Data Paper Zone II Versions EN1 Vol 3 (2) 2018
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Dataset of μCT scan of the holotype specimen of Batrachuperus londongensis Liu and Tian, 1978, an endemic hynobiid (Amphibia, Urodela) from Mount Emei, Sichuan Province, China
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: 2018 - 03 - 01
: 2018 - 03 - 23
: 2018 - 06 - 22
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Abstract & Keywords
Abstract: As a primitive clade of tailed amphibians, hynobiids are significant in understanding the early evolutionary history of salamanders. However, no consensus has been reached in regard to the time and location of origin, the evolutionary history of certain characters, and the phylogenetic relationships of Hynobiidae, due to several factors including: scarce fossil records, insufficient morphological investigations of their living taxa, inconsistent results of molecular data-based cladistic analyses, and lack of morphology-based phylogenetic analyses. Batrachuperuslondongensis , living in the Longdong River area at Mount Emei, Sichuan Province, China, features as the single living hynobiid species that is facultatively neotenic. Despite the fact that the species has been known to scientific community for 40 years, its osteology has not been thoroughly investigated. This paper provides a technical procedure of employing high resolution CT scan (μCT) technique in investigating the osteology of the holotype (CIB 14380) of B.londongensis . μCT scan of the holotype specimen (CIB 14380) of B. londongensis was completed using the Quantum GX microCT Imaging System at Chengdu Institute of Biology, Chinese Academy of Sciences. The voxel size derived from these scans ranges between 67.1 – 144 μm. Several distinctive osteological traits characterizing the neotenic individuals of B. londongensis were revealed, such as their highly ossified hyobranchial apparatus and wholly ossified carpals and tarsals in the limb. This study represents the first attempt of applying μCT scanning techniques in the osteological research of living hynobiids endemic in China. The dataset includes μCT source data of the holotype and associated parameters; reconstructed images and videos displaying the cranial part and the whole skeleton; and a 3D pdf and 3D printable stl files for the cranial part of the holotype. The source data files created from the μCT scan display a clear outline of the skeleton and can be easily read by software, like VG Studio. This dataset benefits researchers and the public interested in the osteology of the facultatively neotenic B.londongensis , and is valuable for investigating the morphology of hynobiids endemic in China.
Keywords: μCT scan; Batrachuperus londongensis; Hynobiidae; Mount Emei; Sichuan Province; 3D pdf; 3D printing
Dataset Profile
Chinese title中国四川省龙洞山溪鲵正模标本(CIB 14380)高精度μCT扫描源数据集
English titleμCT source dataset of the holotype (CIB 14380) of Batrachuperus londongensis from Sichuan Province, China
Data authorsJia Jia, Zhang Meihua, Gao Keqin, Jiang Jianping
Data corresponding authorJia Jia (jia_jia@pku.edu.cn)
Time of collectionThe holotype of B. londongensis was collected on March 23, 1965.
Geographical scopeThe holotype of B. londongensis was found from Longdong River (N29°34′42.85″/E103°17′5.61″), at an elevation of 1300 m, Mount Emei, Sichuan Province, China.
CT scan resolutionEight sections of the holotype of B. londongensis were separately μCT scanned, and the resolution of the resulted images ranges between 90 – 144 μm. A higher resolution (67.1 μm) of the first section was achieved through the subvolume reconstruction option of the Quantum GX μCT Imaging System.
