Research Article |
Corresponding author: Ying-Yong Wang ( wangyy@mail.sysu.edu.cn ) Academic editor: Thomas Ziegler
© 2020 Shuo Qi, Jian Wang, L. Lee Grismer, Hong-Hui Chen, Zhi-Tong Lyu, Ying-Yong Wang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Qi S, Wang J, Grismer LL, Chen H-H, Lyu Z-T, Wang Y-Y (2020) The Stoor Hobbit of Guangdong: Goniurosaurus gollum sp. nov., a cave-dwelling Leopard Gecko (Squamata, Eublepharidae) from South China. ZooKeys 991: 137-153. https://doi.org/10.3897/zookeys.991.54935
|
A new species of the genus Goniurosaurus is described based on three specimens collected from a limestone cave in Huaiji County, Guangdong Province, China. Based on molecular phylogenetic analyses, the new species is nested within the Goniurosaurus yingdeensis species group. However, morphological analyses cannot ascribe it to any known species of that group. It is distinguished from the other three species in the group by a combination of the following characters: scales around midbody 121–128; dorsal tubercle rows at midbody 16–17; presence of 10–11 precloacal pores in males, and absent in females; nuchal loop and body bands immaculate, without black spots; iris orange, gradually darker on both sides. The discovery of yet another limestone-adapted species of Goniurosaurus in Guangdong Province underscores a growing body of evidence for the high biodiversity of limestone habitats and brings into sharp focus the urgent need for their conservation.
Goniurosaurus gollum, sp. nov., karst, limestone cave, taxonomy, systematics
The eublepharid genus Goniurosaurus Barbour, 1908, currently contains 22 species that are scattered throughout much East and northern Southeast Asia (
Currently, three narrowly distributed species within the Goniurosaurus yingdeensis group are known from the karst environments of northern Guangdong, China: G. yingdeensis Wang, Yang & Cui, 2010, G. zhelongi Wang, Jin, Li & Grismer, 2014 and G. varius Qi, Grismer, Lyu, Zhang, Li & Wang, 2020. These three species share consistent morphological features that differentiate them from species of the other groups: (1) base of claws sheathed by four scales, two lateral scales of claw short and shell-shaped; (2) precloacal pores fewer than 15 in males and absent in most females (precloacal pores present in females in G. yingdeensis only); precloacal pores form a continuous transverse series not extending onto the femora; (3) enlarged row of supraorbital tubercles indistinct or absent; (4) nuchal loop rounded posteriorly; and (5) four body bands between the nuchal loop and the caudal constriction.
During our herpetological surveys in Guangdong Province, China, three specimens of Goniurosaurus were collected from a new locality during May 2020. Morphological and molecular analyses place this new population within the Goniurosaurus yingdeensis group but cannot ascribe them to any of the known species. We therefore describe this population as a new species.
Three specimens of the undescribed species were collected from Huaiji County, Guangdong Province, China. Following euthanasia, all specimens were fixed in 10% formalin and transferred to 75% alcohol. Tissue samples were preserved in 99% alcohol and stored at -40 °C. All specimens are deposited in The Museum of Biology, Sun Yat-sen University (
Measurements were taken following
Morphological character data of known congeners were taken from the literature (
Genomic DNA was extracted from muscle tissue samples, using a DNA extraction kit from Tiangen Biotech (Beijing) Co., Ltd. Partial segments of the mitochondrial genes 16S ribosomal RNA gene (16S) and Cytochrome b gene (Cytb) were amplified. Primers used for 16S were r16S-5L (5’- GGTMMYGCCTGCCCAGTG -3’) and 16sbr-H (5’- CCGGTCTGAACTCAGATCACGT-3’) (
Fifty-one sequences from 13 known Goniurosaurus species plus one outgroup sequence from the eublepharid Hemitheconyx taylori Parker, 1930, which was used to root the tree, were obtained from GenBank and composed the dataset (Table
Localities, voucher information, and GenBank accession numbers for all specimens used in this study.
