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. 2019 Jan 25;14(1):e0211069.
doi: 10.1371/journal.pone.0211069. eCollection 2019.

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

Jia Jia  1   2 , Jian-Ping Jiang  3 , Mei-Hua Zhang  3 , Ke-Qin Gao  1
Affiliations

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

Jia Jia et al. PLoS One. .

Abstract

Batrachuperus yenyuanensis, commonly known as Yenyuan Stream Salamander, is a hynobiid species inhabiting high-altitude (2440-4025 m above sea level) mountain stream and pond environments along the eastern fringe of the Qinghai-Tibetan Plateau in western Sichuan Province, China. Although the species has been known for almost 70 years since its initial discovery in 1950, a thorough osteological description has never been provided. Our study provides a detailed account of the bony anatomy of this species, based on micro computed tomography scanning of multiple specimens collected from the type locality Shuangertang at Bailinshan, Yanyuan County, and several other localities in Sichuan Province. Our revised species diagnosis utilizes both bony and soft anatomical features. Comparative study of the specimens from the type locality in Yanyuan area with those from the nearby Xichang and Mianning areas confirms that they all pertain to Batrachuperus yenyuanensis, thereby removing doubt on the occurrence of the species in the latter areas. With this confirmation, the distribution of the species is extended from the type locality northwards some 180 km to the Mianning area, on both the west and east sides of the Yalong River, which is a major tributary of the upper Yangtze River. This distribution pattern indicates that the biogeographic origin and historical evolution of the species are closely associated with the orogeny of the Hengduan Mountains and formation of the Yalong River. Given the basalmost position of Batrachuperus yenyuanensis in relation to other congeneric species based on molecular studies, however, early expansion of the species distribution by dispersal is expected following the origin of the genus in early-middle Miocene in western Sichuan Province. Thus, the species may well have achieved its current distribution in western Sichuan before the drastic uplift of the Qinghai-Tibetan Plateau in Pliocene.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Photographs of the upper and lower ponds showing the high-altitude mountain pond and stream environments inhabited by Batrachuperus yenyuanensis at the type locality Shuangertang, near Yanyuan, Liangshan Yi Autonomous Prefecture, Sichuan Province, Southwest China.
A, upper pond; B, lower pond (both looking to the west; photograph by J Jia).
Fig 2
Fig 2. Photographs of representative formaldehyde-preserved specimens of Batrachuperus yenyuanensis in dorsal view.
A, CIB 14308 from the type locality Shuangertang, Yanyuan County; B, CIB 14550 from Maoniudui, Dechang County; C, CIB 17005 from Shenguozhuang, Yuexi County; D, CIB 72599 from Tuowu, Mianning County.
Fig 3
Fig 3. Micro-CT rendered reconstruction of the skull of Batrachuperus yenyuanensis in dorsal view.
A, CIB 72599 from Tuowu, Mianning County; B, FMNH 49371, paratype specimen from the type locality Shuangertang, Yanyuan County; C, CIB 17308 from Shuangertang, Yanyuan County.
Fig 4
Fig 4. Micro-CT rendered reconstruction of the skull of Batrachuperus yenyuanensis in left lateral and occipital views.
A, D, CIB 72599 from Tuowu, Mianning County; B, E, FMNH 49371, paratype specimen from Shuangertang, Yanyuan County; C, F, CIB 17308 from Shuangertang, Yanyuan County.
Fig 5
Fig 5. Micro-CT rendered reconstruction of the skull of Batrachuperus yenyuanensis in palatal view.
A, CIB 72599 from Tuowu, Mianning County; B, FMNH 49371, paratype specimen from Shuangertang, Yanyuan County; C, CIB 17308 from Shuangertang, Yanyuan County.
Fig 6
Fig 6. Micro-CT rendered reconstruction of the mandible of Batrachuperus yenyuanensis.
