DSpace at VNU: A new species of Cyrtodactylus (Squamata: Gekkonidae) from Ninh Binh Province, Vietnam

DSpace at VNU: A new species of Cyrtodactylus (Squamata: Gekkonidae) from Ninh Binh Province, Vietnam tài liệu, giáo án,...

ZOOTAXA ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)

Copyright © 2016 Magnolia Press

Zootaxa 4162 (2): 268–282

http://www.mapress.com/j/zt/ Article

http://doi.org/10.11646/zootaxa.4162.2.4 http://zoobank.org/urn:lsid:zoobank.org:pub:A6C2B048-C5F3-4B55-B4D7-F60855E2836E

A new species of Cyrtodactylus (Squamata: Gekkonidae)

from Ninh Binh Province, Vietnam

1 Faculty of Biology, Hanoi National University of Education, 136 Xuan Thuy Road, Hanoi, Vietnam

E-mail: letrungdung_sp@hnue.edu.vn

2 Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam E-mail: nqt2@yahoo.com

3 Faculty of Environmental Sciences, Hanoi University of Science, Vietnam National University, 334 Nguyen Trai Road, Hanoi, Vietnam E-mail: le.duc.minh@hus.edu.vn

4 Centre for Natural Resources and Environmental Studies, Hanoi National University, 19 Le Thanh Tong, Hanoi, Vietnam

5 Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024

6 AG Zoologischer Garten Köln, Riehler Strasse 173, D–50735 Cologne, Germany E–mail: ziegler@koelnerzoo.de

7 Institute of Zoology, University of Cologne, Zülpicher Strasse 47b, D–50674 Cologne, Germany

8 Corresponding author E-mail: nqt2@yahoo.com.

Abstract

We describe a new species of the genus Cyrtodactylus on the basis of six specimens collected from the limestone forest

of the Van Long Wetland Nature Reserve, Ninh Binh Province, Vietnam Cyrtodactylus soni sp nov can be distinguished from its congeners by genetic distinction and morphological differences in number of femoral and precloacal pores, fem-oral scales, ventral scales, lamellae, subcaudals, and dorsal tubercle arrangement, as well as in size and color pattern In the phylogenetic analyses, the new species is nested in a clade containing taxa from northwestern and northcentral Viet-nam and northern Laos

Key words: Cyrtodactylus soni sp nov., karst forest, molecular phylogeny, taxonomy, Van Long Wetland Nature Reserve

Introduction

Recent herpetological work has underlined the special role of karst habitats in promoting speciation of gekkonid lizards in Vietnam, particularly the bent-toed geckos of the genus Cyrtodactylus (Nguyen et al 2015) The knowledge on species richness of this genus in Vietnam has dramatically increased from three in 1997 to 37 at present (Nguyen et al 2015) In the northern part of the country, numerous new species have been discovered in karst forests during the past five years, namely Cyrtodactylus bichnganae Ngo & Grismer, 2010 from Son La Province, C cucphuongensis Ngo & Chan, 2011 from Ninh Binh Province, C huongsonensis Luu, Nguyen, Do & Ziegler, 2011 from Hanoi, C martini Ngo, 2011 from Lai Chau Province, C bobrovi Nguyen, Le, Pham, Ngo, Hoang, Pham & Ziegler, 2015, and C otai Nguyen, Le, Pham, Ngo, Hoang, Pham & Ziegler, 2015 from Hoa Binh Province

During recent field work in northern Vietnam, we collected six specimens of an unnamed gekkonid species from Van Long Wetland Nature Reserve in Ninh Binh Province, which can be assigned to Cyrtodactylus based on morphological features and phylogenetic analyses Herein, we describe it as a new species

Material and methods

Sampling Field surveys were conducted in Van Long Wetland Nature Reserve, Ninh Binh Province, northern

