Osteology of Quasipaa Robertingeri (Anura: Dicroglossidae)
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Asian Herpetological Research 2016, 7(4): 242–250 ORIGINAL ARTICLE DOI: 10.16373/j.cnki.ahr.150067 Osteology of Quasipaa robertingeri (Anura: Dicroglossidae) Meihua ZHANG1, Xiaoping CHEN2 and Xiaohong CHEN1* 1 Department of Zoology, College of Life Sciences, Henan Normal University, Xinxiang 453007, Henan, China 2 School of Science and Technology, Jiaozuo Teachers College, Jiaozuo 454000, Henan, China Abstract The objectives of this study are to present a detailed and comprehensive description of the osteology of Quasipaa robertingeri (Anura: Dicroglossidae), to provide osteological evidence for taxonomy, and to explore the adaptive traits of Q. robertingeri. We comprehensively studied the osteology of 2 adult specimens (1 male 98A00351 and 1 female 98A0041) of Q. robertingeri using conventional methods. Our osteological examination of Q. robertingeri shows that 1) the nasals are large and connect with one another medially; 2) the sphenethmoid is completely covered by the nasals and the frontopatietals, and thus it is not exposed dorsally; 3) the vomerine teeth are well-developed; 4) the anterior parts of the diapophyses of the presacral II protrude forward in the male, the same observation was made in the presacrals II and III in the female; 5) the pectoral girdle is firmisternal; 6) the omosternum is fan-shaped posteriorly, and almost equal to the length of the mesosternum; 7) the xiphisternum is W-shaped with a deep incision posteriorly; 8) the humerus of the male is more developed in the crista ventralis, the crista medialis, and the crista lateralis; 9) the metacarpal II of the male presents with a nuptial tuber; and 10) the distal phalanges of the digits are anchor- shaped. Ultimately, the unique characteristics listed are most likely adaptations to the environment and amplexus of Q. robertingeri. Keywords Quasipaa robertingeri, osteological characteristics, sexual dimorphism, environment, adaptation 1. Introduction environments, such as fossorial, terrestrial, aquatic, and arboreal environments (Duellman and Trueb, 1986; Fei et Morphology is primarily comprised of the external al., 2009; Inger, 1967). Within the bounds of their unique morphology, interior morphology, genital structure, shape, morphological differences in the hyoid, larynx, embryology, and karyology (Xiong, 2008). Of sacrum, girdle, limb proportions, and terminal phalanges these morphological components, the osteological likely enabled anurans to navigate different surroundings characteristics of the interior morphology are (Duellman and Trueb, 1986; Jorgensen and Reilly, 2013; comparatively conservative, and are thus utilized Kent and Miller, 1997; Lynch,1969; Simons, 2008; frequently for the taxonomic diagnoses of species, Tihen,1965; Trueb, 1973). genera, and families, as well as for constructing Quasipaa robertingeri (Anura: Dicroglossidae) is phylogenetic relationships (Fei et al., 2009; Hoyos, 2015; endemic to China and inhabits mountainous streams and Lehr and Trueb, 2007; Trueb, 1973; Wei et al., 2009). surrounding riparian areas at elevations of 650–1500 Additionally, habitat environment and behaviors can be meters (Fei et al., 2012). To date, this species has been extrapolated through osteological features, which is of recorded in Hejiang County and Changning County, in great significance when the goal is to ascertain adaptive Sichuan Province (Fei et al., 2009), Wenxin County, evolution. in Yunnan Province (Li et al., 2009), and Chongqing In vertebrate evolution, anurans were one of the earliest City (Huang et al., 2010). Q. robertingeri is classified landing groups and were capable of inhabiting various as endangered because of its declining numbers (Wang * Corresponding authors: Prof. Xiaohong CHEN, from Henan Normal and Xie, 2009). Quasipaa was recognized as a distinct University, Xinxiang, Henan, China, with her research focusing on the subgenus and was subsequently elevated to the genus evolution of anurans. E-mail: [email protected] status mainly based on its external morphology, lacking Received: 13 November 2015 Accepted: 19 January 2016 adequate osteological date (Dubois, 1992, 2005). No. 4 Meihua ZHANG et al. Osteology of Quasipaa robertingeri 243 The objectives of this study are to present a detailed palatina of the maxillae, support the maxillary processes and comprehensive description of the osteology of of the nasals, and contribute to the anterior walls of the Q. robertingeri, to provide osteological evidence for orbits. The rear parts of the cartilages then embed into the taxonomy, and to explore the adaptive traits of this grooves of the anterior rami of the pterygoids. species. Septomaxillae: The septomaxillae are small and lodged in the bottom of the external