A, right mandible in lateral view; B, right mandible in medial view; C, mandibular arch in dorsal view; D, mandibular arch in ventral view. FMNH 49371, paratype specimen, from Shuangertang, Yanyuan County.
Fig 7
Fig 7. Hyobranchial apparatus of Batrachuperus yenyuanensis in dorsal view.
A, CIB 201707YY04 (juvenile); B, CIB 201707YY09 (subadult); C, CIB 201707YY08 (adult). All three specimens from Shuangertang, Yanyuan County.
Fig 8
Fig 8. Micro-CT rendered reconstructions of the whole body skeleton of Batrachuperus yenyuanensis.
A, B, CIB 17308 in dorsal (A) and ventral (B) views; C, D, CIB 72599 in dorsal (C) and ventral (D) views. CIB 17308 from Shuangertang, Yanyuan County; CIB 72599 from Tuowu, Mianning County.
Fig 9
Fig 9. Micro-CT rendered reconstructions of the pectoral girdle and upper arm of Batrachuperus yenyuanensis.
Left scapulocoracoid of CIB 94631 (A, E), CIB 16999 (B, F), CIB 17308 (C, G), CIB 72599 (D, H) in lateral (upper row) and ventrolateral (middle row) views; left humerus of CIB 94631 (I, J), CIB 17308 (M, N), CIB 72599 (O, P) and right humerus of CIB 16999 (K, L) in lateral (left) and medial (right) views. CIB 16999 from Shenguozhuang, Yuexi County; CIB 17308 from Shuangertang, Yanyuan County; CIB 72599 from Tuowu, Mianning County; CIB 94631 from Xieka, Jiulong County.
Fig 10
Fig 10. Micro-CT rendered reconstructions of the forearm and manus of Batrachuperus yenyuanensis.
Left forearm and manus of CIB 94631(A), CIB 17313 (B), CIB 72596 (D) in lateral view; right forearm and manus of FMNH 49371 (C) and CIB 17308 (E) in dorsal and lateral views; right forearm and manus of CIB 17308 in ventral and medial views (F). FMNH 49371, CIB 17308 and CIB 17313 from Shuangertang, Yanyuan County; CIB 72596 from Tuowu, Mianning County; CIB 94631 from Xieka, Jiulong County.
Fig 11
Fig 11. Micro-CT rendered reconstructions of the pelvic girdle of Batrachuperus yenyuanensis in dorsal (left column), ventral (middle column) and left lateral (right column) views.
CIB 14514 (A–C), CIB 16999 (D–F), CIB 17302 (G–I), CIB 17307 (J–L) and CIB 72592 (M–O). Note partly ossified pubis in CIB 14514 (A–C), CIB 17302 (G–I), and CIB 72592 (M–O). CIB 14514 from Maoniudui, Dechang County; CIB 16999 from Shenguozhuang, Yuexi County; CIB 17302 and CIB 17307 from Shuangertang, Yanyuan County; CIB 72592 from Tuowu, Mianning County.
Fig 12
Fig 12. Micro-CT rendered reconstructions of the ypsiloid cartilage and femur of Batrachuperus yenyuanensis.
Ypsiloid cartilage in dorsal view in CIB 201707YY04 (A), CIB 201707YY08 (B), CIB 201707YY09 (C); right femur of CIB 14514 (D, E), CIB 16999 (F, G), CIB 17308 (H, I) and CIB 94632 (J, K) in dorsal (left) and ventral (right) views. CIB 14514 from Maoniudui, Dechang County; CIB 16999 from Shenguozhuang, Yuexi County; CIB 17308, 201707YY04, 201707YY08 and 201707YY09 from Shuangertang, Yanyuan County; CIB 94632 from Xieka, Jiulong County.
Fig 13
Fig 13. Micro-CT rendered reconstructions of the lower hindlimb and pes of Batrachuperus yenyuanensis.
Left lower hindlimb of CIB 17309 (A), CIB 17313 (B), FMNH 49371 (C) and CIB 72597 (E); right lower hindlimb of CIB 14514 (D) and FMNH 49371 (F). Note the preaxial elements (tibiale and/or element y) are delayed in ossification in CIB 17309 and CIB17313; the two centralia are fused in CIB 14514 but remain separated from each other in all other specimens; the postminimus is ossified in FMNH 49371, CIB 14514 and CIB 72597. CIB 14514 from Maoniudui, Dechang County; CIB 17309, 17313, and FMNH 49371 from Shuangertang, Yanyuan County; CIB 72597 from Tuowu, Mianning County.
Fig 14
Fig 14. Patterns of geographic distribution of Batrachuperus yenyuanensis in western Sichuan Province of China.
Note that localities (solid dots) are spread on both the west and east side of the Yalong River (see S1 Table for altitude information of the localities). Small circles denote county towns and large circles denote city towns in the study area.
See this image and copyright information in PMC

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