Vietnam, in July and August 2015 Specimens were anaesthetized and fixed in approximately 85% ethanol, then later transferred to 70% ethanol for permanent storage Specimens referred to in this paper are deposited in the collections of the Museum of Biology, Hanoi National University of Education (HNUE), Hanoi; the Institute of Ecology and Biological Resources (IEBR), Hanoi; the Tay Bac University (TBU), Son La Province; Muséum d'histoire naturelle, Geneva (MHNG), Switzerland; the Vietnam Forest Museum (VFM), Forest Inventory and Planning Institute, Hanoi; the Vietnam National Museum of Nature (VNMN), Hanoi; the Vietnam National University of Forestry (VUF), Hanoi, Vietnam; the Namlik Ecovillage Museum (NEM), Ban That Wang Monh, Vientiane Province, Laos; the National University of Laos (NUOL), Vientiane, Laos; the Senckenberg Naturhistorische Sammlungen Dresden, Museum für Tierkunde (MTD), Dresden; and the Zoologisches Forschungsmuseum Alexander Koenig (ZFMK), Bonn, Germany

Molecular data and phylogenetic analyses We sequenced two samples of Cyrtodactylus collected from Van Long Wetland Nature Reserve and the holotype of C huongsonensis (IEBR A.2011.3A, see Luu et al 2011) We also included all available sequences from members of the C wayakonei species group (Fig 1, Table 1) The species group was defined as clade B in Nguyen et al (2015) Two species, C elok Dring and C pulchellus Gray (see Grismer et al 2012), were used as outgroups

We used the protocols of Le et al (2006) for DNA extraction, amplification, and sequencing A fragment of the mitochondrial gene, cytochrome c oxidase subunit 1 (COI), was amplified using the primer pair VF1-d and VR1-d (Ivanova et al 2006) After sequences were aligned by Clustal X v2 (Thompson et al 1997), data were analyzed using maximum parsimony (MP) and maximum likelihood (ML) as implemented in PAUP*4.0b10 (Swofford 2001) and Bayesian analysis (BA) as implemented in MrBayes v3.2 (Ronquist et al 2012) Settings for these analyses followed Le et al (2006), except that the number of generations in the Bayesian analysis was increased to

selected by Modeltest v3.7 (Posada & Crandall 1998) The cutoff point for the burn-in function was set to 11 in the Bayesian analysis, as -lnL scores reached stationarity after 11,000 generations in both runs Nodal support was evaluated using Bootstrap replication (BP) as estimated in PAUP and posterior probability (PP) in MrBayes v3.2 Uncorrected pairwise divergences were calculated in PAUP*4.0b10 (Table 2)

Morphological characters Measurements were taken with a digital caliper to the nearest 0.1 mm Abbreviations are as follows: snout-vent length (SVL, from tip of snout to anterior margin of cloaca), tail length (TaL, from posterior margin of cloaca to tip of tail), head length (HL, from tip of snout to the posterior margin of the retroarticular), maximum head width (HW), maximum head height (HH, from occiput to underside of jaws), internarial distance (IND), interorbital distance (IOD), greatest diameter of orbit (OD), snout to eye distance (SE, from tip of snout to anteriormost point of eyeball), eye to ear distance (EE, from anterior edge of ear opening to posterior corner of eye), nostril to eye distance (NE, from nostril to anteriormost point of eyeball), ear diameter (ED, maximum diameter of ear), forearm length (ForeaL, from base of palm to elbow), crus length (CrusL, from base of heel to knee), trunk length or axilla-groin distance (AG, from posterior edge of forelimb insertion to anterior edge of hind limb insertion), maximum body width at midbody (BW)

Scale counts were taken using a stereo microscope (Leica M80): supralabials (SL) and infralabials (IL), counted from the first labial scale to the corner of mouth, nasal scales surrounding nare (N, i.e nasorostral, supranasal, postnasals), postrostrals or internasals (IN), ciliaria (CIL, scales on eyelid fringe), postmentals (PM), granular scales surrounding dorsal tubercles (GST), ventral scales in longitudinal rows at midbody (V) counted transversely across the center of the abdomen from one ventrolateral fold to the other, number of scales along the midbody from mental to anterior edge of cloaca (SLB), femoral pores (FP), precloacal pores (PP) or the total number of femoral and precloacal pores (i.e the contiguous rows of femoral and precloacal scales bearing pores combined as a single meristic character referred to as the femoroprecloacal pores), postcloacal tubercles (PAT), dorsal tubercle rows (TubR, counted transversely across the center of the dorsum from one ventrolateral fold to the other), enlarged femoral scales (EFS), number of subdigital lamellae on fingers (NSF I–V) and number of subdigital lamellae on toes (NST I–V) counted from the base of the first phalanx to the claw Bilateral scale counts were given as left/right Other abbreviations are as follows: above sea level (a.s.l.) and nature reserve (NR)

