Remarkable Carapace Morphology of Nanhsiungchelys (Testudines: Nanhsiungchelyidae) Revealed by New Material from Ganzhou Basin, Jiangxi Province, China

Abstract

Two nanhsiungchelyid carapaces from the Upper Cretaceous of Ganzhou Basin, Jiangxi Province, Southern China, are reported and assigned to Nanhsiungchelys sp. The new material reveals an unusual carapace morphology that was either not or poorly preserved in previously known Nanhsiungchelys specimens, including differentiated neurals, alternating costals, significantly modified scutes with vertebrals 4–5 contacting each other at a point, reduced pleurals 2–4 and greatly expanded lateral and posterior marginals. The discovery extends the geographical distribution of Nanhsiungchelys to the Ganzhou Basin.

1. Introduction

Nanhsiungchelys Ye, 1966 (Testudines: Cryptodira: Trionychoidae: Nanhsiungchelyidae) is a large land turtle from the latest Cretaceous of Guangdong, Southern China [1]. Contrary to most nanhsiungchelyids in which the shell morphology is relatively well known (e.g., Basilemys spp. from the Late Cretaceous of North America and Jiangxichelys spp., Kharakhutulia kalandadzei and Zangerlia spp. from Asia [2,3,4,5,6,7,8]), the shell morphology of Nanhsiungchelys, especially that of the carapace, is poorly known. The genus Nanhsiungchelys includes two species; each species was established from a single specimen. The holotype of N. wuchingensis (IVPP V 3106) consists of a partial skeleton, including the skull, lower jaw, shell and some limb bones. The carapace of IVPP V 3106 is poorly preserved, lacking many details of the plates and scutes [1,9]. The second species, N. yangi, is based on a specimen consisting of a skull, lower jaw and the anterior end of the carapace and plastron; thus, a large part of the shell is unknown [10]. Two other nanhsiungchelyid specimens reported from the Nanxiong Basin [11,12] were later assigned to Nanhsiungchelys sp. [13] but remain undescribed. This incompleteness of the knowledge of the shell features of Nanhsiungchelys hinders our understanding of its morphology, phylogeny and evolution.

In this paper, we report on new material of Nanhsiungchelys from the Upper Cretaceous of Ganzhou Basin, Jiangxi Province, Southern China. The material consists of two carapaces. JXGZ(2012)-181 is a complete carapace from the Upper Cretaceous redbeds of Longling Town, Nankang District, Ganzhou City. This specimen was discovered together with a series of specimens of Jiangxichelys ganzhouensis (Nanhsiungchelyidae (see [7], for the geological setting)). GMNHF10008 is a carapace lacking the posterior end, also from the Upper Cretaceous of Ganzhou Basin but the exact location is unknown. The new material extends the geographical distributions of the genus and provides new insight on the morphology of the shell. The specimens described herein are housed in the Mineral Resources Administration of Ganzhou (JXGZ) and Ganzhou Museum (GMNHF), Jiangxi Province, China.

Institutional abbreviations: CUGW, China University of Geosciences (Wuhan); IVPP, Institute of Vertebrate Paleontology and Paleoanthropology; JXGZ, Mineral Resources Administration of Ganzhou; GMNHF, Ganzhou Museum; YLSNHM, Yingliang Stone Natural History Museum.

2. Systematic Palaeontology

Testudines Linnaeus, 1758

Cryptodira Cope, 1868

Trionychoidae Fitzinger, 1826

Nanhsiungchelyidae Ye, 1966

Nanhsiungchelys Ye, 1966

Nanhsiungchelys sp.

(Figure 1 and Figure 2)

2.1. Referred Material

JXGZ(2012)-181, a complete carapace from the Late Cretaceous redbeds of Longling Town, Nankang District, Ganzhou City, Jiangxi Province, China. GMNHF10008, a carapace from the Late Cretaceous of Ganzhou area; the exact location is unknown.

2.2. Description

JXGZ(2012)-181 (Figure 1) is a complete carapace, measuring about 87 cm in length (maximum length in a straight line) and 52 cm in width (at the widest point). The carapace is domed, with a rather flat top. It has a roughly elongate oval outline. The cervical emargination is huge, bordered by a pair of large processes. The process, complete on the left side but lacking the extremity on the right, is stick-like, with a rounded cross-section and extends anteriorly. In comparison, the process of Nanhsiungchelys wuchingensis is dorsoventrally flat. The lateral borders of the carapace are slightly convex and the posterior end is rounded. The whole surface of the carapace is covered with strong sculptures consisting of vermiculated ridges forming large cells.

The nuchal is large and trapezoidal, forming the central part of the deep cervical emargination. The neural series consists of at least seven large and wide neurals. All neurals are wider than they are long, with different shapes (as in Testudinidae). Neurals 1 and 2 are six-sided with short posterolateral sides, contacting costals 1–2 and 2–3, respectively. Neurals 3 and 5 are four-sided, contacting costals 3 and 5, respectively. Neurals 4 and 6 are eight-sided, contacting costals 3 to 5 and 5 to 7, respectively. Neural 7 is probably six-sided but its posterior suture is not discernible. The surface of the posterior part of the carapace has been restored, the suprapygals are not discernible. The pygal is rectangular in shape, vertical and longer than it is wide. There are eight pairs of costals. Costal 1 contacts peripherals 1 to 3. Costals 2 to 6 alternate, with the medial end shorter than the lateral end in costals 2, 4 and 6 and inversely in costals 3 and 5, with the medial end longer than the lateral end. The lateral and posterior peripherals are vertical. Peripheral 1 forms a large anterior process. Peripheral 2 is notably narrow. The height decreases from peripherals 3 to 6, then increases posteriorly.

The scute sulci are well imprinted. The cervical scute is short and wide, with a width about three times its length. There are five vertebral scutes, all wider than they are long. Vertebral 1 is roughly triangular with the lateral borders strongly convergent anteriorly, as in the holotype of N. wuchingensis (IVPP V 3106 [9]). It is narrower than the nuchal and its anterior end is narrower than the cervical scute. Vertebrals 2 and 3 are similar in shape and width. They are roughly hexagonal and much wider than vertebral 1, with parallel anterior and posterior margins and angled lateral borders. Vertebrals 4 and 5 have an unusual morphology among turtles. Vertebral 4 is roughly five-sided; its posterolateral borders are curved and converge posteriorly to meet each other. Vertebral 5 is likely triangular with anterolateral margins that converge anteriorly to meet each other, and vertebral 4. On the whole, vertebrals 4 and 5 meet each other at a point and form together X-shaped sulci, with a meeting point located on neural 7. There are four pleural scutes. Pleural 1 is large and wide. It extends onto the nuchal and peripherals 1 to 4. Inversely, pleurals 2 to 4 are unusually narrow, covering only the middle portion of the costals. As a result of the modification of vertebrals 4 and 5, pleural 4 extends onto neural 7, nearly meeting each other along the midline. Most marginal scutes are discernible. Marginals 1 to 4 are shorter than the corresponding peripherals. Marginal 1 covers the anterolateral process and sends a medial process to contact the cervical scute. Marginal 2 is trapezoidal, whereas marginal 3 appears to be triangular, with its medial border convergent towards the lower margin of the carapace. As the lower margin of the carapace is not visible, the morphology of marginal 4 cannot be determined. There is a strip-like scute anterior to marginal 5; it may be part of marginal 4 or an additional scute. Corresponding with the narrow pleurals 2–4, the lateral and posterior marginals from marginal 5 backward are unusually high, extending onto the lateral third of the costal plates. Posteriorly, marginal 12 is long and narrow, with its length almost twice its width.

GMNHF10008 (Figure 2) is an almost complete carapace, lacking the posterior end. It measures about 93 cm in length and 63 cm in width, with an estimated total length of about 105 cm, based on the proportion of JXGZ(2012)-181. The whole surface is covered with strong sculptures, similar to JXGZ(2012)-181 and Nanhsiungchelys spp. [1,9,10].

As in JXGZ(2012)-181, the carapace is elongated when seen from above, with convex lateral borders. However, it appears to be wider and lower than that of JXGZ(2012)-181. The cervical emargination is deep and bordered by a pair of anterolateral processes. The process is shorter than that of JXGZ(2012)-181, dorsoventrally flat and entirely formed by peripheral 1. The carapace margin exhibits a notch lateral to the process.

The nuchal is trapezoidal and is almost twice as wide as it is long. The complete series of seven neurals is present. The neurals are wide and differentiated, as in JXGZ(2012)-181. Neural 1 is six-sided, with short posterolateral sides contacting costals 1–2. Neurals 2–3 are four-sided, with convex lateral margins. Neural 4 is probably seven-sided but the sutures with surrounding plates are not all visible. It probably contacts costals 3–5 on the left but only costals 3–4 on the right. Neural 5 is five-sided and asymmetrical, contacting costal 5 on the left but costals 4–5 on the right. Neural 6 is six-sided, contacting costals 5–6. Neural 7 is eight-sided and narrows posteriorly, contacting costals 6–8. Posterior to neural 7 is a roughly tetragonal plate. It contacts costal 8 and is likely suprapygal 1 (see Section 4). Posterior to this plate is a large but incomplete suprapygal 2, lacking its posterior portion. As in JXGZ(2012)-181, there are eight pairs of costals. The intercostal sutures are not all discernible and are somewhat curved and irregular. The costals alternate slightly but less than in JXGZ(2012)-181. Peripheral 1 is longer than it is wide, forming the anterolateral process. Peripheral 2 is narrow, with a length about twice its width. The lateral peripherals from peripheral 3 backward are high, vertical and barely visible in dorsal view.

Most scute sulci are clearly imprinted. The cervical is wider than it is long, with its width twice its length. There are five wide vertebral scutes. The vertebrals increase in width from vertebral 1 to 3 then decrease to vertebral 4, with vertebral 3 being the widest. Vertebral 1 is trapezoidal and wider than it is long, with the lateral margins strongly convergent anteriorly. Its anterior end is wider than that of JXGZ(2012)-181 and is as wide as the cervical. Vertebrals 2–3 are roughly rectangular and wider than they are long, with convex lateral margins. The shapes of vertebrals 4 and 5 are similar to those of JXGZ(2012)-181. These two scutes meet one another at a point on neural 7, as in JXGZ(2012)-181. As in JXGZ(2012)-181, pleural 1 covers the posterior part of the nuchal and peripherals 1–4. Pleurals 2–3 are very narrow, whereas the width of pleural 4 is unknown because its lateral sulci are not discernible. As a consequence of the narrow pleural scutes, the marginals are high, extending to half the width of the costals, whereas the intermarginal sulci are mostly invisible.

3. Phylogenetic Analysis

A parsimony phylogenetic analysis was performed using TNT 1.5 software [14]. The data matrix used was updated from Ke et al. [15] and included 20 taxa and 58 characters (Supplementary Materials). Character 28 of Nanhsiungchelys wuchingensis was changed from 1 to 0. Five characters were added. These were Character 54 (differentiated neural series): (0) no (Jiangxichelys ganzhouensis), (1) yes (Nanhsiungchelys sp. (JXGZ(2012)-181)); Character 55 (alternating costals): (0) no (Jiangxichelys ganzhouensis), (1) yes (Nanhsiungchelys sp. (JXGZ(2012)-181)); Character 56 (narrow pleurals 2–4): (0) no (Jiangxichelys ganzhouensis), (1) yes (Nanhsiungchelys sp. (JXGZ(2012)-181)); Character 57 (marginal 5 and those more posterior height): (0) marginals lower than the corresponding peripherals (Jiangxichelys ganzhouensis), (1) marginals clearly higher than the corresponding peripherals (Nanhsiungchelys sp. (JXGZ(2012)-181)); and Character 58 (contact between fourth and fifth vertebral scutes): (0) along a line (Anomalochelys angulata); (1) at a point (Nanhsiungchelys sp. (JXGZ(2012)-181)). A total of 22 and 18 characters out of 58 could be coded for JXGZ(2012)-181 and GMNHF10008, respectively. The analysis was conducted using a traditional search with 1000 replicates. A tree bisection reconnection (TBR) swapping algorithm was employed and 10 trees were saved per replicate. All characters were treated as unordered and of equal weight. Standard bootstrap support values were calculated using a traditional search with 1000 replicates. Bremer support values were also calculated [16].

The phylogenetic analysis retrieved a single tree with a length of 97 steps, a consistency index (CI) of 0.629 and a retention index (RI) of 0.681 (Figure 3). The tree recovered that JXGZ(2012)-181, GMNHF10008, Nanhsiungchelys wuchingensis and Nanhsiungchelys yangi formed a monophyletic group, with six unambiguous synapomorphies identified. These were Character 28 (sulcus between pleural 1 and marginals 2-3 clearly situated on peripherals); Character 29 (sulcus between pleural 3 and marginals 7-9 clearly situated on costals); Character 52 (first peripheral significantly enlarged to form the anterolateral process); Character 54 (differentiated neural series); Character 56 (narrow pleurals 2–4); and Character 57 (marginal 5 and those more posterior clearly higher than the corresponding peripherals). Nanhsiungchelys spp. and Xianyuechelys yingliangi also formed a clade, which was supported by three unambiguous synapomorphies. These were Character 53 (the length of the first costal was nearly equal to that of the second costal); Character 55 (alternating costals present); and Character 58 (the fourth and fifth vertebral scutes contacted at a point). Unlike the result of Ke et al. [15], our phylogenetic results placed Anomalochelys angulata at the basalmost position in the Anomalochelys (Xianyuechelys +Nanhsiungchelys) clade, suggesting that the anterolateral processes of the carapace are not homologous in Anomalochelys and Nanhsiungchelys.