Species name | Locality | Specimen voucher | 16S | Cytb | References |
---|---|---|---|---|---|
Ingroup: Goniurosaurus | |||||
Goniurosaurus yingdeensis species group | |||||
(1) Goniurosaurus gollum sp. nov. | Huaiji, Guangdong, China |
|
MT995784 | MT995787 | This study |
(2) Goniurosaurus gollum sp. nov. | Huaiji, Guangdong, China |
|
MT995785 | MT995788 | This study |
(3) Goniurosaurus gollum sp. nov. | Huaiji, Guangdong, China |
|
MT995786 | MT995789 | This study |
(4) G. varius | Yangshan, Guangdong, China |
|
MT995753 | MT995768 |
|
(5) G. varius | Yangshan, Guangdong, China |
|
MT995754 | MT995769 |
|
(6) G. varius | Yangshan, Guangdong, China |
|
MT995755 | MT995770 |
|
(7) G. varius | Yangshan, Guangdong, China |
|
MT995756 | MT995771 |
|
(8) G. varius | Yangshan, Guangdong, China |
|
MT995757 | MT995772 |
|
(9) G. yingdeensis | Yingde, Guangdong, China |
|
MT995759 | MT995774 |
|
(10) G. yingdeensis | Yingde, Guangdong, China |
|
MT995760 | MT995775 |
|
(11) G. yingdeensis | Yingde, Guangdong, China |
|
MT995761 | MT995776 |
|
(12) G. yingdeensis | Yingde, Guangdong, China |
|
MT995762 | MT995777 |
|
(13) G. zhelongi | Yingde, Guangdong, China |
|
KJ423105 | MT995778 |
|
(14) G. zhelongi | Yingde, Guangdong, China |
|
MT995763 | MT995779 |
|
(15) G. zhelongi | Yingde, Guangdong, China |
|
MT995764 | MT995780 |
|
(16) G. zhelongi | Yingde, Guangdong, China |
|
MT995765 | MT995781 |
|
Goniurosaurus luii species group | |||||
(17) G. huuliensis | Vietnam | N/A | AB853453 | AB853479 |
|
(18) G. liboensis | Libo, Guizhou, China |
|
KC900230 | N/A |
|
(19) G. luii | Jingxi, Guangxi, China |
|
KC765083 | N/A |
|
(20) G. luii | Jingxi, Guangxi, China |
|
KC765084 | N/A |
|
(21) G. luii | Cao Bang,Vietnam | ZFMK 87057 | EU499391 | N/A |
|
Goniurosaurus lichtenfelderi species group | |||||
(22) G. bawanglingensis | Bawangling, Hainan, China |
|
MT995758 | MT995773 |
|
(23) G. bawanglingensis | Bawangling, Hainan, China | BL-RBZ-021 | MH247190 | MH247201 |
|
(24) G. hainanensis | Jianfengling, Hainan, China |
|
KC765080 | N/A |
|
(25) G. zhoui | Central area, Hainan, China |
|
MT995766 | MT995782 |
|
(26) G. zhoui | Central area, Hainan, China |
|
MT995767 | MT995783 |
|
(27) G. zhoui | Central area, Hainan, China | BL-RBZ-001 | MH247196 | MH247207 |
|
Goniurosaurus kuroiwae species group | |||||
(28) G. kuroiwae | Northern Okinawajima Island, Japan | N/A | AB853448 | AB853473 |
|
(29) G. orientalis | Iejima Island, Japan | N/A | AB853446 | AB853467 |
|
(30) G. splendens | Tokunoshima Island, Japan | N/A | AB853451 | AB853477 |
|
(31) G. yamashinae | Kumejima Island, Japan | N/A | AB853442 | AB853460 |
|
Outgroup | |||||
(32) Hemitheconyx taylori | East Africa | N/A | AB308457 | N/A |
|
The ML and BI analyses resulted in identical topologies (Fig.
Uncorrected P-distance of 16S gene among 14 Goniurosaurus species used in this study.
