Gracixalus guangdongensis, Wang & Zeng & Lyu & Liu & Wang, 2018

Wang, Jian, Zeng, Zhao-Chi, Lyu, Zhi-Tong, Liu, Zu-Yao & Wang, Ying-Yong, 2018, Description of a new species of Gracixalus (Amphibia: Anura: Rhacophoridae) from Guangdong Province, southeastern China, Zootaxa 4420 (2), pp. 251-269 : 257-265

Gracixalus guangdongensis sp. nov.

Fig. 3

Holotype. SYS a005724, adult male, collected on 13 April 2017 by Jian Wang (JW), Zhao-Chi Zeng (ZCZ) and Dian-Cheng Yang (DCY) from DWL (22°17′31.27″ N, 111°12′50.42″E; 1600 m a.s.l.) in Maoming City, Guangdong Province, China.

Paratypes. Two adult females were collected from the same locality as the holotype: SYS a004686, collected by Ying-Yong Wang (YYW), Zhi-Tong Lyu (ZTL), JW and ZCZ on 16 April 2016 ; SYS a004698, collected by JW, ZCZ, Can-Rong Lin ( CRL) and Chun-Peng Guo (CPG) on 28 June 2016. Eight adult males: SYS a004672–4673 , SYS a004685, 4687–4689, collected by Hai-Long He (HLH), Run-Lin Li (RLL) and ZTL on 16 April 2016 from the same locality as the holotype ; SYS a004983/ CIB106882 , collected by JW, ZTL and ZCZ on 28 June 2016, and SYS a005241, collected by JW on 16 August 2016 from DWL (22°15′57.58″ N, 111°11′18.10″ E; 1000 m a.s.l.). Three adult males: SYS a004902–4904, collected by YYW and ZTL on 5 June 2016 from MNK (23°38′16.40″ N, 113°50′49.40″ E; 600 m a.s.l.) in Huizhou City, Guangdong Province, China . Five adult males: SYS a005750– 5751, collected by YYW and ZTL on 20 April 2017 and SYS a005773–5775, collected by JW, ZTL and HLH on 5 May 2017, all from NNR (24°55′53.82″ N, 113°01′19.66″ E; 1000 m a.s.l.) in Shaoguan City , Guangdong Province, China .

Referred specimen. A single juvenile of the species ( SYS a004671), collected at the same locality as the holotype by ZCZ on 15 April 2016.

Etymology. The specific epithet “ guangdongensis ” refers to the distribution of this species, Guangdong Province, China. We propose the common English name “ Guangdong Tree Frog”, Chinese name “Guang Dong Xian Shu Wa (ḞṪḤṄḂ)” for this species.

Diagnosis. Gracixalus guangdongensis sp. nov. is assigned to genus Gracixalus based upon our preliminary mtDNA phylogenetic analyses and the following morphological characters: the presence of an intercalary cartilage between the terminal and penultimate phalanges of digits, tips of digits expanded into large discs bearing circum marginal grooves, vomerine teeth absent, horizontal pupil, tibia length greater than four times width, distance between nostrils less than or equal to between eyes, rictal gland connected to the mouth ( Delorme et al. 2005; Rowley et al. 2014), and the back bearing dark X-or inverted V-shape ( Fei et al. 2009).

Gracixalus guangdongensis sp. nov. can be distinguished from its congeners by a combination of the following morphological characters: (1) relatively small body size (SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females); (2) upper eyelid and dorsum lacking spines; (3) supratympanic fold and tympanum distinct; (4) dorsal and lateral surface rough, sparsely scattered with tubercles; (5) ventral skin granular; (6) tibiotarsal projection absent; (7) toe-webbing moderately developed, finger webbing rudimentary; (8) heels slightly overlapping when flexed hindlimbs are held at right angles to the body axis; (9) brown to beige above, with an inverse Y-shaped dark brown marking extendeing from the interorbital region to the centre of the dorsum; (10) males with a single subgular vocal sac and protruding nuptial pads with minute granules on the dorsal surface of the base of first finger.