Phylogenetic analyses

The final matrix consisted of 657 aligned characters, of which 212 are parsimony informative The alignment contained no gap MP analysis of the dataset recovered two most parsimonious trees with 578 steps (CI = 0.58; RI

= 0.76) In the ML analysis, the score of the single best tree found was 3361.12 after 2448 arrangements were tried The topology derived from the Bayesian analysis (Fig 1) is similar to clade B in Nguyen et al (2015), but C bichnganae was supported as the sister taxon to C huongsonensis + the new species instead of being placed as the basal taxon of the clade as shown in Nguyen et al (2015) (Fig 1) However, both placements received low statistical support values from all analyses The new species was recovered as the sister taxon to C huongsonensis with high statistical support values from all phylogenetic analyses These two species were approximately 5.0– 5.5% genetically divergent from each other (Table 1)

TABLE 1 Uncorrected (“p) distance matrix showing percentage pairwise genetic divergence (COI) between new and closely related species

Cyrtodactylus soni sp nov

(Figs 2–4)

Holotype HNUE VL.2015.78, adult male, collected on 24 July 2015 by D T Le, A M Luong, D T Pham, and

Commune, within Van Long Wetland Nature Reserve, Gia Vien District, Ninh Binh Province, Vietnam

Paratypes IEBR R.2016.4, adult female, HNUE VL.2015.94, adult female, collected on 24 July 2015; IEBR R.2016.5, adult male, HNUE VL.2015.131, adult female, and HNUE VL.2015.132, adult female, collected on 18 August 2015, the same data as the holotype

Diagnosis The new species can be distinguished from other members of the genus Cyrtodactylus from Indochina by a combination of the following characters: medium size (SVL up to 103 mm); internasal single; dorsal tubercles in 10–13 irregular rows; ventral scale rows 41–45; lateral skin folds present, without interspersed

1 C bichnganae

(KT004372)

–

2 C bobrovi

(KT004367-8)

16.3 –

3 C cf martini

(KF929537)

15.8 16.9-17.1 –

4 C huongsonensis

(KX430034)

14.5 15.8 16.0 –

5 C otai

(KT00370-1)

16.0 3.8 17.8 15.4 –

6 C puhuensis

(KF929529)

18.9 7.3–7.5 17.8 18.3 7.4 –

7 Cyrtodactylus

soni sp nov

(KX430032-3)

13.4–13.9 16.7–16.9 16.4–16.7 5.0–5.5 16.1–16.4 19.1–19.5 –

8 C spelaeus

(KP199947-8)

15.2–15.5 9.7–10.0 15.0–15.4 16.5–16.9 11.0–11.3 11.3–11.7 15.4–16.1 –

9 C vilaphongi

(KJ817434-5)

15.7 9.3 15.5 15.2 9.4 10.4 15.7–16.1 11.7–12.0 –

10 C wayakonei

(KJ817438/

KP199950)

14.8 16.6–16.8 6.7–6.9 16.6–16.9 18.1–18.4 18.2–18.4 17.2–17.7 16.1–16.5 15.8–16.2 –

tubercles; precloacal pores 6 or 7 in males, 7 or 8 pitted scales in females, in a continuous row; femoral pores 6–8

on each side in males, separated by 8–11 poreless scales from precloacal pore series; enlarged femoral scales present; postcloacal spurs 2 or 3; subcaudal scales transversely enlarged; lamellae under toe IV 18–22; dorsal pattern consisting of a dark nuchal loop, a continuous or partly interrupted neck band, and five or six in part irregular transverse body bands between limb insertions

FIGURE 1 Phylogram based on the Bayesian analysis Number above and below branches are MP/ML bootstrap values and Bayesian posterior probabilities (>50%), respectively Asterisk represents 100% value

Description of holotype Adult male, snout-vent length (SVL) 89.5 mm; body elongate (AG/SVL 0.44); head distinct from neck, elongate, depressed (HL/SVL 0.28, HW/HL 0.71, HH/HL 0.44); loreal region concave; snout long (SE/HL 0.44), round anteriorly, longer than diameter of orbit (OD/SE 0.54); snout scales small, round, granular; eye large (OD/HL 0.24), pupils vertical, spinous ciliaries 32; ear oval shaped, small (ED/HL 0.08); rostral wider than high with a medial suture, bordered by first supralabial, nostril, and supranasal on each side; supranasals separated from each other by two small scales; nares round, surrounded by supranasal, rostral, first supralabial, and three postnasals; mental triangular, slightly wider than rostral; postmentals two, enlarged, in broad contact posteriorly, bordered by mental anteriorly, first infralabial laterally, and an enlarged chin scale posteriorly; supralabials 10/10; infralabials 9/9

Dorsal scales granular; dorsal tubercles round, conical, present on occipital region and back, each surrounded

by 9 or 10 granular scales; ventral scales smooth, medial scales 2 or 3 times larger than dorsal scales, round, subimbricate, largest posteriorly, in 41 longitudinal rows at midbody; lateral skin folds distinct without tubercles; gular region with homogeneous smooth scales; 186 ventral scales between mental and cloacal slit; precloacal groove absent; enlarged femoral scales present; precloacal pores 6, femoral pores 6 on each side, in distal scale portion of enlarged femoral scales, separated by 8 poreless scales from precloacal pore series

Fore and hind limbs moderately slender (ForeaL/SVL 0.17, CrusL/SVL 0.2); forelimbs dorsally covered by few slightly developed tubercles; hind limb dorsally covered by distinctly developed tubercles; fingers and toes without distinct webbing; each claw bordered by two scales; subdigital lamellae: finger I 11 (including 2 basally

broadened lamellae), finger II 14 (4), finger III 15 (4), finger IV 16 (4), finger V 16 (5), toe I 11 (2), toe II 14 (4), toe III 17 (5), toe IV 18 (6), toe V 19 (7)

Tail regenerated (TaL 70.6 mm); postcloacal spurs 2/2; dorsal tail base with tubercles; subcaudals distinctly enlarged

Coloration in life Ground color light brownish grey; dorsal surface of head with irregular dark markings, largest at occiput; a dark postocular streak, edged in yellowish white, in contact with nuchal loop; neck with a dark transverse band; dorsum with five distinct dark transverse bands between limb insertions, edged by yellowish tubercles; upper surfaces of limbs with dark bands and reticulations; dorsal surface of the regenerated tail with indistinct transverse bands; gular region cream with indistinct grey marbling; venter cream; ventral surface of the regenerated tail dark grey with yellow marbling

Morphological comparisons We compared the new species with its congeners from Vietnam and neighbouring countries in mainland Indochina, including Laos, Cambodia, and Thailand based on the examination

of specimens (see Appendix) and data obtained from the literature (Bauer et al 2002, 2003, 2010; David et al

2004, 2011; Geissler et al 2009; Hoang et al 2007; Kunya et al 2014, 2015; Luu et al 2011, 2014, 2015, 2016a, 2016b, 2016c; Nazarov et al 2008, 2012, 2014; Ngo 2011, 2013; Ngo & Grismer 2010; Ngo & Chan 2011; Nguyen et al 2010, 2015; Nguyen et al 2013, 2014; Panitvong et al 2014 ; Pauwels & Sumontha 2014; Pauwels

et al 2013, 2014a, 2014b, 2016; Phung et al 2014; Schneider et al 2011, 2014 a, 2014b; Smith 1921; Sumontha et

al 2015; Ziegler et al 2010, 2013)

Cyrtodactylus soni sp nov has distinctly enlarged subcaudals, which are only slightly or not enlarged in the following species: C bidoupimontis Nazarov, Poyarkov, Orlov, Phung, Nguyen, Hoang & Ziegler, C buchardi David, Teyni & Ohler, C bugiamapensis Nazarov, Poyarkov, Orlov, Phung, Nguyen, Hoang & Ziegler, C cattienensis Geissler, Nazarov, Orlov, Böhme, Phung, Nguyen & Ziegler, C cryptus Heidrich, Rösler, Vu, Böhme