ID | 1–3 | 4–8 | 9–12 | 13–16 | 17 | 18 | 19–21 | 22–23 | 24 | 25–27 | 28 | 29 | 30 | 31 | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1–3 | Goniurosaurus gollum sp. nov. | 0–0 | |||||||||||||
4–8 | G. varius | 5.6 | 0–0.1 | ||||||||||||
9–12 | G. yingdeensis | 5.9 | 4.2 | 0–0.3 | |||||||||||
13–16 | G. zhelongi | 5.5 | 3.3 | 4.7 | 0–0.2 | ||||||||||
17 | G. huuliensis | 17.4 | 12.9 | 15.5 | 14.5 | / | |||||||||
18 | G. liboensis | 15.7 | 13.1 | 13.4 | 13.5 | 6.1 | / | ||||||||
19–21 | G. luii | 16.4 | 13.9 | 14.5 | 14.7 | 1.4 | 5.9 | 0–0.5 | |||||||
22–23 | G. bawanglingensis | 17.3 | 15.9 | 16.8 | 15.8 | 17.4 | 14.5 | 17.3 | 0–0.3 | ||||||
24 | G. hainanensis | 17.3 | 16.6 | 16.6 | 17.9 | 14.8 | 14.5 | 15.3 | 8.3 | / | |||||
25–27 | G. zhoui | 16.7 | 16.3 | 18.1 | 17.3 | 16.1 | 16.5 | 17.2 | 7.0 | 7.5 | 0-0 | ||||
28 | G. kuroiwae | 22.7 | 21.2 | 20.3 | 22.4 | 22.2 | 23.4 | 21.5 | 18.7 | 18.9 | 18.9 | / | |||
29 | G. orientalis | 21.3 | 18.5 | 18.2 | 19.6 | 21.3 | 22.2 | 21.3 | 19.6 | 19.8 | 18.8 | 3.6 | / | ||
30 | G. splendens | 21.9 | 19.7 | 19.0 | 21.8 | 22.9 | 23.3 | 22.2 | 19.8 | 18.1 | 20.2 | 7 | 7.9 | / | |
31 | G. yamashinae | 22 | 18.5 | 18.8 | 19.9 | 21.4 | 22.9 | 22 | 20.3 | 19.1 | 19.2 | 3.7 | 3.1 | 7 | / |
Bayesian inference tree of 14 species of Goniurosaurus, based on the partial DNA sequences of the mitochondrial 16S rRNA and Cytb genes. Hemitheconyx taylori is the outgroup. Numbers before slash indicate Bayesian posterior probabilities (BPP) and numbers after slash are bootstrap support for ML (1000 replicates) analyses.
Holotype.
Goniurosaurus gollum sp. nov. can be distinguished from all other congeners by the following combination of characters: (1) adult body size moderate, 91.0–93.4 mm SVL; (2) nasal scales surrounding nares seven or eight; (4) internasal single; (5) eyelid fringe scales 59–63; (6) granular scales of upper eyelids similar in size to those on top of head; (7) scales around midbody 121–128; (8) longitudinal dorsal tubercle rows at midbody 16 or 17; (9) paravertebral tubercles between limb insertions 25 or 26; (10) claws sheathed by four scales, dorsal claw scales small, two lateral claw scales short and shell-shaped; (11) axillary pockets deep; (12) presence of 10 or 11 precloacal pores in males and absent in females; (13) dorsal ground color of head, body, and limbs in adults yellowish brown and mottled with irregularly shaped dark-brown blotches; (14) nuchal loop complete, rounded posteriorly; (15) presence of three or four thin dorsal body bands between nuchal loop and caudal constriction, with black anterior and posterior borders, bands usually irregularly shaped; (16) iris orange, gradually darker on both sides.
Type series of Goniurosaurus gollum sp. nov. A holotype, male,
Goniurosaurus gollum sp. nov. can be distinguished from the other 21 known species in the genus by the following combination of characters: base of claws being sheathed by four scales, two lateral claw scales short and shell-shaped (vs. claws sheathed by four scales, two lateral scales of claw long, curved in G. lichtenfelderi group and G. luii group, and not sheathed in G. kuroiwae group); having 10 or 11 precloacal pores in males (vs. 17–46 in G. lichtenfelderi group, 16–33 in G. luii group and absent in G. kuroiwae group); and lacking an enlarged row of supraorbital tubercles (present in G. lichtenfelderi group and G. luii group).