Data volume2.84 GB
Data format*.jpg, *.pdf, *.rmvb, *.stl, *.tif, *.xml
Data service system<http://www.sciencedb.cn/dataSet/handle/557>
Sources of fundingNational Natural Science Foundation of China (41702002, 41072007, 41272016); Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences (Nanjing Institute of Geology and Palaeontology) (2017KF03); The National Key Research and Development Program of China, Ministry of Science and Technology (2017YFC0505202)
Dataset compositionThis dataset consists of two subsets in total. The first subset comprises the source data generated from μCT scan of the eight sections of the holotype of B. londongensis, and the source data of the skull portion at a higher resolution produced through the subvolume reconstruction at the Quantum GX μCT Imaging System. The second subset comprises the photographs, 3D reconstructed images, and videos of the holotype, a 3D pdf and stl files for the cranium. The dataset consists of the following 12 documents: (1) skull90um.zip stores the μCT source data for the skull portion, including 512 tiff images and a text file skull90um.xml containing all scanning parameters, with a data volume of 256 MB; (2) skull67_1um.zip stores the μCT source data for the skull portion at a higher resolution achieved through the subvolume reconstruction function of the Quantum GX μCT Imaging System, including 512 tiff images, with a data volume of 256 MB; (3) forelimb120um.zip stores the μCT source data for the forelimb portion, including 512 tiff images and a text file forelimb120um.xml containing all scanning parameters, with a data volume of 256 MB; (4) trunk120um.zip is the μCT source data for the trunk portion, including 512 tiff images and a text file trunk120um.xml containing all scanning parameters, with a data volume of 256 MB; (5) hindlimb144um.zip is the μCT source data for the hindlimb portion, including 512 tiff images and a text file hindlimb144um.xml containing all scanning parameters, with a data volume of 256 MB; (6) tail_1_120um.zip stores the μCT source data for the anterior portion of the tail, including 512 tiff images and a text file tail_1_120um.xml containing all scanning parameters, with a data volume of 256 MB; (7) tail_2_120um.zip stores the μCT source data for the middle part of the tail, including 512 tiff images and a text file tail_2_120um.xml containing all scanning parameters, with a data volume of 256 MB; (8) tail_3_120um.zip stores the μCT source data for the posterior part of the tail, including 512 tiff images and a text file tail_3_120um.xml containing all scanning parameters, with a data volume of 256 MB; (9) tail_4_120um.zip stores the μCT source data for the tail tip, including 512 tiff images and a text file tail_4_120um.xml containing all scanning parameters, with a data volume of 256 MB; (10) pics.zip stores the photographs and 3D reconstructed images of the holotype, including two jpg and nine tiff files, with a data volume of 84.1 MB; (11) videos.zip stores the videos of the 3D reconstructed cranium and whole skeleton of the holotype in rmvb format, with a data volume of 38.5 MB; (12) pdf_stl.zip contains a 3D pdf file of the cranium and 3D printable stl files for each bone of the cranial portion of the holotype, with a data volume of 484 MB.
1.   Introduction
Salamanders, or tailed amphibians, are a group of small to moderate sized amphibians with well-developed limb and tail. As a primitive clade of living tetrapods, salamanders are more similar in morphology to the already extinct early amphibians (e.g., temnospondyls) than other living groups of lissamphibians, frogs, toads, and caecilians, and therefore bear high significance in understanding the water-to-land transition of vertebrates, and the origin and early evolution of tetrapods.1
Hynobiidae are a group of small salamanders (total body length ranges between 70 – 260 mm),2 including 67 – 68 species in 9 – 11 genera. The hynobiids distribute primarily in East Asia, with only few species dwelling in the Middle East (Paradactylodon) or European and Siberian Russia (Salamandrella).3–4 With well-developed external gill and tail fin, larvae of hynobiids live in water, whereas adults live either in water or on land with their external gill and tail fin resorbed during metamorphosis. The only exception is Batrachuperus londongensis: some individuals fail to metamorphose, but retain gill slits and live permanently in water as facultative neotenes.2 Hynobiidae have been widely accepted as a primitive clade of living salamanders due to their possession of multiple plesiomorphic features: external fertilization, high number of chromosomes (over 40), presence of microchromosomes, spinal nerves (except the first pair) passing through intervertebrally, and independent angular and prearticular bones in the lower jaw.5–7 Therefore, Hynobiidae are a critical group in investigating the origin of salamanders.
