Limnonectes kiziriani, Pham & Le & Ngo & Ziegler & Nguyen, 2018

Pham, Cuong The, Le, Minh Duc, Ngo, Hanh Thi, Ziegler, Thomas & Nguyen, Truong Quang, 2018, A new species of Limnonectes (Amphibia: Anura: Dicroglossidae) from Vietnam, Zootaxa 4508 (1), pp. 115-130 : 117-127

Limnonectes kiziriani sp. nov.

( Figs. 2–5 )

Holotype: IEBR 4343 (Field no. AL 2017.18), adult male, collected by C. T. Pham, T. V. Nguyen and B. V. Ngo on 3 April 2017 in the evergreen forest near Sao La Ranger Station 16 0 06.720’N, 107 0 27.195’E, at an elevation of 485 m asl.), Sao La Nature Reserve , A Luoi District, Thua Thien Hue Province, Vietnam.

Paratypes: Four specimens collected from the evergreen forest of Kon Ka Kinh National Park, Gia Lai Province, Vietnam: One adult male, VNMN 0 7035 (Field no. NQT 2011.28 ), collected by T.Q. Nguyen and C.V. Hoang on 2 June 2011 (14 o 25.087’N, 108 o 25.042’E, at an elevation of 1135 m asl.) and one adult female, VNMN 0 7036 (Field no. NQT 2011.158 ) collected by T.Q. Nguyen and C.V. Hoang on 8 June 2011 (14 0 12.855’N, 108 0 18.929’E, at an elevation of 958 m asl.); one adult male, IEBR 4344 (Field no. KKK 2012.30 ), collected by C.T. Pham and C.V. Hoang on 23 February 2012 (14 0 25.452’N, 108 0 22.595’E, at an elevation of 1103 m asl.) and one adult female, IEBR 4345 (Field no. KKK 2012.152 ), collected by C.T. Pham and C.V. Hoang on 28 February 2012 (14 o 24.976’N, 108 o 23.099’E, at an elevation of 1200 m asl.) .

Five specimens collected from the evergreen forest of Dong Chau Proposed Nature Reserve, Le Thuy District, Quang Binh Province, Vietnam: Two adult males, IEBR 4346 (Field no. QB 2015.206) and ZFMK 101286 (Field no. QB 2015.235), collected by T.Q. Nguyen and C.T. Pham on 21 March 2015 (16 0 58.880’N, 106 0 36.571’E, at an elevation of 359 m asl.); one adult female, ZFMK 101287 (Field no. QB 2015.300), collected by C.T. Pham and T.T. Nguyen on 26 July 2015 (16 0 57.042’N, 106 0 37.294’E, at an elevation of 470 m asl.); and one adult male, IEBR 4347 (Field no. QB 2015.338) and one adult female, VNMN 0 7037 (Field no. QB 2015.354), collected by C.T. Pham and C.V. Hoang on 30 October 2015 (16 0 58.883’N, 106 0 36.527’E, at an elevation of 377 m asl.).

Ten specimens collected from the evergreen forest of Sao La Nature Reserve, A Luoi District, Thua Thien Hue Province, Vietnam: Seven adult males, IEBR 4348–4352 (Field Nos. AL 2017.86, 113, 115, 116, 119), VNMN 0 7038 (Field no. AL 2017.121), ZFMK 101288 (Field no. AL 2017. 123) and three adult females, IEBR 4371 (Field no. AL 2017.114), VNMN 0 7039 (Field no. AL 2017.117), ZFMK 101289 (Field no. AL 2017. 118), collected by C.T. Pham, T.V. Nguyen and B.V. Ngo on 6 April 2017 (16 0 04.306’N, 107 0 29.062’E, at an elevation of 750 m asl.).

Diagnosis: Analysis of molecular and morphological data (including the presence of fang-like odontoid processes on the lower jaw and sexual dimorphism, with males larger than females and hypertrophy of the head in males, Emerson et al. 2000), found the new species to be nested within Limnonectes . Limnonectes kiziriani sp. nov. is distinguishable from its congeners by a combination of the following morphological characters: (1) SVL 47.5– 60.9 mm in males, 42.3–51.1 mm in females; (2) males with moderately enlarged head (HL/SVL 0.48); (3) head slightly longer than wide; (4) vomerine teeth present; (5) external vocal sacs absent; (6) rostral length short (RL/ SVL 0.14 in males, 0.15 in females); (7) tympanum invisible; (8) dorsal surface of head, body and flanks smooth; (9) dorsal surface of tibia and foot distinctly tuberculate, covered with moderately dense, small, low tubercles; (10) supratympanic fold present; (11) dorsolateral fold absent; (12) toes webbed to posterior of terminal phalanx; (13) in life, dorsum light yellowish with brown marking; throat and chest white with brown markings; ventral surface of abdomen white or white with brown markings.

