INTRODUCTION

The Chinese crocodile lizard, Shinisaurus crocodilurus Ahl, is an enigmatic anguimorph lizard that today is known only to inhabit portions of southeastern China and northeastern Vietnam. In this paper, we expand on the relatively limited history of anatomical investigations on S. crocodilurus by providing the first detailed description of the braincase, cephalic osteoderms, and inner ear cavities. These descriptions largely are based on digital data derived from X-ray computed tomography, a nondestructive technique well suited for studying such rare and scientifically important specimens.

Shinisaurus crocodilurus is a relatively small-bodied (up to 397 mm body length) anguimorph lizard that occupies mountain stream habitats characterized by humid climate with annual rainfall up to 2 m (Shen and Li 1982, 1987). In China, S. crocodilurus was found between 200 and 1,500 m elevation (Zhao and Adler 1993; Zhao et al. 1999) in Guangxi Province between 23º25’ to 24º45’ N latitude and 110º48’ to 110º00’ E longitude (Zhao et al. 1999). Until recently, the species was thought to be restricted to this limited area of southeastern China. A newly discovered population in Quang Ninh Province of northeastern Vietnam was reported by Quyet and Ziegler (2003). Specimens from that new population were collected between 600 and 800 m elevation in habitats along stream banks, but no natural history data are available.

The species is ovoviviparous (Shen and Li 1982, 1987; Zhang and Tang 1985; Mägdefrau 1987; Zhao et al. 1999), and breeds in July and August in the wild (Zhang and Tang 1985; Zhang 1991) but at different times in captivity (Hofmann 2000). Individuals are largely diurnal, but generally do not engage in intensive activity (Zhao et al. 1999), spending long hours perched on rocks or branches above slow-moving streams and ponds (Zhao et al. 1999; Hofmann 2000). Relatively long periods of absolute immobility are apparently not uncommon in captivity (Sprackland 1989, 1995), and similar behavior in the wild earned the lizards the local common name “large sleeping serpent” (Zhao et al. 1999). When disturbed, individuals retreat to water for escape (Fan 1931; Quyet and Ziegler 2003); adults were observed to remain submerged for 10 to 20 minutes in the wild (Zhao et al. 1999; Quyet and Ziegler 2003), and in one case a captive lizard stayed underwater for six hours (Sprackland 1995).

Foraging activity in the wild is concentrated in early morning and in the evening. Diet in the wild includes dragonflies, aquatic beetle larvae, lepidopteran larvae, aquatic insects, grasshoppers, small fish, tadpoles, and grass seeds (Fan 1931; Shen and Li 1982, 1987) and possibly worms, rice borers, cockroaches, and small, metamorphosed anurans (Zhao et al. 1999). Individuals congregate in winter months and hibernate in rock crevices or tree holes from late October through late March (Zeng and Zhang 2002).

The relatively rugged terrain inhabited by S. crocodilurus in China and Vietnam provides some measure of protection for populations, but also restricts enforcement of conservation laws. Specimens of S. crocodilurus were exported for the pet trade in Europe and the United States in great numbers in the mid 1980s (Mägdefrau 1987; Sprackland 1989). The species was listed in CITES Appendix II in January 1990 and now receives full State protection in several areas of China (Zhao et al. 1999). Habitat destruction and human predation reduced known Chinese population sizes to an estimated 3,000 individuals by 1999 (Zhao et al. 1999) with some populations reduced to fewer than 20 individuals (Zhang and Zeng 2002). Illegal logging threatens the newly discovered Vietnamese population (Quyet and Ziegler 2003).

Fortunately, many individuals who obtained imported specimens established captive breeding programs and produced several publications detailing various aspects of general biology and behavior, including: 1) courtship; 2) copulation; 3) gestation period; 4) thermal preferences; 5) agonistic behavior; 6) sexual dimorphism; 7) ontogenetic variation; and 8) variation in coloration (e.g., Wilke 1985, 1987; Mägdefrau 1987, 1997; Sprackland 1989, 1993, 1995; Gritis 1990; Thatcher 1990; Kudrjawtsew and Wasiljew 1991; Grychta 1993; Kudryavtsev and Vassilyev 1998; Hofmann 2000).