Description of holotype. Adult male, dorsoventrally compressed; head width almost equal to head length (HDW:HDL 1.01); snout triangularly pointed in dorsal view, projecting beyond margin of the lower jaw; canthus rostralis distinct and rounded; loreal region oblique and concave; nostrils oval, significantly protuberant, closer to tip of snout than to the eye; interorbital region flat, interorbital distance slightly broader than internasal distance (IOD:IND 1.03); eye large, horizontal diameter slightly smaller than snout length (ED:SL 0.83); pupil horizontal; tympanum distinct, tympanic rim weakly developed; tympanum diameter smaller than half of eye diameter (TYD:ED 0.41); supratympanic fold distinct, extending from the posterior corner of the eye above insertion of arm; vomerine teeth absent; tongue deeply notched behind; a single subgular vocal sac present.

Forelimb moderately robust; forearm and hand relatively long (FAHL:SVL 0.48), hand significantly longer than forearm (HAL:SVL 0.46); fingers dorsoventrally compressed, webbing rudimentary, with narrow lateral fringes on outer edge of all fingers; relative finger length I <II <IV <III; tips of all fingers with well expanded discs with distinct transverse circum-marginal grooves; disc of third finger large, its width significantly broader than width of distal phalanx of finger III (FDW III:FPW III 2.1), and slightly larger than tympanum diameter (FDW III:TYD 1.24); subarticular tubercles markedly elevated and prominent, rounded, one on finger I and II, two on finger III and IV; supernumerary tubercles present; prepollex distinct, oval; a nuptial pad with barely visible minute granules present on the first finger; nuptial pad on dorsolateral surface of first finger strongly dilated, extending from hand base to level of subarticular tubercle; several tubercles on palmar, the outer palmar tubercle largest.

Hindlimb long (TIBL:SVL 0.47, FTL:SVL 0.69); tibio-tarsal articulation reaching the middle of the eye when hindlimb adpressed along the side of the body; heels slightly overlapping when the flexed hindlimbs are held at right angles to the body axis; toes moderately long, relative toe lengths I <II <III <V <IV; tips of toes with expanded discs with distinct transverse circum-marginal grooves; discs of toes smaller than those of fingers; subarticular tubercles distinct, rounded, one on finger I and II, two on finger III and V, three on finger IV; webbing formula I (2), (2½) II (1½), (3) III (2), (3) IV (3), (2) V; sole smooth with small tubercles; inner metatarsal tubercle elongated, ellipsoid; outer metatarsal tubercle absent; inner tarsal fold absent.

Skin of dorsal surface of head, body and limbs rough, sparsely scattered with tubercles; temporal region and corner of the mouth densely covered with large tubercles; pectoral and subgular skin smooth with barely visible granules; belly granular; anterior surface of hindlimbs smooth, posterior and ventral surface of hindlimbs with tubercles, relatively smooth; tarsal fold absent.

Measurements of holotype (in mm). SVL 30.2, HDL 10.7, HDW 10.8, SL 5.1, IND 3.5, IOD 3.6, ED 4.2, TYD 1.7, TED 0.8, HAL 9.8, FAHL 14.6, TIBL 14.1, FTL 20.7, FDW III 2.1, FPW III 1.0, TDW IV 1.9, TPW IV 1.2.

Coloration of holotype in life. Dorsal surface brown, with an inverse Y-shaped, dark-brown marking, starting at the interorbital region, bifurcating into two branches on shoulder, extending posteriorly; dorsal surface of fore- and hindlimbs with dark brown transverse bands; several faint, small, black blotches scattered on ventrolateral region of flanks and on ventral surface; ventral surface of hindlimbs, throat and chest creamy white, surface of belly and forelimbs light brown; iris brown, pupil black.

Coloration of holotype in preservative. Color of dorsal surface dark grey; ventral surface of head and body greyish white; the Y-shaped marking and transverse black bands, blotches on the ventrolateral region of the flanks and the ventral surface are greyish black, and more distinct than in life.

Variation. The external morphology and color pattern of all paratypes corresponds to that of the holotype, except for the following characters: background color of dorsal surface of head, body and limbs is beige in SYS a004671 (the single juvenile), SYS a004672 and SYS a004686 (vs. brown in holotype SYS a005724); adult males collected in the breeding season (SYS a004672–4673, 4685, 4687–4689, 4983, 4902–4904, 5724, 5750–5751, 5773–5775) possess nuptial pads on the dorsal surface of first finger, but the single specimen collected in the nonbreading season (SYS a005241) has barely visible nuptial pads; specimens from MNK and NNR have a smaller body size than specimens from DWL, measurement and body proportions of the type series specimens of G. guangdongensis sp. nov. are given in Table 3.