& Ziegler, C cucdongensis Schneider, Phung, Le, Nguyen & Ziegler, C huynhi Ngo & Bauer, C irregularis (Smith), C otai Nguyen, Le, Pham, Ngo, Hoang, Pham & Ziegler, C phuocbinhensis Nguyen, Le, Tran, Orlov, Lathrop, Macculloch, Le, Jin, Nguyen, Nguyen, Hoang, Che, Murphy & Zhang, C pseudoquadrivirgatus Rösler, Nguyen, Vu, Ngo & Ziegler, C quadrivirgatus Taylor, C ranongensis Sumontha, Pauwels, Panitvong, Kunya & Grismer, C taynguyenensis Nguyen, Le, Tran, Orlov, Lathrop, Macculloch, Le, Jin, Nguyen, Nguyen, Hoang, Che, Murphy & Zhang, C thuongae Phung, van Schingen, Ziegler & Nguyen, C vilaphongi Schneider, Nguyen, Le, Nophaseud, Bonkowski & Ziegler, and C ziegleri Nazarov, Orlov, Nguyen & Ho

Cyrtodactylus soni sp nov has enlarged femoral scales which are absent in C angularis (Smith), C badenensis Nguyen, Orlov & Darevsky, C bobrovi Nguyen, Le, Pham, Ngo, Hoang, Pham & Ziegler, C buchardi,

C chauquangensis Hoang, Orlov, Ananjeva, Johns, Hoang & Dau, C cryptus, C grismeri Ngo, C nigriocularis Nguyen, Orlov & Darevsky, C otai, C pageli Schneider, Nguyen, Schmitz, Kingsada, Auer & Ziegler, C pseudoquadrivirgatus, C sumonthai Bauer, Pauwels & Chanhome, C taynguyenensis, C vilaphongi, and C wayakonei Nguyen, Kingsada, Rösler, Auer & Ziegler

Cyrtodactylus soni sp nov has more femoral and precloacal pores in males (6–7+6–7+6–8) than the following species: C angularis (3), C condorensis (Smith) (0–4), C kunyai Pauwels, Sumontha, Keeratikiat & Phanamphon (5+3+6), C martini (4), C nigriocularis (0–2), C oldhami (1–4), C pageli (4), C phetchaburiensis Pauwels, Sumontha & Bauer (0+5+0), C quadrivirgatus (4), C sumonthai (2), C sanook Pauwels, Sumontha, Latinne & Grismer (3 or 4), C sayiok Panitvong, Sumontha, Tunprasert & Pauwels (0+5+0), C takouensis Ngo & Bauer (3 or 4), and absent in C badenensis, C cucphuongensis, C eisenmanae Ngo, C grismeri, and C ranongensis

Cyrtodactylus soni sp nov has more femoral and precloacal pores (or pitted scales) in females (6–8+7–8+5–6) than the following species: C angularis (3), C cucdongensis (4–6), C dumnuii Bauer, Kunya, Sumontha, Niyomwan, Pauwels, Chanhome & Kunya (0+0–7+0), C irregularis (0–6), C pageli (4), C quadrivirgatus (4); femoral and precloacal pores (or pitted scales) are absent in the females of C auribalteatus Sumontha, Panitvong

& Deein, C badenensis, C bidoupimontis, C bobrovi, C buchardi, C caovansungi Orlov, Nguyen, Nazarov, Ananjeva & Nguyen, C cattienensis, C condorensis, C cryptus, C eisenmanae, C grismeri, C interdigitalis Ulber, C jarujini Ulber, C martini, C multiporus Nazarov, Poyarkov, Orlov, Nguyen, Milto, Martynov, Konstantinov & Chulisov, C nigriocularis, C otai, C phuocbinhensis, C sanook, C soudthichaki Luu, Calame, Nguyen, Bonkowski & Ziegler, C spelaeus Nazarov, Poyarkov, Orlov, Nguyen, Milto, Martynov, Konstantinov & Chulisov, C sumonthai, C takouensis, C taynguyenensis, C thuongae, C thirakhupti, C vilaphongi, and C yangbayensis Ngo & Chan

FIGURE 2 The male holotype (HNUE VL.2015.78) of Cyrtodactylus soni sp nov in life (A: Dorsal view, B: Ventral view) Photo D T Le