However, debates continue in regard to the time and location of their origin,8–12 the evolutionary history of certain characters,13–14 and the phylogenetic relationships of Hynobiidae.11,15–17 Hynobiidae was even claimed as a paraphyletic18 or polyphyletic14 group; and its monophyletic status had not been confirmed until recent cladistic analyses using molecular data.11,15 Factors of the above controversies include: First, scarce fossil records. To date, only five taxa have been found in the Cenozoic Era (from 66 million years ago to today), most of which are preserved as fragmentary and disarticulated vertebrae and limb elements, presenting few informative characters for cladistic analyses. Recently, six hynobiid-like fossil taxa were discovered from the strata of Middle Jurassic to Early Cretaceous (125 – 165 million years ago) at western Liaoning Province, northern Hebei Province, and Inner Mongolia of China, including: Laccotriton orientalis, Sinerpetonfengshanensis , Liaoxitritonzhongjiani , Liaoxitritondaohugouensis , Regalerpetonweichangensis and Nuominerpetonaquilonaris .19–20 Fossil specimens of these taxa are articulated and complete, providing valuable materials to explore the origin of salamanders. Unfortunately, relationships between most of these fossil taxa and living hynobiids remain obscure (see below), except that Liaoxitritonzhongjiani and Nuominerpetonaquilonaris were identified as stem hynobiids by recent studies;20–22 Second, insufficient morphological investigations of living hynobiids, particularly those derived species (such as B. londongensis) endemic in China, render it difficult to identify synapomorphies among hynobiids, a clade rife with plesiomorphic features. Third, inconsistent results of cladistic analyses using molecular data. With rapid development in sequencing techniques, a large volume of molecular data of living hynobiids is quickly accumulated at a low cost. Massive data of gene loci have been gathered, serving as informative phylogenetic signals to investigate the phylogenetic relationships of hynobiids. However, no consensus in this regard has been reached by cladistic studies based on mitochondrial DNA,11,23 nuclear DNA,17 or a combination of both molecular sources.15–16,24–25 Fourth, lack of morphology-based phylogenetic analyses. Previous studies have summarized morphological characters with taxonomic and phylogenetic signals,10,26–27 tentatively analyzed them following non-Hennig cladistic theories,28 and produced results greatly different from those of molecular studies.
Despite the already large, continually growing volume of molecular data as mentioned above, morphological characters remain indispensable in investigating the phylogeny of hynobiids. On the other hand, it is bony structures that are most likely to have been preserved in fossil specimens, albeit soft tissues are occasionally preserved as impressions under very limited conditions. Therefore, morphological characters, especially osteological features, are the only linkage between living and extinct species. Previously, clearing and double staining prevailed as the preferred research method in morphological studies of living hynobiids.29–31 By staining bones and cartilages into red and blue, respectively, outlines and boundaries of these bones are rendered clearly visible,32 but by doing so this method not only causes irretrievable damages to specimens but is also incapable of acquiring their three dimensional interior structures. By exploiting high energy X-ray, high-resolution X-ray tomography, or μCT scan, features as an efficient and nondestructive technique for obtaining three dimensional information of the specimens.
In view of the above-mentioned situation, we investigated the osteology of Batrachuperuslondongensis , a derived hynobiid inhabiting the Longdong River area of Mount Emei, Sichuan Province, China. By μCT scanning the skeleton of the holotype (CIB 14380), we were able to, for the first time, apply this technique in the osteological study of living hynobiids endemic in China. This study represents an outcome of a series of investigations on the osteology of living hynobiids.33 Among living hynobiids, Batrachuperus londongensis is unique in that its individuals exhibit two developmental modes of metamorphosed and facultative neotenes. Yet, in-depth osteological studies of B. londongensis are not available to date, though this species has been known to scientific community for 40 years.34 Our μCT scan of the holotype of B. londongensis reveals several special features in the skull, hyobranchial apparatus and appendicular skeleton of this taxon.
This dataset offers μCT scan data of the holotype specimen (CIB 14380) of B. londongensis, videos and images showing its three dimensional reconstruction, and a 3D pdf file and 3D printable stl files of the cranium of the holotype. These original raw data enable researchers to investigate the osteology of B. londongensis, and also provide the public with an access to the virtual model of B. londongensis.