Comparisons. Gracixalus guangdongensis sp. nov. was assigned with strong node supporting values (0.82 in BI and 86% in ML) to Clade I in our phylogenetic tree containing G. jinxiuensis , G. jinggangensis , G. sapaensis , G. nonggangensis and G. waza . The new species differs from G. jinxiuensis by the relatively larger body size, SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females (vs. 24.2–26.3 mm in males, 28–29.2 mm in females of G. jinxiuensis ), more developed webbing (formula of webbing of the fourth toes in (3) IV (3)) (vs. (3½) IV (3½) in G. jinxiuensis ), ventral surface of hand, foot and palm smooth with sparse small tubercles (vs. rough with dense large tubercles in G. jinxiuensis ), tibio-tarsal articulation reaching the middle of the eye (vs. reaching the posterior corner of eye the in G. jinxiuensis ), and having heels overlapping when the flexed hindlimbs are held at right angles to the body axis (vs. just meeting in G. jinxiuensis ); from G. jinggangensis by the relatively larger body size in females, SVL 34.9–35.4 mm (vs. 31.6 mm in G. jinggangensis ), presence of nuptial pad on the first finger of male (vs. on first and second fingers of male G. jinggangensis ), and heels overlapping when the flexed hindlimbs are held at right angles to the body axis (vs. just meeting in G. jinggangensis ); from G. sapaensis by the presence of a distinct tympanum (vs. indistinct in G. sapaensis ), presence of a single vocal sac (vs. paired vocal sac in in G. sapaensis ), brown to beige background color of the dorsal surface of head, body and limbs in life (vs. greyish to reddish brown in G. sapaensis ), creamy white to light brown ventral surface (vs. venter pink in G. sapaensis ), and rough dorsal surface (vs. nearly smooth in G. sapaensis ); from G. nonggangensis by the more developed webbing (formula of webbing of the fourth toes in (3) IV (3)) (vs. (3½) IV (3½) in G. nonggangensis ), ventral surface of hand, foot and palm smooth with sparse small tubercles (vs. rough with dense large tubercles in G. nonggangensis ), presence of nuptial pad on the first finger of males (vs. absent in G. nonggangensis ), presence of rudimentary finger webbing (vs. finger webbing absent in G. nonggangensis ), tibio-tarsal articulation reaching the middle of the eye (vs. reaching the tip of the snout in G. nonggangensis ), and brown to beige background color of the dorsal surface of the head, body and limbs in life (vs. yellowish olive in G. nonggangensis ); from G. waza by the relatively small body size in adult females, SVL 34.9–35.4 mm (vs. 37.6 mm in G. waza ), brown to beige background color of the dorsal surface of the head, body and limbs in life (vs. greyish green to moss-green in G. waza ), and rough dorsal skin with tubercles (vs. nearly smooth dorsal skin in G. waza ).