Goniurosaurus gollum sp. nov. can be distinguished from its closest relatives in the Goniurosaurus yingdeensis group by the following combination of characters: scales around midbody 121–128 (vs. 101–110 in G. varius, 101–116 in G. yingdeensis, 99–109 in G. zhelongi); longitudinal dorsal tubercle rows at midbody 16 or 17 (vs. 21–24 in G. varius, 20–25 in G. yingdeensis, 23–28 in G. zhelongi); absence of ten precloacal pores in females (vs. present in G. yingdeensis); nuchal loop and body bands immaculate (vs. having black spots in G. varius); iris orange, gradually darker on both sides (vs. iris orange-red in G. varius, iris gray and becoming orange near the pupil in G. yingdeensis, iris gray-white and tinged with orange in G. zhelongi). Additional comparisons of morphological characteristics are provided in Table
Comparisons of iris color with three closely related congeners A Goniurosaurus gollum sp. nov. (holotype,
Adult male with original tail; SVL 93.4 mm; HL 24.2 mm; HW 16.2 mm; SE 9.3 mm; EE 9.3 mm; SVL:HL 3.9; HL:HW 1.5; SE:EE 1. Head triangular, wider than neck, covered with granular scales, densely interspersed with tubercles in the temporal and occipital regions; area between orbits uniformly covered by small granular scales; supraorbital tubercles nearly uniform in size; scales of rostrum slightly larger than those in between orbits; rostral convex and hemi-elliptic, 1.8 times as broad as high, middorsal portion of rostral partially sutured dorsomedially, bordered laterally by first supralabial and prenasal, dorsolaterally by supranasal, dorsally by one internasal; external nares oval, surrounded by 8/9 nasals each, anteriorly by prenasal and supranasal, dorsally by supranasal and a granular scale, posteriorly by 7/8 smaller granular scales, and ventrally by the prenasal; prenasal with long recurved ventral portion; supranasals large, separated by one internasals; supralabials rectangular, 10/10; preorbital scales 16/17; eyes relatively large, pupils vertical; eyelid fringe scales 59/60; outer surface of upper eyelid composed of granular scales of about same size of those on top of head; external auditory meatus circular, tympanum deeply recessed; mental triangular, bordered laterally by first infralabial and posteriorly by three postmentals; infralabials rectangular, 10/10; gular scales juxtaposed uniform granular, abruptly into flat juxtaposed pectoral scales, and grading posteriorly imbricated larger ventral scales. Tongue with a small notch at tip. Crowns of teeth expanded, occlusal margins bearing multiple ridges.
Dorsal surface of neck and body covered with uniform granular scales, interspersed with densely sharply pointed conical tubercles; scales around midbody 125; longitudinal rows of dorsal tubercles at midbody 16; vertebral row of scales indistinct; paravertebral tubercles between limb insertions 25; dorsal body tubercles surrounded by 9–10 granular scales; dorsal scales grading ventrally into larger flattened imbricate ventral scales; ten precloacal pores in a transverse series; postcloacal region greatly swollen, covered with imbricate flattened scales, containing 2/2 postcloacal tubercles laterally at level of the vent.
Tail original, long and thin, thickest at base, bearing whorls anteriorly, gradually narrowing to the tip; composed of nine recognizable annuli anteriorly that are 8–9 scales wide, annuli fade abruptly posteriorly into flat juxtaposed scales; incorporating 2–8 sharply pointed conical tubercles in a transverse row, tubercles do not encircle the tail; ventral caudals larger and more nearly square than dorsal caudals.