The Anatomy of Shinisaurus

For more than two decades following its original description in 1930, virtually nothing was known about the anatomy of S. crocodilurus. General descriptions of external scale counts and variation in coloration were provided by Fan (1931) and were accompanied by photographs of the ventral surface of the body, a lateral view of the anterior torso and head, and a lateral view of the tail. The first major anatomical contribution was that of McDowell and Bogert (1954). Their discussion centered on osteology (with additional comments on the tongue) but was based upon dissection of a single, skeletally immature specimen in the American Museum of Natural History (AMNH 44928). That same specimen served as the basis for the first description of masticatory muscles (Haas 1960; followed by subsequent papers detailing additional observations by Haas 1973 and Rieppel 1980) and the eye (Underwood 1957, 1970). Subsequent papers addressed the vertebral column (Hecht and Costelli 1969), appendicular skeleton (Costelli and Hecht 1971), myology (Rieppel 1980; Huang 1992), brain and both cranial and spinal nerves (Hu 1980), liver and kidney enzymes (Zhao et al. 1980), digestive and urogenital systems (Zhang 1982), hemipenial morphology (Zhang 1986; Böhme 1988; Ziegler and Böhme 1997), optic nerve (Li and Wu 1988), microscopic anatomy of scales (Harvey 1993), karyotype (Zhang et al. 1996; Zhao et al. 1999), cellular ultrastructure (Zhang et al. 1996), mitochondrial DNA sequence (Macey et al. 1999), and protein electrophoresis (Wei et al. 2000). An overview of the general anatomy of S. crocodilurus was provided by Zhang and Cao (1984a, 1984b) and a more detailed treatment by Zhang (1991); both of these works are in Chinese, but the latter provides a brief English summary.

In this paper, we focus on two anatomical systems of S. crocodilurus that have as yet received inadequate attention: the detailed morphology of the braincase and the cephalic osteodermal armor. Our discussion of the braincase is augmented by description of some aspects of the inner ear structure. When we first conceived this project, our intention was to provide a complete and detailed review of the cranial osteology of S. crocodilurus. This became unnecessary upon the recent publication of an excellent study by Jack Conrad (2004). That paper is by far the most complete contribution to the osteology of S. crocodilurus. Additional important works discussed and/or illustrated the skull (McDowell and Bogert 1954; Rieppel 1980; Wu and Huang 1986; Zhang 1991), dentition (McDowell and Bogert 1954; Wu and Huang 1986; Zhang 1991), hyoid (McDowell and Bogert 1954; Wu and Huang 1986; Zhang 1991), vertebral column (Wu and Huang 1986; Zhang 1991), pectoral girdle (McDowell and Bogert 1954; Costelli and Hecht 1971; Wu and Huang 1986; Zhang 1991), pelvic girdle (Costelli and Hecht 1971; Wu and Huang 1986; Zhang 1991), limb skeleton (Costelli and Hecht 1971), and scleral ossicles (Underwood 1957, 1970; Zhang 1991).

Fossil Record

There is no fossil record for S. crocodilurus, and Asian fossils potentially referable to Shinisauridae are few. Hemishinisaurus latifrons is known from a broken frontal and prefrontals and the fragmentary tip of a maxilla. These specimens were described and illustrated by Li (1991) who placed them in “Xenosauridae.” The anterior dentition in Li’s (1991, figure 2B) appears to have acrodont implantation, suggesting a more likely affinity with Acrodonta.

Disarticulated dentaries referred to Oxia karakalpakiensis from the Cretaceous of Uzbekistan were assigned to “Xenosauridae” by Nessov and Gao (1993), but in a subsequent detailed analysis Gao and Nessov (1998) recognized that definitive placement of these elements was problematic. Although Alifanov (2000) retained Oxia in “Shinisauridae,” its phylogenetic position is best considered uncertain (Gao and Norell 1998). Additional undescribed specimens from the Early Cretaceous Höövör locality in Mongolia were tentatively referred to Shinisauridae by Alifanov (2000).

The phylogenetic position of Carusia intermedia was uncertain for many years. It was initially considered to be of scincomorphan affinity (Borsuk-Bialynicka 1985, 1987; Gao and Hou 1996), a hypothesis maintained by Alifanov (2000). A possible relationship with Xenosauridae was acknowledged in the original description (Borsuk-Bialynicka 1985) and appears to have been accepted a few years later (Borsuk-Bialynicka 1991a, 1991b). The recovery of numerous well-preserved specimens of Carusia intermedia was reported by Gao and Norell (1998), and their phylogenetic analysis supports a clade (Carusioidea) that minimally includes Carusia (basal), Xenosaurus, and S. crocodilurus. The North American lizards Exostinus and Restes also are likely members of this clade (reviews of their fossil record and hypotheses of relationship were summarized by Gauthier [1982] and Gao and Norell [1998]).

More recently, an exquisitely preserved fossil from the Green River Formation in Wyoming (USA) was discovered. Preliminary notice and discussion of the specimen was provided by Conrad (2002) who indicated that its skeleton is remarkably similar to that of S. crocodilurus.