Description of holotype: Adult male (IEBR 4343); SVL 55.3 mm; habitus robust with enlarged head (HL/ SVL 0.47, HW/SVL 0.46); head slightly longer than wide (HL 26.2 mm, HW 25.5 mm); snout round anteriorly in dorsal view, projecting beyond lower jaw; nostril lateral, closer to eye than to snout tip (NS 4.3 mm, EN 3.7 mm); canthus rostralis indistinct; loreal region oblique and slightly concave; rostral length greater than eye diameter (RL 7.8 mm, ED 6.6 mm); interorbital distance wider than internarial distance and upper eyelid width (IOD 5.7 mm, IND 4.9 mm, UEW 3.2 mm); tympanum invisible; vomerine teeth in two oblique ridges; tongue cordiform, notched posteriorly; lower jaw with two tooth-like, odontoid processes robust with very sharp tips; external vocal sac absent.

Forelimbs: Arms short; upper arm lengh (UAL) 8.9 mm, forearm length (FAL) 24.5 mm; relative finger lengths: I<II<IV<III; fingers free of webbing; dermal ridge on sides of fingers absent; tips of fingers blunt, not expanded; subarticular tubercles prominent, round, formula 1, 1, 2, 2; inner metatarsal tubercle oval, elongate; outer metatarsal tubercle small; finger I with nuptial pad, composed of minute spines on inner edge.

Hind limbs: Tibia length shorter than thigh length (FeL 25.8 mm, TbL 24.5 mm), approximately 2.5 times longer than wide (TbW 9.5 mm); tips of toes blunt, slightly rounded; relative length of toes: I<II<V<III<IV; toes webbed to posterior of terminal phalanx; dermal ridge on outer sides of toes I and V; subarticular tubercles prominent, elongate, formula 1, 1, 2, 3, 2; inner metatarsal tubercle elongate; outer metatarsal tubercle absent; tibio-tarsal articulation reaching to middle of eye.

TABLE 1. Uncorrected (“p”) distance matrix showing percentage pairwise genetic divergence (16S) between the new and closely related Limnonectes species.

Skin texture in life: Dorsal surface of head, body and flanks smooth; small tubercles on upper eyelid; supratympanic fold distinct, extending from eye to angle of jaw; dorsolateral fold absent; small tubercles around cloaca; dorsal surface of limbs and thighs smooth; dorsal surface of tibia and foot distinctly tuberculate, covered with moderately dense, small, low tubercles; throat, chest, belly and ventral surface of thighs smooth.

Coloration in life: Iris coppery orange in upper half and grayish white in lower half; head with a pale yellow bar in anterior interorbital region and a dark brown bar in posterior interorbital region; dorsum and upper part of flanks pale with yellowish brown marking; lower part of flanks yellowish white; lips with dark bars; supratympanic fold dark brown; dorsal surface of limbs yellowish brown with dark crossbars; ventral surface of limbs, throat, chest, and abdomen white; toe webbing brown.

Coloration in preservative: Dorsum and upper part of flanks pale brown with dark brown marking; lower part of flanks white with small brown spots; lips with dark bars; head with a narrow dark brown bar in anterior interorbital region; supratympanic fold dark brown; dorsal surface of limbs pale brown with dark crossbars; ventral surface of limbs, throat, chest white with brown marking; abdomen white; toe webbing brown.

Variation and sexual dimorphism: Measurements and morphological characters of the type series are provided in Table 2. Two specimens (ZFMK 101288, 101289) have a yellow middorsal stripe. Males are larger females (SVL 54.1± 4.1 mm, n = 13 vs. 46.8± 3.3 mm, n = 7). Males have a larger head than females (HL/SVL 0.48 vs. 0.42, HW/SVL 0.43 vs. 0.40). The male specimens have a nuptial pad on finger I. The males have robust fanglike odontoid processes, which are less pronounced in the females.

Etymology. The specific epithet is a patronymic noun for David Kizirian (American Museum of Natural History) and his penchant for small brown biodiversity. Common name suggestions include Kizirian’s Frog (English) and Ếch nhẽo ki-zi-ri-an (Vietnamese).