Limbs relatively long and slender; dorsal surface covered with granular scales, densely interspersed with tubercles; ventral surface covered by flat scales, juxtaposed, subimbricate or imbricate; dorsal surface of pes and manus covered with granular scales, interspersed with several conical tubercles on top of pes, lacking tubercles on top of manus; hind limbs slightly larger than forelimbs; ventral surfaces of pes and manus covered with large granular scales; axillary pockets deep; subdigital lamellae wide, 10/10 on Finger I, 12/14 on Finger II, 15/16 on Finger III, 16/14 on Finger IV, 13/14 on Finger V, 12/12 on Toe I, 15/ 16 on Toe II, 20 / 19 on Toe III, 22 / 23 on Toe IV, and 18 / 20 on Toe V; fingers laterally compressed, relative finger lengths I<V<II<IV<III; toes laterally compressed, third toe nearly as long as the fourth toe, relative toe length I<II<V<III<IV; base of claws sheathed by four scales, two lateral scales of claw short, asymmetrical shell-shaped.
Dorsal ground color of head, neck, body, and limbs yellowish brown, mottled with irregularly shaped dark-brown blotches; nuchal loop complete and rounded posteriorly, anterior ends terminating at posterior margins of ear openings, edged dorsally and ventrally by wide dark-brown margin, yellow. Only two complete body bands can be recognized between nuchal loop and caudal constriction: first band located posterior to axilla; second band inserts onto dorsal surface of thigh, bands on limbs dirty yellow, lacking dark spots, edged by broad dark-brown borders anteriorly and posteriorly, other blotches incomplete, not forming a complete bands. Supralabials and infralabials grayish brown; pupils vertical and appear black; iris orange, gradually darkening on both sides; dorsal surface of limbs light grayish brown with dark brown and dirty yellow tubercles and dark spots and blotches; chin, throat, thorax, and ventral surfaces of body pink, tinged brownish, with dark-brown lateral spots; ventral surface of limbs pink, tinged brownish, without dark-brown spots; digits light grayish brown; ground color of original tail dark brown with nine immaculate white caudal bands completely encircling the tail, and a white tip. Body color becomes darker after capture.
Dorsal ground color of head, body, and limbs become darker; ventral surface faded to grayish white; all darker spots, blotches and bands on dorsal surface blurred.
Measurements of type series specimens are shown in Table
Mensural (mm) and meristic diagnostic characters (minimum/maximum) of type series of Goniurosaurus gollum sp. nov. See Materials and methods for abbreviations. * holotype, # paratype.
Morphological character |
|
|
|
---|---|---|---|
Sex | male | male | female |
SVL | 93.4 | 93.3 | 91.0 |
TaL | 83.5 | Regenerated | 76.0 |
HL | 24.2 | 24.0 | 23.3 |
HW | 16.2 | 15.3 | 14.8 |
SE | 9.3 | 9.3 | 9.1 |
EE | 9.3 | 9.4 | 8.6 |
SPL | 10/10 | 10/10 | 10/10 |
IFL | 10/10 | 10/10 | 10/10 |
N | 8/9 | 9/8 | 8/9 |
IN | 1 | 1 | 1 |
PostIN | 2 | 2 | 2 |
PM | 2 | 3 | 3 |
GP | 7 | 8 | 8 |
CIL | 59/60 | 59/61 | 63/63 |
PO | 16/17 | 15/15 | 16/17 |
GST | 9–10 | 9–10 | 9–11 |
PTL | 25 | 26 | 25 |
DTR | 16 | 16 | 17 |
MB | 125 | 121 | 128 |
PP | 10 | 11 | Absent |
PAT | 2 | 2 | 2 |
The specific epithet “gollum” is named after the fictional character, Gollum, from J.R.R. Tolkien’s The Lord of the Rings book series. This new species and Gollum have similar cave-dwelling habit and emaciated body. We suggest the common name as “Gollum Leopard Gecko”, and according to the type locality, we suggest the Chinese formal name as “guǎng dōng jiǎn hǔ” (广东睑虎).