FIGURE 3 Cloacal (A) and femoral (B) regions of the holotype (HNUE VL.2015.78) of Cyrtodactylus soni sp nov in preservative Photo D T Le

FIGURE 4 Female paratype (IEBR R.2016.4) of Cyrtodactylus soni sp nov in life: A) Dorsal view and B) Ventral view Photo D T Le

TABLE 2 Measurements (in mm) and scalation of Cyrtodactylus soni sp nov from Ninh Binh Province, Vietnam (M = male, F = female, * = regenerated or broken tail, min = minimum, max = maximum, other abbreviations defined in the text)

HNUE

VL.2015.78

IEBR A.2016.5

IEBR A.2016.4

HNUE VL.2015.94

HNUE VL.2015.131

HNUE VL.2015.132

Min–Max (n=6)

PP 6 7 7 (pitted scales) 8 (pitted scales) 7 (pitted scales) 7 (pitted scales) 6–8

NSF

NST

FIGURE 5 Map showing the type locality of Cyrtodactylus soni sp nov (red circle) in Van Long Wetland Nature Reserve, Ninh Binh Province, Vietnam

Cyrtodactylus soni sp nov differs from the following species by having fewer femoral and precloacal pores in males (6–7+6–7+6–8): C astrum Grismer, Wood, Quah, Anuar, Muin, Sumontha, Ahmad, Bauer, Wangkulangkul, Grismer & Pauwels (31–38), C bansocensis Luu, Nguyen, Le, Bonkowski & Ziegler (34), C calamei Luu, Bonkowski, Nguyen, Le, Schneider, Ngo & Ziegler (35–39), C chanhomeae Bauer, Sumontha & Pauwels (32), C darevskii Nazarov, Poyarkov, Orlov, Nguyen, Milto, Martynov, Konstantinov & Chulisov (38–44), C erythrops Bauer, Kunya, Sumontha, Niyomwan, Panitvong, Pauwels, Chanhome & Kunya (10+9+9), C hinnamnoensis Luu, Bonkowski, Nguyen, Le, Schneider, Ngo & Ziegler (36–44), C jaegeri Luu, Calame, Bonkowski, Nguyen & Ziegler (44), C jarujini (52–54), C khammouanensis Nazarov, Poyarkov, Orlov, Nguyen, Milto, Martynov, Konstantinov & Chulisov (40–44), C lekaguli Grismer, Wood, Quah, Anuar, Muin, Sumontha, Ahmad, Bauer, Wangkulangkul, Grismer & Pauwels (31–41), C lomyenensis Ngo & Pauwels (39–40), C multiporus (58–60), C phongnhakebangensis Ziegler, Rösler, Herrmann & Vu (32–42), C rufford Luu, Calame, Nguyen, Le, Bonkowski

& Ziegler (42–43), C sommerladi Luu, Bonkowski, Nguyen, Le, Schneider, Ngo & Ziegler (20–26), and C soudthichaki (29)

Cyrtodactylus soni sp nov has a dorsum with banded color pattern, which is blotched in C brevipalmatus (Smith), C buchardi, C bugiamapensis, C erythrops, C irregularis, C jarujini, C phetchaburiensis, C phuocbinhensis, C pseudoquadrivirgatus, C taynguyenensis, C teyniei David, Nguyen, Schneider & Ziegler, and

C thuongae; the dorsum is uniformly brown in C nigriocularis and striped in C oldhami, C quadrivirgatus, and

C ranongensis

Cyrtodactylus soni sp nov differs from C kingsadai Ziegler, Phung, Le & Nguyen by having fewer dorsal tubercle rows (10–13 vs 17–23 in C kingsadai)

Cyrtodactylus soni sp nov differs from the following species by having more ventral scale rows (41–45): C badenensis (25–29), C bichnganae (30–31), C buchardi (30), C chanhomeae (36–38), C chauquangensis (36– 38), C doisuthep Kunya, Panmongkol, Pauwels, Sumontha, Meewasana, Bunkhwamdi & Dangsri (29–35), C erythrops (28), C grismeri (33–38), C inthanon Kunya, Sumontha, Panitvong, Dongkumfu, Sirisamphan & Pauwels (29–34), C jaegeri (31–32), C jarujini (32–38), C khammouanensis (32–38), C khelangensis Pauwels,