2.   Data collection and processing
2.1   Specimen and data collection
2.1.1   Specimen collection
The holotype specimen of B. londongensis was collected on March 23, 1965 by Professor Liu Chengzhao and his colleagues in the vicinity of Linggongli scenic area of Mount Emei, Sichuan Province, China (N29°34′42.85″, E103°17′5.61″), at an altitude of 1300 m. This specimen had been kept in formalin solution at the holotype specimen room of Chengdu Institute of Biology, Chinese Academy of Sciences, under field catalogue No. CIB 65I0013 and archive catalogue No. CIB 14380. This is a male adult, with a total length of 265 mm, a snout-vent length (distance from snout tip to the posterior extremity of the anus) of 129 mm, a skull length (length between snout tip and the posterior extremity of occipital condyle) of 27.5 mm, and a skull width (maximum length between the cranial joints) of 23.8 mm. This individual is neotenic, as evidenced by the presence of gill slits on the posterolateral side of the cranium. We carefully took out this specimen from the formalin solution, and photographed it with a Canon EOS 5D camera (Figure 1).
2.1.2   Collection of μCT scan data
μCT scan of the holotype specimen of B. londongensis was conducted by using the Quantum GX microCT Imaging System (PerkinElmer®, Massachusetts, USA) at Chengdu Institute of Biology.
Before scanning, the specimen was carefully rolled into an elongated rod and was transferred into a resealable bag. It was fastened on the small bed of this scanner, with the long axis of the specimens paralleled with that of the bed. The voltage and current was set as 50 Kv and 60 μA, respectively. Adjust the parameters of acquisition and reconstruction in the field of view to obtain a maximal image of the specimen. In live mode, rotate the X-ray source generator by changing the rotation control parameters to ensure that all parts of the specimen fall within the scan field. Then, set the high resolution mode as 57 minutes and start the scan. In order to obtain high-resolution images, the holotype of B. londongensis was scanned section by section due to its excessive length (Figure 1), as compared with the field of view of the CT scanner: slowly move the small bed horizontally along the long axis of the specimen until its next section is in place, and repeat the procedures above. To ensure contiguous image stitching, a small overlap of two adjacent sections was retained during μCT scan.


Fig.1   Photograph of the holotype specimen (CIB 14380) of Batrachuperus londongensis and our design of μCT scan
The scan of each section generated a data file of 10.3 GB containing 803 files in the raw format. This data file was then converted into an image stack containing 512 16-bit tiff images along the transverse plane of the specimen by using the Quantum GX microCT software. Each image stack was 256 MB, and a total of eight image stacks were generated following the above procedure, which constituted the first subset of this dataset: skull90um.zip, forelimb120um.zip, trunk120um.zip, hindlimb144um.zip, tail_1_120um.zip, tail_2_120um.zip, tail_3_120um.zip, and tail_4_120um.zip.
It is worth noting two differences between the Quantum GX microCT Imaging System and other commonly used CT scanners, such as GE Phoenix v|tome|x s Industrial High-Resolution CT & X-Ray System or Nikon XT H scanners. First, during scanning, the specimen within the Quantum GX scanner remains motionless, and it is the X-Ray source generator that rotates around the specimen for 360°; but the other way around for other scanners. Second, the Quantum GX scanner is able to obtain a higher voxel size of region of interest (ROI) by using its subvolume reconstruction function that comes along with the scanner. A higher resolution of the skull of the holotype of B. londongensis was achieved by imposing subvolume reconstruction on the file for first section, skull90um.zip, and the voxel size increased from 90 μm to 67.1 μm. The resulting file was deposited in the first subset of the dataset as skull67_1um.zip.
2.2   Data processing
The image stacks were processed by using the software package VG Studio Max 2.2 (Volume Graphics, Heidelberg, Germany), including merging adjacent sections of the specimen, segmenting the skeleton, rendering and 3D reconstructing virtual models, and exporting images, videos and stl files.
The first step was to merge files for adjacent sections of the holotype. Sequentially import all 512 16-bit tiff files of each image stack into the software, and save each image stack as a vgl-formatted file. Open a blank file in VG Studio, and import all the vgl files sequentially by using the merge function in the file menu. Then join the two adjacent sections together by referring to the overlapping area.
The second step was to segment and 3D reconstruct the skeletons. Take the cranium for instance, erect a new ROI for each of the bones in the window of VG Studio showing two-dimensional section of the specimen. In each ROI, use the brush tool to draw an outline of the bone that appeared on each slice in the two-dimensional window. Smooth or refine each ROI to generate a smooth appearance for each bone, and extract and render ROIs as digital models (Figure 2).