Diagnostic characters distinguishing Goniurosaurus gollum sp. nov. from all other known species of Goniurosaurus. Data come from
Character | G. kuroiwae group | G. lichtenfelderi group | G. luii group | G. yingdeensis group (4 species) | |||
(5 spp.) | (5 spp.) | (7 spp.) | Goniurosaurus gollum sp. nov. | G. varius | G. yingdeensis | G. zhelongi | |
Scales of upper eyelid one-half the size of scales on the top of head or equal in size | Equal | Equal | Equal or 1/2 | Equal | Equal | Equal | Equal |
Enlarged row of supraorbital tubercles | Absent | Absent or present | Absent or present | Absent | Absent | Absent or indistinct | Absent or indistinct |
Eyelid fringe scales | <52 | 43–77 | 41–67 | 59–63 | 50–56 | 46–64 | 42–53 |
No. of paravertebral tubercles | Unknown | 23–36 | 27–38 | 25–26 | 27–29 | 22–33 | 28–33 |
Dorsal tubercle rows at midbody | Unknown | 19–22 | 20–25 | 16–17 | 21–24 | 20–25 | 23–28 |
Scales around midbody | Unknown | 95–140 | 112–147 | 121–128 | 101–110 | 101–116 | 99–109 |
Nasal scales surrounding nares | Unknown | 8–9 | 5–9 | 7–8 | 7–9 | 7–11 | 6–8 |
Internasals | Unknown | 1 | 0–3 | 1 | 1–2 | 1–3 | 1–2 |
Tubercles between orbits | Present or absent | Present or absent | Present or absent | Absent | Present | Present | Absent |
Claws sheathed by scales | Absent | Present | Present | Present | Present | Present | Present |
Lateral scales of claw sheaths | Absent | Long, curved | Long, curved | Short, shell-shaped | Short, shell-shaped | Short, shell-shaped | Short, shell-shaped |
No. of precloacal pores in males | 0 | 17–46 | 16–33 | 10–11 | 10 | 10–13 | 9–12 |
Posterior shape of nuchal loop | Rounded | Protracted or rounded | Protracted | Rounded | Rounded | Rounded | Rounded |
No. of body bands between nuchal loop and the caudal constriction | 3 or 4 | 3 or 4 | 3, 4 or 5 | 2,3 or 4 | 4 | 4 | 4 |
Dark spotting in body bands | Present or absent | Present or absent | Present or absent | Absent | Present or absent | Absent | Absent |
Lateral spotting on belly present or absent | Absent | Absent | Present or absent | Present | Present | Present | Present |
Currently, Goniurosaurus gollum sp. nov. is known only from Huaiji County, Guangdong Province, China. All individuals were found within a barren limestone cave approximately 50 m from the cave entrance at night after 2130 hrs (Fig.
With the description of Goniurosaurus gollum, there are now 23 known species in the eublepharid genus Goniurosaurus, 15 of which occur in China. The G. yingdeensis group is endemic in Guangdong Province, with only two species recognized previously, but the discoveries of G. varius (
Although the species of Goniurosaurus are also called “cave geckos”, they prefer inhabiting the forest floor, limestone cliffs, rocky and cement drains along the road, and near the entrances of caves. However, the cave-dwelling species G. gollum appears to be a true cave dweller as opposed to other Goniurosaurus. The fact that all three specimens were found at least 50 m inside the cave from its entrance supports this hypothesis.
These results support the growing body of evidence from China (
We thank Truong Nguyen, Nikolai L. Orlov, Minh Duc Le and Thomas Ziegler for their helpful comments and suggestions on the manuscript. We thank the Zhaoqing City Forestry Bureau for provided information. This study is supported by the Goniurosaurus yingdeensis Population Conservation Research of Guangdong Shimentai National Nature Reserve and the Mohamed bin Zayed Species Conservation Fund (project no.14259912).
Examined specimens
Goniurosaurus bawanglingensis (N = 3): China: Hainan Province: Bawangling National Nature Reserve:
Goniurosaurus hainanensis (N = 2): China: Hainan Province: Jianfengling National Forest Park:
Goniurosaurus liboensis (N = 3): China: Guizhou Province: Libo County: Maolan National Nature Reserve:
Goniurosaurus luii (N = 4): China: Guangxi Zhuang Autonomous Region: Jingxi City:
Goniurosaurus varius (N = 5): China: Guangdong Province: Yangshan County:
Goniurosaurus yingdeensis (N = 10): China: Guangdong Province: Yingde City:
Goniurosaurus zhelongi (N = 5): China: Guangdong Province: Yingde City:
Goniurosaurus zhoui (N = 2): China: Hainan Province: