrolldongi has a dorsal length 255 mm (IVPP V4070; Chen et al., 2015) and Eohupehsuchus brevicollis is incomplete at 236 mm (WGSC 26003; Chen et al., 2014b), up to Parahupehsuchus longus with a dorsal length of 500 mm (WGSC 26005; Chen et al., 2014a). Estimates of presacral length vary given the different morphological proportions of compared taxa, but suggest little more than 200 mm, and likely smaller than 329 mm (Table 1).

Ontogenetic assessment

Maturity of the specimen is determined from comparisons with closely related Sauropterygia and modern lepidosaurs and archosaurs. This is made problematic due to the focus on cranial determinants that aren’t preserved in the material described herein. However, we identified the following characters that support a mature determination: neural spines fused to the vertebral centrum (Klein, 2012; Griffin et al., 2021); ossified zygantrum-zygosphene articulation, long bone epiphyses, and ossified ulnare (Lin & Rieppel, 1998; Griffin et al., 2021); humerus as robust as the femur (Lin & Rieppel, 1998).

Centra & Ribs

In WGSC V1701-1, there are 11 dorsal centra preserved that are covered by the neural arches dorsally, and six centra in WGSC V1701-2, which are obscured by the gastralia and pelvic elements. Adding two impressions of anterior dorsal vertebrae gives a total of around 20 presacrals (Fig. 2). The vertebral centra are oblong in dorsal view with straight lateral faces to the centra, unlike the concave shape seen in later Sauropterygia (e.g., Dianmeisaurus (Shang, Li & Wu, 2017) and Keichousaurus (Lin & Rieppel, 1998)) and in Largocephalosaurus (Li et al., 2014). The anteriormost rib impression does not join to an impression of a vertebra, but more posterior elements are generally well articulated. The first rib impression is much shorter than the posterior neighboring impressions as in Largocephalosaurus (Fig. 2B; Li et al., 2014), suggesting that the first rib impression represents the last cervical rib. The shape and length of the second rib impression is like the posterior neighboring ones. The first partially preserved rib anteriorly and first completely preserved rib correspond to the second and third impressions, respectively. So, we interpret the partially preserved rib to be the first dorsal rib. Based on this interpretation, there are 18 dorsal and two sacral vertebrae present in both parts of the specimen; this is much fewer than in Largocephalosaurus (24 dorsal, two sacral centra; Li et al., 2014), Lariosaurus sanxiaensis (~26 dorsal; Li & Liu, 2020), and Anarosaurus (25 dorsals; Klein, 2012), but similar to the pachypleurosaurs Keichousaurus yuananensis (19–20 dorsals; Young, 1965) also from the Early Triassic, and Dianopachysaurus (19 dorsals, three sacrals; Liu et al., 2011), Diandongosaurus (18 dorsals, three sacrals; Sato et al., 2014), and Dianmeisaurus (18 dorsals, four sacrals; Shang & Li, 2015) from the Middle Triassic.

Dorsal Vertebrae

The transverse processes of the dorsal vertebrae are elongate: about twice the lateral width of the centrum (e.g., 9.06 vs 17.22 mm in the anteriormost preserved vertebra), or more than twice the width across the prezygapophyses (e.g., 8.71 vs 18.52 mm in the eighth preserved vertebra). These are longer than in Lariosaurus sanxiaensis (Li & Liu, 2020) and in later small pachypleurosaurs (e.g., Dianmeisaurus (Shang, Li & Wu, 2017), Diandongosaurus (Liu et al., 2015)), but shorter than in Saurosphargidae. Laterally the transverse processes narrow to a rhombus-like shape in dorsal view (Figs. 2B, 3A, 3B), rather than the more narrow, elongate forms that are found in Saurosphargis and Largocephalosaurus (Nosotti & Rieppel, 2003; Li et al., 2014). It appears to be rounded in cross section, but the specimen has been dorsoventrally compressed, so the original shape cannot be determined. The zygantrum-zygosphene articulation, as preserved, is present above and between the zygapophyses, as shown between dorsals four and five (Figs. 3A, 3B).

The neural spines of the new taxon are unusual. Each neural spine is very low (just exceeding the height of the neural arch; Figs. 2C, 3A, 3B, 4A), like in Lariosaurus sanxiaenesis, Keichousaurus yuananensis, and later pachypleurosaurs (Fig. 4D; Young, 1965; Shang, Li & Wu, 2017; Li & Liu, 2020), and does not extend dorsally as in Sinosaurosphargis (Fig. 4F; Li et al., 2011). The neural spine then expands horizontally near the neural arch, particularly anteroposteriorly (Figs. 3A, 3C, 4A), so that the neighboring two neural spines contact each other on their anterior and posterior margins (Figs. 2A, 3A, 3B). However, the neural spine differs from Lariosaurus sanxiaenesis, Keichousaurus yuananensis, Hanosaurus hupehensis, and pachypleurosaurs by quickly expanding posteriorly and becoming laterally broader towards its posterior (Figs. 2A, 3A, 3B, 4A, 4D, 4G; Young, 1965; Rieppel, 1998). Additionally, the size of the neural spines increases posteriorly along the vertebral column (Figs. 2A, 3A). The length/width ratios of neural spines 10 to 13 are 8.82/8.23, 8.68/7.27, 9.15/7.78, 9.32/7.62, respectively (Figs. 2A, 2C).

Each dorsal neural spine forms an elliptical table (Figs. 2C, 3A, 4A), as in Largocephalosaurus, Eusaurosphargis, Placodontoidea, and Eorhynchochelys (Nosotti & Rieppel, 2003; Li et al., 2014, 2018; Cheng et al., 2015; Scheyer et al., 2017). However, the surface of this table in the new taxon is slightly convex dorsally, with abundant tuber-like ornaments in the surface, whereas the dorsal neural spine in Largocephalosaurus, Eusaurosphargis, and Placodontoidea is flattened or slightly concave (Figs. 3A, 3B, 4A, 4C, 4E). The tubers in the center of the neural spine’s table are distinctly larger than the surrounding ones and sub-circular, while the surrounding tubers are elongated radially (Figs. 3A, 3B). In Largocephalosaurus, Eusaurosphargis, Placodontoidea, and Eorhynchochelys, the dorsal neural spines are covered by at least one layer of osteoderms. It is difficult to identify the shape in Sinosaurosphargis, because its body trunk is covered by small dense osteoderms (Li et al., 2011). However, there are no osteoderms preserved near the vertebral column in this specimen, indicating that the table of the neural spine was possibly covered by soft tissue.

Dorsal Ribs

The dorsal ribs are single-headed (shown at their contact with the lateral centra and on anterior broken surfaces of the part specimen), as in Lariosaurus sanxiaensis, Majiashanosaurus discocoracoideus, and Middle Triassic pachypleurosaurs (Jiang et al., 2014; Li & Liu, 2020; Liu et al., 2021), and apparently articulate with the vertebral centra ventral to the transverse process (Figs. 2A, 3A, 3B, 4A); however, compaction of the specimen has made the positions of the rib uneven. Proximally, the ribs are somewhat thickened for approximately one-quarter of their length and narrow only slightly to the rather stout, rounded distal end of the rib. In cross section, the ribs are rounded and sub-circular.

The anterodorsal margin of the rib develops a low crest near the distal end in each of dorsal ribs 1 to 15. The crest forms an elliptical facet that extends distally along the shaft of the rib with a flat, smoothed surface (Figs. 2A, 4B). This is different from Saurosphargis, Largocephalosaurus, and Eusaurosphargis in which the dorsal rib develops an uncinate process at the shoulder region (Fig. 4E; Nosotti & Rieppel, 2003; Li et al., 2014), however, no uncinate process is present in Sinosaurosphargis (Fig. 4F; Li et al., 2011). The distal rib in Lariosaurus sanxiaensis and Hanosaurus hupehensis distally narrow (Figs. 4D, 4G; Rieppel, 1998; Chen et al., 2016), but a small crest is seen in Eusaurosphargis and a larger uncinate process the placodont Paraplacodus (Rieppel, 2000; Klein & Sichelschmidt, 2014; Scheyer et al., 2017).

All dorsal ribs in the present specimen are more slender than other saurosphargiforms, so the inter-rib spacing is distinct to Pomolispondylus biani. The posterior two ribs present in the part specimen (WGSC V1701-1) orientated slightly anteriorly in their proximal region with a strong posterior curve strongly distally. Impressions of posterior three slender and short dorsal ribs are preserved to the right of the vertebral column with pointed distal ends (Fig. 2B). The 16^th dorsal rib curves posteromedially like the anterior ones. The distinctly short and slender last two dorsal ribs extend anterolaterally (Fig. 2B).

Sacral & Caudal Ribs

There are two impressions of sacral ribs in the counterpart that are almost equal in size and shape (Figs. 2B, 3C, 3D). The sacral rib is distinctly short, stout, and slightly expanded distally. There are three impressions of caudal ribs. The first caudal rib impression extends anterolaterally, with the tip close to the second sacral rib. The latter two caudal ribs are oriented laterally, with conical tips.

Gastralia & Osteoderms

Gastralia are present associated with the vertebrae and ribs between the posterior coracoid and the anterior pubis, packed densely and forming a ventral sheet covering the abdomen (Figs. 2A, 2B, 3, 4A, 4B). Most of the gastralia are covered by the vertebral column and dorsal ribs as preserved, however, several of the most posterior gastralia are visible on the counterpart specimen (WGSC V 1701-2; Fig. 2B) and parts of other gastralia can be seen between the ribs (Figs. 2A, 3, 4A, 4B). Each gastral row consists of five elements: one medial and two lateral on each side (named first lateral and lateralmost here).

The median gastral element is relatively broad and slightly bowed with the distal tips curving posteriorly; there is no anterior process as in Sinosaurosphargis and Largocephalosaurus (Li et al., 2011, 2014), which differs from Lariosaurus sanxiaensis and Hanosaurus hupehensis (Rieppel, 1998; Chen et al., 2016; Li & Liu, 2020). The distal tips of the medial element taper to a fine point that inserts between the immediately anterior row and the associated first lateral and lateralmost elements in the same row (Fig. 2A). Laterally the ramus extends to contact the first lateral and lateralmost elements, spreading across about one-half of the width of the trunk; the contact is close but appears to be a simple butt join. The first lateral element is the shortest and fits posterior to the medial and lateralmost elements, extending medially nearly to the trunk midline and laterally approximately ventral to the dorsal ribs. The lateralmost element is slender and straight, with an extensively tapered medial end but a blunt, rounded distal end. This configuration is similar to Saurosphargidae and Early Triassic Sauropterygia (Rieppel, 1998; Li et al., 2014).

The gastral series is very dense: medial elements contact neighboring medial elements anteroposteriorly along the trunk midline (Fig. 2B), while more distally they are inserted between the first lateral and lateralmost elements from the same gastral row and the row immediately anterior to it (Fig. 2A). The lateralmost elements are positioned closely between rows, but do not contact each other distally as they are separated by the first lateral element. Four rows of gastralia correspond to one dorsal vertebra.

A series of small, irregularly shaped bone plates are found lateral to each gastral row that we interpret as rudimentary osteoderms (Figs. 2A, 4B). These plates form two rows along the lateral part of the gastral basket. Some of the more prominent plates are spindle shaped, and the dorsal surface develops ridge-like protrusions along the long axis (Fig. 4B). In Sinosaurosphargis, a bony plate covers the entire torso, possibly including the lateral ribs (Fig. 4F; Li et al., 2011). In Largocephalosaurus, the distal ribs are not connected to the osteoderms (Fig. 4E; Li et al., 2014), but in Eusaurosphargis the lateral rib contact a larger teardrop-shaped osteoderm (Nosotti & Rieppel, 2003; Scheyer et al., 2017). Osteoderms have not been reported for Lariosaurus sanxiaensis, Hanosaurus hupehensis, and Keichousaurus yuananensis (Figs. 4D, 4G; Young, 1965; Rieppel, 1998; Chen et al., 2016). Eusaurosphargis has larger lateral osteoderms than in WGSC V 1701 with distinct processes forming a triangle- or T-shape (Scheyer et al., 2017), while the osteoderms in placodonts like Cyamodus are also more strongly developed (Pinna, 1992), although notably absent in the plesiomorphic Paraplacodus (Rieppel, 2000; Neenan, Klein & Scheyer, 2013).

Appendicular Skeleton

The posterior portions of the two coracoids can be seen between dorsal vertebra four and five on the part specimen (WGSC V1701-1) with a convex lateral margin (Figs. 2B, 3A, 3B), but no detail can be determined. Other appendicular elements including fragments of the possible left scapula, much of the right pubis, and fragments of the possible left ischium respectively, with their impressions, are preserved in the counterpart (WGSC V 1701-2: Fig. 2B). Only the proximal part of the left scapula is preserved in the counterpart specimen presenting the lateral process, if this is identified correctly based on its association with the humerus (Fig. 2B). The process, together with the responding impression, roughly shows the shape of the whole left scapula. The scapula impression is bow-like, with a slight angle at its mid-length where it is widest and narrows to a sharp distal terminus. This is similar in form to the scapula in dorsal view in Largocephalosaurus qianensis (Li et al., 2014), and broadly corresponds to Sauropterygia (e.g., Placodus, Paraplacodus, Cyamodus, Dianmeisaurus) and Eusaurosphargis (Pinna, 1980; Rieppel, 1995, 2000; Shang, Li & Wu, 2017; Scheyer et al., 2017).

The distal portion of the right pubis is lost, but the proximal portion is preserved in ventral view (Figs. 2A, 3C, 3D). The medial margin is strongly convex and covers around three vertebral centra. More distally the pubis narrows slightly (seen on the anterior margin). There is only a small fragment and subtle impression of the ischium, but it appears to be a short, bar-shaped element. Impressions of the humerus and femur are also present in the counterpart specimen. The humerus impression is somewhat more robust than the femur impression and has a posteriorly-directed curve (Fig. 2B), like other saurosphargiforms (Li et al., 2011, 2014) and Early Triassic Sauropterygia (Rieppel, 1998; Chen et al., 2016; Li & Liu, 2020), but little sign of a median constriction can be seen. However, the femur is straight and expands somewhat towards the proximal end, like in most Eosauropterygia and all Saurosphargiformes (Li et al., 2011, 2014; Jiang et al., 2014).