4. Discussion

4.1. Taxonomy

The carapace surfaces of both the JXGZ(2012)-181 and GMNHF10008 are covered with a strong ornamentation of large cells formed by a network of vermiculated ridges, characteristic of the family Nanhsiungchelyidae [17]. Although some differences can be observed between JXGZ(2012)-181 and GMNHF10008 (such as the anterolateral processes (stick-like in JXGZ(2012)-181; flat in GMNHF10008), excavation depth of the anterior margin of the nuchal, details of neural differentiation and strength of costal alternating), both specimens exhibit characters of the genus Nanhsiungchelys, including a pair of large anterolateral processes formed by peripheral 1, a roughly triangular vertebral 1, wide neurals and wider than long vertebrals 2–3 [9]. In most nanhsiungchelyids, the anterolateral processes are absent, the neurals and vertebrals are narrow and vertebral 1 is trapezoidal or tetragonal with roughly parallel lateral margins (e.g., Hanbogdemys orientalis, Jiangxichelys spp. and Zangerlia testudinimorpha [4,6,7,17] as well as Basilemys spp. [2,8]). Anomalochelys angulata, a close relative of Nanhsiungchelys from the Cenomanian of Japan differs in the anterolateral processes formed by the nuchal, narrower and regular neurals and square vertebrals 2–3 [18].

Erected by Ye in 1966, the genus Nanhsiungchelys remained monospecific for a long time [1,9]. An additional species, Nanhsiungchelys yangi, reported recently, is distinct from N. wuchingensis, mainly by the skull characters because only the anterior end of the shell is preserved [10].

The carapace of N. wuchingensis (IVPP V 3106) was deformed by crushing and has been restored. Only neurals 1–4 are preserved in the neural series and most of them are incomplete and deformed, showing no clear differentiation in shape, with a neural formula of 6 < 4 > 6 > 6. The nuchal is relatively narrow and the cervical scute is small and as wide as it is long. Costal 1 is unusually short and costal 2 is slightly shorter medially than laterally [9]. Compared with IVPP V 3106, both JXGZ(2012)-181 and GMNHF10008 have a wider nuchal plate and a wider cervical scute. GMNHF10008 more resembles IVPP V 3106 in the dorsoventrally flattened anterolateral processes; the anterior end of vertebral 1 is as wide as the cervical scute and a less-excavated anterior margin of the nuchal. whereas JXGZ(2012)-181 has stick-like anterolateral processes; the anterior border of vertebral 1 is narrower than the cervical and deeply excavated anterior margin of the nuchal. The morphology of vertebrals 4–5 and the pleurals in IVPP V 3106 is unknown. The detailed comparisons of the carapace features of the new material with known Nanhsiungchelys spp. and Xianyuechelys yingliangi are shown in

Table 1. Comparison between new material, Nanhsiungchelys spp. and Xianyuechelys yingliangi (* estimated).

	N. sp. (JXGZ(2012)-181)	N. sp. (GMNHF10008)	N. wuchingensis (IVPP V 3106)	N. yangi (CUGW VH108)	Xianyuechelys yingliangi (YLSNHM01577)
Carapace length (cm)	87	105 *	115 *	55.5 *	32
Cervical emargination	Deep	Shallower	Deep	Deep	Deep
Anterolateral processes	Stick-like	Flat	Flat	Flat	Absent
Nuchal width 1 versus vertebral 1 width 2	1 > 2	1 = 2	1 = 2	?	1 = 2
Nuchal width (nuchal width/carapace width at level of maximum nuchal width)	Wide (59%)	Wide (52%)	Narrower (30%)	Wide (55% estimate)	Wide (52%)
Neural formula	6 < 6 < 4-8-4- 8 > 6	6 < 6 < 4-7-5 > 6 > 6	6 < 4 > 6 > 6	?	6 < 6 < 4 > 6 > 6-(4)-6<
Anterior margin of nuchal	Deeply excavated	Moderately excavated	Slightly excavated	?	Deeply excavated
Cervical scute	Wide; width three times its length	Wide; width twice its length	Square	?	?
Vertebral 1	Roughly triangular	Roughly triangular	Roughly triangular	?	Roughly square
Vertebrals 4–5	Meeting at a point on neural 7	Meeting at a point on neural 7	?	?	Meeting at a point on neural 7
Pleurals 2–3	Narrow	Narrow	?	?	Wide
Marginals	Lateral and posterior marginals (5–12) high	Similar to JXGZ(2012)-181	?	?	Lateral and posterior marginals low

. As the shell of N. yangi is poorly known, we assigned JXGZ(2012)-181 and GMNHF10008 to Nanhsiungchelys sp., pending the discovery of more complete material with an associated skull and shell.

4.2. Unusual Carapace Morphology of Nanhsiungchelys

The new material reveals an unusual carapace morphology that was previously unknown or poorly preserved in Nanhsiungchelys specimens. In JXGZ(2012)-181 and GMNHF10008, the neural series is differentiated and the costals alternate, as seen in testudinids [19,20,21]. Alternating costals are also present in the nanhsiungchelyid Xianyuechelys yingliangi [15]. In Nanhsiungchelys wuchingensis (IVPP V 3106), it seems that there is no clear neural differentiation for neurals 1–4 but alternating costals are apparent. Another notable feature is the posterior neurals/suprapygals. JXGZ(2012)-181 has seven preserved neurals but the posterior part of the carapace is damaged. In GMNHF10008, there is no interruption in the midline row of plates on the carapace (nuchal, neural series and suprapygals) but only seven neurals are present. Posterior to neural 7, there is a smaller tetragonal plate. We interpret this plate to be suprapygal 1 from a comparison with other nanhsiungchelyids (e.g., Basilemys spp. and Hanbogdemys orientalis [2,17]) because it is located between the posterior part of costal 8 and is not in contact with costal 7. This plate is followed by a large and triangular suprapygal 2 (incomplete). Neural 8 is likely fused with neural 7; the plate is in contact with costals 6 to 8. It is worth noting that Xianyuechelys yingliangi, a newly described sister taxon of Nanhsiungchelys, also has a continuous neural series that reaches the suprapygal but only has seven neurals [15]. However, neural 8 in Xianyuechelys is likely fused with suprapygal 1 because the plate between neural 7 and suprapygal 2 contacts costals 6 to 8. The reduction in the number of neurals in the Nanhsiungchelys–Xianyuechelys clade by fusion is unusual. It is in contrast to many other turtles with a reduced neural series that does not reach the suprapygal but where the right and left posterior costals meet each other along the midline, such as in Adocus spp. [22,23,24].

The most remarkable feature is the greatly modified scute pattern on the carapace. Vertebrals 4–5 contact each other at a point in JXGZ(2012)-181 and GMNHF10008 instead of along a line, as in most turtles. This character is shared only with Xianyuechelys yingliangi [15] and not known in any other nanhsiungchelyids. Even in its close relative Anomalochelys angulata, vertebral 4 has a long contact with vertebral 5 along a line [18]. Pleurals 2–4 are reduced in width and marginals 5–12 are greatly expanded in height and much higher than the corresponding peripherals, which is unique among nanhsiungchelyids but reminiscent of some Adocus species (e.g., A. atmgai and A. aksary [22,23]). In other nanhsiungchelyids, the marginals are shorter than the corresponding peripherals, except marginals 11–12 in all Basilemys spp. [2,5,8] as well as in Jiangxichelys spp. [6,7] and Zangerlia zdaminchondi [4]. In Kharakhutulia kalandadzei, Hanbogdemys orientalis, Zangerlia testudinimorpha and Yuchelys nanyangensis, the pleuromarginal sulcus is close to or reaches the costoperipheral suture [3,4,17,25].

5. Conclusions

Two carapaces from the Upper Cretaceous of Ganzhou Basin are described and assigned to Nanhsiungchelys sp. on the basis of diagnostic features of the genus (a pair of large anterolateral processes formed by peripherals 1, a roughly triangular vertebral 1 with anteriorly convergent lateral margins, wide neurals and wider than long vertebrals 2–3). The new material reveals characters of the carapace that were previously unknown in described Nanhsiungchelys taxa due to the incompleteness of specimens (differentiation of neurals; alternating costals; significant modification of scutes, including vertebrals 4–5 contacting at a point; reduced pleurals 2–4; and greatly expanded lateral and posterior marginals). The specimens hitherto referred to Nanhsiungchelys showed different shapes of anterolateral processes and morphologies of the nuchal, as well as significant variations in the shape of neurals. More complete specimens with associated skulls and shells are needed to determine if these characters represent diagnostic features of distinct species, intraspecific variations or sexual dimorphism within a species.