Osteology ofBatrachuperus londongensis(Urodela, Hynobiidae): study of bony anatomy of a facultatively neotenic salamander from Mount Emei, Sichuan Province, China

Abstract

The Longdong Stream Salamander Batrachuperus londongensis, living in a mountain stream environment at Mt. Emei in Sichuan Province, China, represents a rare species that is facultatively neotenic in the family Hynobiidae. Although the species has been known to science for some 40 years since its initial discovery in the late 1970s, anatomical details of its osteology remain poorly understood and developmental information is still lacking for the species. This study (1) provides a detailed osteological account of B. londongensis based on micro-CT scanning and clearing and staining of multiple specimens from the type locality; (2) provides a discussion of intraspecific variation related to life-history differences; and (3) presents a discussion on limb features related to morphological evolution of limb patterns correlative with ecological adaptation to mountain stream environments. Osteological comparisons with congeneric species has led to recognition of several diagnostic features that are unique to B. londongensis, including: vomers widely separated from one another, lacking a midline contact; presence of uncommon perichondral ossification of the ascending process of the palatoquadrate as part of the suspensorium; and presence of a prominent posterodorsal process of the scapular blade, which serves as a ligamentous insertion of the levator muscle of the scapula. In addition, some but not all neotenic individuals retain the palatine as a discrete element, indicative of its delayed absorption after sexual maturity. Postmetamorphic and neotenic individuals are strikingly different in the complexity of hyobranchial structures. Neotenes display a high degree of ossification of hyobranchial elements, tend to increase ossification of both hypobranchial I and ceratobranchial I during aging, and retain fully ossified ceratobranchial III and IV; in contrast, these elements remain entirely cartilaginous or are totally lost by resorption in postmetamorphic individuals. In addition, all postmetamorphic forms display an inverted “T”-shaped basibranchial II, whereas neotenes show transformation from a “fork”-shaped to the “T”-shaped configuration after sexual maturity. B. londongensis displays a mosaic of apomorphic and plesiomorphic states in its limb ossifications: presence of a single centrale element in both the manus and pes is a derived condition in Hynobiidae and other families as well, whereas retention of a postminimus in the pes is obviously plesiomorphic within Urodela. Reduction in number of digits from five to four in the pes and possession of a cornified sheath covering the terminal phalanges are also derived features shared with some but not all mountain stream salamanders that are adapted to a similar type of environment.

Osteology of Batrachuperus yenyuanensis (Urodela, Hynobiidae), a high-altitude mountain stream salamander from western China

“…The tooth rows, widely separated from one another, are located medial to the choanae, posterior to the mid-length of the vomerine plate. A similar pattern is commonly seen in other congeneric species, except for Batrachuperus londongensis , in which the tooth row is basically straight and extends antero-posteriorly in its orientation [26].…”

“…Dorsally, at the posterior border of the orbit, the parietal swings laterally to form a small triangular process that slightly curves downward to contact the prootic. This process is perforated by a small foramen for passage of the nervus trochlearis (CN IV), as has been identified in other salamanders [24–26]. Posterior to this process, the parietal table widens laterally to form a boot-like extension in articulation with the squamosal in fully grown adults (e.g., CIB 17308, 17310, 17313, 72599; Fig 3A–3C).…”

“…Dorsal to the otic process of the pterygoid, a pillar-like structure represents the perichondral ossification of the ascending process of the palatoquadrate [24] (but epipterygoid in reference [17]; metapterygoid in [36]) as seen in some other salamanders [24, 26]. This bony pillar can only be seen in those fully-grown adults (e.g., CIB 72599; Fig 4A; S2A and S2B Fig), whereas it is incompletely or not ossified at all in many adult or young adult specimens (e.g., CIB 17002, 17308, 72595; Fig 4B and 4C; S2C–S2F Fig).…”

“…The blunt distal end of the stylus is for a ligamentous connection (ligamentum squamoso-columellare in reference [37]) with the quadrate and/or squamosal. There is no trace of a stapedial foramen, in contrast to Batrachuperus londongensis , in which the foramen is present in some, but not all individuals [26]. No operculum, either bony or cartilaginous, is identified in any specimens of B .…”

Synchrotron microtomography applied to the volumetric analysis of internal structures of Thoropa miliaris tadpoles

“…Since the introduction of microtomography (micro-CT) as a tool for anatomical investigations of vertebrates, several studies have used the reconstructed images as a way to present morphological information and to perform comparative studies based on them 1 – 4 . Recent studies have focused on adult morphology and on descriptive aspects of biology of several species of living fishes 5 – 7 , salamanders 8 – 10 , caecilians 11 – 14 , frogs and toads 15 – 19 , lizards 20 – 22 , snakes 23 – 25 , amphisbaenians 26 – 28 , turtles 29 – 31 , crocodiles 32 – 34 , birds 35 – 37 , and mammals 38 – 40 , besides fossils of several vertebrate groups 41 , 42 . On herpetological research, studies that encompass developmental series, together with other purely anatomical studies, represents the most of works reported this way, mainly for anurans and squamates species 43 .…”