Ecological notes. Specimens were found between 19:00 and 23:00 h in rocky streams ( Fig. 6a ). They were found in the water or on the ground of stream banks. The surrounding habitat was secondary forest of large, medium and small hardwoods mixed with shrubs and vines. Air temperature at the sites was 18.4–28.3 o C and relative humidity was 73–89%. Advertisement calls and tadpoles of the species have not been recorded during our field surveys. The females collected in June 2011 from Gia Lai Province, in July and in October 2015 from Quang Binh Province, and in April 2017 from Thua Thien Hue Province contained yellow eggs of varying sizes. Other amphibian species found at the sites included: Limnonectes poilani (Bourret) , Quasipaa verrucospinosa (Bourret) , Amolops spinapectoralis Inger, Orlov & Darevsky , Odorrana morafkai (Bain, Lathrop, Murphy, Orlov & Ho) , Gracixalus supercornutus (Orlov, Ho & Nguyen) , Kurixalus bisacculus (Taylor) , Rhacophorus annamensis (Smith) , and R. exechopygus Inger, Orlov & Darevsky.

Distribution. Limnonectes kiziriani sp. nov. is currently known only from Quang Binh, Thua Thien Hue, and Gia Lai provinces, central Vietnam ( Fig. 7 ). Data obtained from GenBank showed that this species was also recorded from Laos and Phong Dien Nature Reserve in Thua Thien Hue Province, Vietnam ( McLeod 2010; Suwannapoom et al. 2016; see Discussion below).

Comparisons. We compared the new species with its congeners from Vietnam and neighboring countries in mainland Indochina, including Laos, Cambodia, Thailand, and China.