Gracixalus guangdongensis sp. nov. can also be easily distinguished from the six members of Clade II ( Fig 2 ). It differs from G. seesom by the relatively larger body size, SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females (vs. 21.6–23 mm in males and 23.2–25.4 mm in female G. seesom ), presence of nuptial pads on the first finger of males (vs. absence in male G. seesom ), and rough dorsal skin with tubercles (vs. nearly smooth dorsal skin in G. seesom ); from G. quangi by the relatively larger body size, SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females (vs. 21.4–22.9 mm in males and 26.8–27.3 mm in females of G. quangi ), absence of spines on the upper eyelid (vs. presence in G. quangi ), absence of a tibiotarsal projection (vs. presence in G. quangi ), and brown to beige background color of the dorsal surface of the head, body and limbs in life (vs. greenish to brownish green in G. quangi ); from G. gracilipes by the brown to beige background color of dorsal surface of head, body and limbs and the presence of inverse Y-shaped dark brown marking on back in life (vs. transparent green with Xshaped brown markings in G. gracilipes ), absence of a white patch under the eye to the tympanum (vs. presence in G. gracilipes ), and absence of spines on upper eyelid (vs. presence in G. gracilipes ); from G. supercornutus by the brown to beige background color of the dorsal surface (vs. yellowish green in G. supercornutus ), the absence of a white patch extending from under the eye to the tympanum (present in G. supercornutus ), absence of spines on upper eyelid (vs. present in G. supercornutus ), absence of a tibiotarsal projection (vs. present in G. supercornutus ); from G. quyeti by having distinct supratympanic fold (vs. indistinct in G. quyeti ), brown to beige background color of dorsal surface of head, body and limbs (vs. brown to moss-green in G. quyeti ); from G. lumarius by the relatively smaller body size, SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females (vs. 38.9–41.6 mm in males and 36.3 mm in female of G. lumarius ), distinct tympanum and supratympanic fold (vs. indistinct in G. lumarius ), skin on dorsal surface of head, body rough, sparsely scattered with brown tubercles (vs. dorsum with distinctive dense network of white conical tubercles in adult males in G. lumarius ), venter creamy white to greyish white (vs. venter pink in G. lumarius ), single vocal sac in males (vs. a pair of vocal sacs in G. lumarius ).

The new species also differs from the two congeners for which comparative molecular material is not available. The new species differs from Gracixalus megdogensis by the presence of rudimentary finger webbing (vs. absence of finger webbing in G. megdogensis ), tibio-tarsal articulation reaching the middle of the eye (vs. reaching the anterior corner of the eye in G. megdogensis ), rough dorsal skin with tubercles (vs. smooth dorsal skin in G. megdogensis ), and brown to beige background color of dorsal surface of head, body and limbs in life (vs. green in G. megdogensis ); from G. carinensis by the relatively smaller body size in females, SVL 34.9–35.4 mm (vs. 38 mm in G. carinensis ), more developed webbing (webbing formula of the fourth toe (3) IV (3)) (vs. webbing formula (2½) IV (2) in G. carinensis ), and snout length slightly longer than diameter of eye (SL> ED) (vs. snout length shorter than diameter of eye (SL <ED) in G. carinensis ).

Gracixalus guangdongensis sp. nov. further differs from Kurixalus ananjevae (Matsui & Orlov) , which is morphologically and likely molecularly similar to the Gracixalus species of Clade II (i.e. Clade I in this study) according to Rowley et al. 2011, by the smaller body size in females, SVL 34.9–35.4 mm (vs. 43.0 mm in female K. ananjevae ), dark grey dorsum in preservation (vs. pinkish gray in preservation in K. ananjevae ), snout length slightly longer than diameter of eye (SL> ED) (vs. snout length equal to or shorter than diameter of eye (SL ≤ ED) in K. ananjevae ), and more developed webbing (webbing formula of the fourth toes is (3) IV (3)) (vs. (3) IV (2½) in K. ananjevae ).