Fig.2   Reconstructed and rendered images showing the cranium of the holotype specimen (CIB 14380) of Batrachuperus londongensis (A. skull in dorsal view; B. skull in ventral view; C. hyobranchial apparatus in dorsal view; D. hyobranchial apparatus in ventral view)
Notes: bb – basibranchial; cb – ceratobranchial; ch – ceratohyal; fr – frontal; hb – hypobranchial; mx – maxilla; na – nasal; obs – orbitosphenoid; pa – parietal; ps – parasphenoid; pt – pterygoid; sq – squamosal; vo – vomer.
The third step was to export images, videos and stl files. In the window showing the three dimensional model, rotate and enlarge the skull to a certain aspect (such as dorsal, ventral or lateral views), save images by clicking the save button in the file menu and store them as pics.zip. Similarly, rotate the skull along a certain axis by using the keyframer mode in the animation menu, and export videos and store them as videos.zip. Then impose surface determination on each exported ROI, and store the results as pdf_stl.zip in this dataset.
3.   Sample description
3.1   File naming format
The files in this dataset are named as follows:
(1) The first subset of the dataset contains 9 files. Take the first file “skull90um.zip” and the fifth file “tail_1_120um” as examples: “skull” denotes μCT scan images of the skull, and “90um” represents the voxel size of this section; “tail_1” denotes scan images of the first section of the tail, and “120um” represents the voxel size of this section. Each file in the first subset contains a parameter file in xml format, and 512 16-bit tiff images. Names of the tiff files were supplemented by a sequentially labeled suffix “p001 – p512”. Hence we suggest that these files be sequentially imported and/or read by software like VG Studio to ensure the integrity of the bony structure.
(2) The second subset of the dataset consists of three files, namely, pics.zip, videos.zip and pdf_stl.zip, which store images and videos of the reconstructed skeleton, and a 3D pdf file and stl files of the cranium of the holotype specimen of B. londongensis, respectively. Physical casts of the cranium of the holotype of B. londongensis can be created by printing these stl files using 3D printers based on further processing the stl files.
3.2   Data sample
Information on the systematic zoology of Batrachuperus londongensis are as below:
Class Amphibia Linnaeus, 1758
Subclass Lissamphibia Haeckel, 1866
Superorder Caudata Scopoli, 1777
Order Urodela Duméril, 1806
Suborder Cryptobranchoidea Dunn, 1922
Family Hynobiidae Dunn, 1922
Genus Batrachuperus Boulenger, 1878
Batrachuperus londongensis Liu and Tian, 1978
Batrachuperus londongensis is unique among hynobiids, in having both metamorphosed and neotenic individuals with adults of the latter having larval features such as gill slits. This holotype specimen (CIB 14380) is a neotenic individual with gill slits. μCT scan of the holotype demonstrates that the bony components of its hyobranchial apparatus is of a complex structure, including paired hypobranchial I, hypobranchial II, ceratobranchial I – IV, ceratohyal and a single basibranchial II (Figure 2). Compared with other hynobiids which usually have the paired hypobranchial II and ceratobranchial II as bony elements, B. londongensis possesses an obviously higher ossification level in its hyobranchial apparatus.33–34
Figure 3 shows the reconstructed whole skeleton of the holotype of B. londongensis. The holotype has 17 presacrals, and both carpals (labeled in red) in the forelimb and tarsals (labeled in blue) in the hind limb are fully ossified, in contrast to the cartilaginous carpals and tarsals seen in other neotenic salamanders (e.g., sirenids, amphiumids).


Fig.3   Reconstructed and rendered images showing the complete skeleton of the holotype specimen (CIB 14380) of Batrachuperus londongensis (left: dorsal view; right: ventral view)
4.   Quality control and assessment
This dataset contains original data resulted from μCT scan of the holotype of B. londongensis and corresponding parameter data, which can be read by commonly used software, such as Amira, Dragonfly, ImageJ, Mimics, or VG Studio.
Resolution or voxel size of the images in this dataset are affected by the following two factors: first, the size of the field of view, which determines the resolution of images generated by the Quantum GX microCT Imaging System. The size of the field of view is restricted by acquisition and reconstruction parameters (Table 1). There are two acquisition parameters: 36 and 72, and several corresponding reconstruction parameters: 36, 25, 10, 5 and 72, 60, 45.