nares between the nasals 2. Materials and Methods and the maxillae; they are not in contact with any bones. The inner border of the bone is arc-shaped with a medial We examined 2 adult specimens (1 male 98A00351 and projection. The posterior edge is triangular (Figure 2B, 1 female 98A0041) of Q. robertingeri in this study. Both C). of the specimens were collected from the type locality Sphenethmoid: The tubular sphenethmoid forms the in Hejiang County, Sichuan Province, China, during the anterolateral walls of the braincase. From the dorsal 1998 breeding season. The specimens were euthanized in view, the bone is completely hidden by the nasals and the the laboratory and fixed in 10% neutral buffered formalin. frontoparietals. The sphenethmoid is ventrally supported We dissected the frogs by hand using a dissecting by the cultriform process of the parasphenoid. The microscope. We documented the dissection process with posterior end of the bone bears an inverted U-shaped photographs taken using a digital microscope combined incision dorsally, and an inverted V-shaped incision with a Nikon D7100 camera. We used Photoshop CS5 ventrally (Figure 2D). to combine the photos into a single figure. We adopted Frontoparietals: The frontoparietals roof the braincase general osteological terminology from Trueb (1973), and are slightly wider posteriorly than anteriorly. They Duellman and Trueb (1986), and Fabrezi (1992). The articulate with the nasals anteriorly, and posteriorly with terminology we use for the hyoid and larynx follows the exoccipitals and the prootics (Figure 2E). Trewavas(1933). All of the osteological features we Prootics: The prootics are large, form the posterolateral discuss herein are based on the female Q. robertingeri walls of the braincase, and house the auditory capsules. specimen, unless we specify otherwise. The elements dorsomedially articulate with the frontoparietals and the exoccipitals. Laterally, they are 3. Results invested by the squamosals and the pterygoids (Figure 2F, G, H). The osteology is generally comprised of the axial skeleton Exoccipitals: The exoccipitals form the posteriormost and the appendicular skeleton. The axial skeleton includes parts of the braincase, and the posteromedial walls of the the skull, the vertebral column, and the sternum. The auditory capsules. Medially, the exoccipitals encircle the appendicular skeleton includes the girdles, and the limbs. foramen magnum. Posteriorly, the elements bear a pair of 3.1 Axial Skeleton occipital condyles and jugular foramen (Figure 2I, J). 3.1.1 Skull The skull of Q. robertingeri is arc-shaped Vomers: The vomers obliquely lie anterior to the anteriorly, and wider than its length (Figure 1A, B). palatines. The anterior process of the vomer is moderately Nasals: The nasals are large, funnel-shaped, and cover expanded and points anterolaterally. The prechoanal two-thirds of the nasal capsules dorsally. They articulate process is long, thin, orients laterally, and supports the with one another medially and reach the frontoparietals anterior end of the choana. The postchoanal process is posteriorly. The maxillary process of the nasal is long, broad, robust, slants posterolaterally, and supports the tapered, and extend laterally to the preorbital process of posterior end of the choana. The medial process of the the pars facialis of the maxilla. They contribute to the vomer is a roughly rectangular lamina. The dentigerous anterior margin of the orbit (Figure 2A). process bears approximately 7 vomerine teeth (Figure Nasal cartilages: The bodies of the nasal cartilages are 2K). situated between the premaxillae and the sphenethmoid, Parasphenoid: The sword-like parasphenoid supports and have 3 paired differentiated rami. Dorsally, the front the braincase ventrally. The anterior tip of the cultriform parts of the nasal cartilages extend anterolaterally and process is pointed, extends to the level of the anterior form the anterior wall of the nasal cavity. Ventrally, the margin of the orbit, and connects with the vomers and front margins of the cartilages extend 2 short club-shaped palatines. The alae orient laterally, perpendicular to the rami and attach to the alary processes of the premaxillae. cultriform process. The posteromedial process of the The rear parts of the cartilages extend laterally to the pars parasphenoid is short and invests the ventral surface of 244 Asian Herpetological Research Vol. 7 Figure 1 Osteology of Quasipaa robertingeri, specimen 98A0041, adult female. A: skull, dorsal view; B: skull, ventral view (abbreviations: alary p, alary process; col, columella; exoc, exoccipital; fpar, frontoparietal; jug f, jugular foramen; max, maxilla; nas, nasal; pal, palatine; oper, operculum; opt f, optic foramen; pmax, premaxilla; pro, prootic; prsph, parasphenoid; pter, pterygoid;