Gracixalus guangdongensis sp. nov. further differs from the small- and medium-sized rhacophorids occurred in southern China and northern Vietnam: the new species differs from Liuixalus calcarius Milto, Poyarkov, Orlov & Nguyen , L. feii Yang, Rao & Wang , L. jinxiuensis Li, Mo, Jiang, Xie & Jiang , L. hainanus (Liu and Wu) , L. ocellatus (Liu & Hu) , L. romeri (Smith) , L. shiwandashan Li, Mo, Jiang, Xie & Jiang , Raorchestes longchuanensis (Yang and Li) and Ra. menglaensis (Kou) by the significantly larger body size, SVL 26.1–34.7 mm in adult males, 34.9–35.4 mm in adult females (vs. SVL values not-overlaping and less than 21.0 mm in males and 22.0 mm in females) and the more developed webbing on toes (vs. very poorly-developed webbing on the toes); from Philautus abditus Inger, Orlov & Darevsky by the presence of nuptial pads in males and a distinct tympanum (vs. nuptial pads absent and tympanum completely hidden under skin); from Buergeria oxycephala (Boulenger) by the significantly smaller body size and the absence of vomerine teeth (vs. SVL 34–38 in males and 60–68 in females, vomerine teeth present); from Thelerdema albopunctatum (Liu & Hu), T. annae Nguyen, Pham, Nguyen, Ngo & Ziegler, T. bicolor (Bourret), T. corticale (Boulenger), T. gordoni Taylor, T. lateriticum Bain, Nguyen & Doan and T. rhododiscus (Liu &Hu) by the absence of skin ridges and large warts on dorum (vs. presence of irregular skin ridges and large warts on dorsum in T. bicolor, T. corticale, T. gordoni; and presence of irregular skin ridges on dorsum in T. albopunctatum and T. rhododiscus), presence of a single vocal sac (vs. paired vocal sac in T. albopunctatum, and absent in T. annae, T. lateriticum and T. rhododiscus), and the absence of vomerine teeth (vs. vomerine teeth present in T. bicolor and T. corticale); from Kurixalus bisacculus (Taylor) by the presence of a single vocal sac in males and fingers with rudiment of web (vs. paired vocal sac in males and fingers without web), from K. lenquanensis Yu, Wang, Hou, Rao & Yang and K. odontotarsus (Ye and Fei) by the absence of vomerine teeth and absence of conical tubercles on posterolateral surface of forearms and tibia (vs. vomerine teeth present, distinct conical tubercles on posterolateral surface of forearms and tibia present); from Chiromantis doriae (Boulenger) by having rough dorsal skin with tubercles and a “Y-shaped” marking on the back (vs. smooth dorsal skin with granules and five longitudinal stripes on the back); from Feihyla fuhua Fei, Ye & Jiang , F. palpebralis (Smith) and F. vittata (Boulenger) by the single vocal sac in males (vs. paired vocal sac in males); from Polypedates braueri (Vogt) , Po. impresus Yang , Po. megacephalus Hallowell and Po. mutus (Smith) by the absence of vomerine teeth and presence of rudiment of web on fingers (vs. vomerine teeth present and webbing on fingers absent); from Rhacophorus dorsoviridis Bourret , Rh. hoanglienensis Orlov, Lathrop, Murphy & Ho , Rh. laoshan Mo, Jiang, Xie & Ohler , Rh. larissae Ostroshabov, Orlov & Nguyen , Rh. leucofasciatus Liu & Hu , Rh. minimus Rao, Wilkinson & Liu , Rh. nigropunctatus Liu, Hu & Yan , Rh. pinglongensis Mo, Chen, Liao & Zhou , Rh. puerensis (He) , Rh. rhodopus Liu & Hu , Rh. yaoshanensis Liu & Hu and Rh. yinggelingensis Chou, Lau , and Chan by the absence of vomerine teeth (vs. vomerine teeth present), rudimentary webbing on the fingers (vs. welldeveloped webbing on the fingers in Rh. leucofasciatus and Rh. rhodopus ), heels overlapping when the flexed hindlimbs are held at right angles to the body axis (vs. heels not meeting in Rh. dorsoviridis and Rh. nigropunctatus ; heels just meeting in Rh. yaoshanensis and Rh. yinggelingensis ), presence of nuptial pads on the first finger (vs. presence of nuptial pads on first and second fingers in Rh. puerensis ), absence of tibiotarsal projection (vs. tibiotarsal projection present in Rh. hoanglienensis and Rh. larissae ).

Advertisement calls. The advertisement calls of Gracixalus guangdongensis sp. nov., are compared to all species nested in Clade I of our phylogenetic analyses for which acoustic data is available, G. jinggangensis and G. nonggangensis . All advertisement calls of the four male G. guangdongensis sp. nov. recorded (two from DWL, one from MNK and one from NNR) are similar in structure, composed of an introductory note followed by a single ‘click’ note ( Fig. 4 , A–D). The call of the new species therefore differs from that of G. jinggangensis (which has an introductory note followed by two or three click notes, Fig. 4E ) and G. nonggangensis (which has an introductory note followed by 39–71 click notes, Fig. 4F ). Moreover, the call of G. guangdongensis sp. nov. differs from G. jinggangensis in the duration of the introductory note (0.40 ± 0.05 vs. 0.20 ± 0.02 in two click notes form and 0.16 ± 0.01 in three click notes form). Measurements of the advertisement calls of the three species are listed in Table 4.