Table 1   Field of view and corresponding voxel size in using the small bed of the Quantum GX microCT Imaging System
Field of ViewVoxel Size (μm)Section of the Holotype
AcquisitionReconstruction
36510
361020
362550
363672
7245901
72601202, 3, 5, 6, 7, 8
72721444
Second, different widths of the different parts of the holotype lead to varied image resolutions. Kept in formalin solution for 50 years, the holotype specimen had stiff muscles and cartilaginous tissues. As a result, images of the hind limb section have the lowest resolution (144 μm), because the hind limb stretches bilaterally and is under full coverage only within the maximum field of view, when acquisition and reconstruction parameters are both set as 72. Despite lowest resolution, the images of the hind limb show a clear and recognizable outline of bones on any transverse section (Figure 4).


Fig.4   μCT scan of the holotype specimen (CIB 14380) of Batrachuperus londongensis showing the outline of bones in different transverse sections
Notes: A. cranium section after subvolume reconstruction (voxel size: 67.1 μm); B. cranium section (voxel size: 90 μm); C. forelimb section (voxel size: 120 μm); D. hind limb section (voxel size: 144 μm)
5.   Value and significance
This dataset contains high-resolution μCT scan data of the holotype specimen (CIB 14380) of Batrachuperus londongensis, a hynobiid endemic in the Longdong River area of Mount Emei, Sichuan Province, China. This study represents the first application of μCT scan in the investigation of living hynobiids in China. Easy to use, this dataset provides researchers with raw data for comparative studies of living salamanders. Although platforms like DigiMorph offer μCT scan data of several salamander specimens, there is a substantial shortage of information on the species endemic in China. In this sense, this dataset provides data that are essential for the establishment of such platforms in China, and is valuable for morphological studies of Chinese hynobiids.
Acknowledgments
We thank Wang Yuezhao (Chengdu Institute of Biology, Chinese Academy of Sciences) for his support for, and approval of, our request to access the holotype of Batrachuperus londongensis, and Li Yulong (Chengdu Institute of Biology, Chinese Academy of Sciences) for his efforts in μCT scanning several other specimens of this taxon.
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Data citation
1. Jia J, Zhang M, Gao K et al. μCT source dataset of the holotype (CIB 14380) of Batrachuperus londongensis from Sichuan Province, China. Science Data Bank. DOI: 10.11922/sciencedb.557
Article and author information
How to cite this article
Jia J, Zhang M, Gao K et al. Dataset of μCT scan of the holotype specimen of Batrachuperus londongensis Liu and Tian, 1978, an endemic hynobiid (Amphibia, Urodela) from Mount Emei, Sichuan Province, China. China Scientific Data 2(2018). DOI: 10.11922/csdata.2018.0005.zh
Jia Jia
manuscript writing and revision, design of the μCT scan and data processing, segmentation and 3D reconstruction of the holotype of Batrachuperus londongensis, preparation of the figures, videos and 3D pdf file.
jia_jia@pku.edu.cn
PhD, Boya Postdoctoral Fellow; research area: taxonomy and evolutionary study of fossil amphibians.
Zhang Meihua
manuscript writing and revision, photographing and μCT scanning of the holotype specimen, clearing and double staining of other specimens of Batrachuperus londongensis, design of the μCT scan and data processing.
PhD student; research area: systematics and evolution of amphibians.
Gao Keqin
manuscript revision, design of the μCT scan.
PhD, Cheung Kong Professor, Boya Professor; research area: taxonomy and evolutionary study of Mesozoic tetrapods.
Jiang Jianping
manuscript revision, design of the μCT scan.
PhD, Professor; research area: evolution and systematics, protection and utilization of amphibians.
National Natural Science Foundation of China (41702002, 41072007, 41272016); Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences (Nanjing Institute of Geology and Palaeontology) (2017KF03); The National Key Research and Development Program of China, Ministry of Science and Technology (2017YFC0505202)
Publication records
Published: June 22, 2018 ( VersionsEN1
Released: March 23, 2018 ( VersionsZH4
Published: June 22, 2018 ( VersionsZH6
References
中国科学数据
csdata