Distribution. Currently, Gracixalus guangdongensis sp. nov. is known from Dawuling Forestry Station in western Guangdong, Mount Nankun in central Guangdong, and Nanling Nature Reserve in northern Guangdong. The unique advertisement call of the species is also heard in adjacent Mangshan Nature Reserve (MNR) in southeastern Hunan Province ( Fig. 1 ).

Ecology and behavior. The new species appears to be restricted to bamboo forest with evergreen broad-leaf forest ( Fig. 5 ), at elevations of approximately 600 m at MNK, 1000–1600 m at DWL, and 1000–1200 m at NNR and MNR. The single juvenile (SYS a004671) from DWL was collected from a shrub ( Litsea sp.) adjacent to a stream, 50 m away from bamboo forest.

According to our observations, the main breeding season of the DWL population begins in April and lasts at least three months, as males with distinct nuptial pads and calling males were observed at these times. A small number of males were also heard calling in August. The female collected in April (SYS a004686) has a distinct fat body and visible fallopian tubes, while a female collected in June (SYS a004984) has barely visible fallopian tubes. The male holotype was found calling on a bamboo stem about 1.7 m above the ground on 9 April 2017 at DWL ( Fig. 3A ), at the same time, two individuals were found sitting on another bamboo pole (male above and female below) about 2 m above the ground ( Fig. 6A ). Eggs with jelly coating were discovered after splitting apparently air-tight bamboo joints on 28 June 2016. On 17 April 2017 at DWL, eggs were found on the walls of an openended bamboo joint half full of water where a female individual was found inside the night before ( Fig. 6 , B & C). Eggs and embryos were also found in another water-filled bamboo joint the next day ( Fig. 6D ). Other details of the ecology and behavior of the new species remains unknown.

Figures

FIGURE 1. Map showing the type localities of four Gracixalus species from southeastern China. Squares: localities of G. guangdongensis sp. nov.: (1): Dawuling forest station, Maoming City, Guangdong Province; (2): Mount Nankun, Huizhou City, Guangdong Province; (3): Nanling Nature Reserve, Shaoguan City, Guangdong Province and the adjacent Mangshan Nature Reserve, Yizhang City, Hunan Province. Circles: type localities of other three Gracixalus species: (4): Mt. Jinggang, Jinggangshan City, Jiangxi Province; (5): Mt. Dayao, Jinxiu County, Guangxi Province; (6): Nonggang Nature Reserve, Chongzuo City, Guangxi Province.

FIGURE 2. Bayesian inference tree of Gracixalus guangdongensis sp. nov. and the known congeners of the genus (except G. carinensis and G. medogensis) derived from partial DNA sequences of the mitochondrial 16S rRNA gene with Bayesian posterior probabilities (BPP>70% retained) and maximum-likelihood bootstrap values (1000 replicates; BS>60 retained), respectively.

FIGURE 3. The adult male holotype of Gracixalus guangdongensis sp. nov. (SYS a005724) in life. A: general aspect; B: lateral view; C: ventral view; D: showing nuptial pads with minute granules on the dorsal surface of the first finger; E: ventral view of hand; D: ventral view of foot.

FIGURE 4. Waveforms and spectrograms of the advertisement calls of Gracixalus guangdongensis sp. nov., G. jinggangensis and G. nonggangensis, respectively. A & B: The advertisement call of Gracixalus guangdongensis sp. nov. from Dawuling Forest Station; C: The advertisement call of Gracixalus guangdongensis sp. nov. from Mount Nankun; D: The advertisement call of Gracixalus guangdongensis sp. nov. from Nanling Nature Reserve. E: The advertisement call of Gracixalus jinggangensis, E1: Call with 3 notes, E2: Call with 4 notes; F: The advertisement call of Gracixalus nonggangensis.

FIGURE 5. Habitat of Gracixalus guangdongensis sp. nov. in Dawuling Forest Station, Maoming City, Guangdong Province, China.

FIGURE 6. Ecology and behavior of Gracixalus guangdongensis sp. nov.: A: mating behavior and sexual dimorphism: a pair on the bamboo stem prior to amplexus, the male (with distinctly visible nuptial pad on the first finger) above and female (with a larger body size than the male and without nuptial pads) below; B & C: a female sitting in an open bamboo joint, filled with numerous eggs and embryos; D: different clutches of eggs in different stages of developments on the wall of an open bamboo joint.