Limnonectes kiziriani sp. nov. differs from L. fragilis (Liu & Hu) by having a greater ratio of HL/SVL in males (HL/SVL=0.48, n=13 vs. HL/SVL=0.44, n= 6 in L. fragilis ), tibia length shorter than thigh length (vs. tibia length longer than thigh length in L. fragilis ), dorsal surface of body and flanks smooth (vs. with tubercles in L. fragilis ), and males with nuptial pad on finger I (vs. absent in males of L. fragilis ); from L. bannaensis Ye, Fei & Jiang by having a smaller size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 74.9 mm in males, 60.8 mm in females in L. bannaensis ), tips of toes blunt (vs. tips of toes expanded into discs in L. bannaensis ), and dorsal surface of tibia and foot with tubercles (vs. smooth in L. bannaensis ), males with nuptial pad on finger I (vs. males with nuptial pad on fingers I and II in L. bannaensis ); from L. dabanus (Smith) by having the head longer than wide (vs. broader than long in L. dabanus ), the absence of caruncle on head in males (vs. present in L. dabanus ), tympanum invisible (vs. distinct in L. dabanus ), toes fully webbed (vs. webbing formula I0–1/ 3II 0–1/ 4III 0– 1IV 1– 0V in L. dabanus ); from L. fujianensis Ye & Fei by having a greater ratio of HL/SVL in males (HL/SVL=0.48, n=13 vs. HL/SVL=0.44, n= 20 in L. fujianensis ), dorsal surface of body and flanks smooth (vs. with tubercles in L. fujianensis ), and males with nuptial pad on finger I (vs. nuptial pad on fingers I and II in L. fujianensis ); from L. gyldenstolpei (Andersson) by having the head longer than wide (vs. broader than long in L. gyldenstolpei ), the absence of caruncle on head in males (vs. present in L. gyldenstolpei ), tympanum invisible (vs. distinct in L. gyldenstolpei ), toes fully webbed (vs. webbing formula I0–3/ 4II 0– 1III 1/ 4–1IV11 /2–0V in L. gyldenstolpei ); from L. hascheanus (Stoliczka) by having a larger size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 18.8– 25.4 mm in males, 20.5–25.0 mm in females of L. hascheanus ), dorsolateral folds absent (vs. present in L. hascheanus ), males with nuptial pad on finger I (vs. absent in males of L. hascheanus ), tympanum invisible (vs. distinct in L. hascheanus ); from L. isanensis McLeod, Kelly & Barley by having a smaller size in males (SVL 47.5–60.9 mm vs. 71.5 mm in L. isanensis ), nostril closer to eye than to tip of snout (vs. nostril closer to tip of snout than eye in L. isanensis ), males with nuptial pad on finger I (vs. nuptial pad on fingers I and II in L. isanensis ); from L. jarujini Matsui, Panha, Khonsue & Kuraishi by having a smaller size in males (SVL 47.5–60.9 mm vs. 72.9 in L. jarujini ), nostril closer to eye than to tip of snout (vs. nostril midway between tip of snout and eye in L. jarujini ), length of fingers I<II (vs. fingers II=I in L. jarujini ), tibio-tarsal articulation extends to middle of eye (vs. reaching to point far posterior to eye in L. jarujini ), toes fully webbed (vs. toes webbed to middle of terminal phalanx in L. jarujini ); from L. khammonensis (Smith) by having a larger size (SVL 42.3–51.1 mm in females vs. 37 mm in L. khammonensis ), tympanum invisible (vs. distinct in L. khammonensis ); from L. kohchangae (Smith) by having a larger size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 31.0– 42.2 mm in males, 32.2–41.5 mm in females of L. kohchangae ), head longer than wide (vs. broader than long in L. kohchangae ), and tympanum invisible (vs. distinct in L. kohchangae ); from L. limborgi (Sclater) by having a larger size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 29.8–37.6 mm in males, 28.0– 36.2 mm in females of L. limborgi ), dorsolateral folds absent (vs. present in L. limborgi ), males with nuptial pad on finger I (vs. absent in males of L. limborgi ), tympanum invisible (vs. distinct in L. limborgi ); from L. liui (Yang) by having a larger size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 32–38.5 in males, 32.7 in female of L. liui ), tympanum invisible (vs. distinct in L. liui ), belly white or white with brown markings (vs. pale yellow in L. liui ), and dorsolateral fold absent (vs. present in L. liui ); from L. longchuanensis by having a smaller size in males (SVL 47.5–60.9 mm vs. 75.5 in L. longchuanensis ), dorsal surface of body and flanks smooth (vs. with tubercles in L. longchuanensis ), males with nuptial pad on finger I (vs. nuptial pad on fingers I and II in L. longchuanensis ); from L. lauhachindai Aowphol, Rujirawan, Taksinum, Chuaynkern & Stuart by having a larger size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 30.5–42.0 mm in males, 32.9–37.9 mm in females in L. lauhachindai ), the absence of caruncle on head (vs. present in L. lauhachindai ), tympanum invisible (vs. distinct in L. lauhachindai ), and males with nuptial pad on finger I (vs. absent in L. lauhachindai ); from L. macrognathus (Boulenger) by having a larger size (SVL 47.5–60.9 mm in males vs. 43.2–44.8 mm in males of L. macrognathus ) and the absence of caruncle on head (vs. present in L. macrognathus ), tympanum invisible (vs. distinct in L. macrognathus ); from L. megastomias McLeod by having a smaller size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 80.2 mm in males, 74.0 with nuptial pad on fingers I and II in L. megastomias ), dorsal surface of tibia and foot with tubercles (vs. smooth in L. megastomias ); from L. nguyenorum by having a smaller ratio of HL/SVL (0.48 in males, 0.42 in females vs. 0.42–0.43 in males, 0.39– 0.39 in females in L. nguyenorum ), nostril closer to eye than to tip of snout (vs. nostril closer to tip of snout than to eye in L. nguyenorum ), tibia shorter than thigh (vs. tibia longer than thigh in L. nguyenorum ), males with nuptial pad on finger I (vs. nuptial pad on fingers I and II in L. nguyenorum ); from L. poilani (Bourret) by having a smaller size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 81.1–99.5 mm in males, 69.5–95.3 mm in females of L. poilani ), rostral length greater than eye diameter (vs. eye diameter greater than rostral length of L. poilani ), tympanum invisible (vs. distinct in L. poilani ), ventral surface of limbs and abdomen white or white and brown markings (vs. yellow in L. poilani ); from L. quangninhensis Pham, Le, Nguyen, Ziegler, Wu & Nguyen by having tympanum invisible (vs. distinct in L. quangninhensis ), tibia shorter than thigh (vs. tibia longer than thigh in L. quangninhensis ), toes fully webbed (vs. webbing formula I0–0II0–1/ 3III 0–1/ 3IV 1/2–0V in L. quangninhensis ), and dorsal surface of tibia and foot with distinctly tubercles (vs. small tubercles in L. quangninhensis ); from L. taylori Matsui, Panha, Khonsue & Kuraishi by having a smaller size (SVL 47.5–60.9 mm in males, 42.3–51.1 mm in females vs. 66.0 mm in males, 51.9 mm in females of L. taylori ), nostril closer to eye than to tip of snout (vs. nostril closer to tip of snout than to eye in L. taylori ), dorsal surface of body and flanks smooth (vs. dorsal surface of body and flanks with tubercles in L. taylori ).

Within the focal geographic area, there are currently no nomina considered as synonyms of species of Limnonectes which would need to be considered as possible earlier available names for the new species, except for the following: L. toumanoffi (Bourret) was synonymized with L. dabanus by Stuart et al. (2006), but the new species described herein differs from L. toumanoffi by the absence of caruncle on head in males and invisible tympanum. L. sinensis (Peter) was synonymized with L. fujianensis by Jang-Liaw & Chou (2011), but the new species can be distinguished from the latter by having dorsal surface of body and flanks smooth and males with nuptial pad on finger I only. L. pileata (Boulenger) was synonymized with L. gyldenstolpei by Ohler & Dubois (1999), but the new species can be distinguished from the latter by the absence of caruncle on head in males and invisible tympanum.

Figures

FIGURE 2. Dorsolateral view (A) and ventral view (B) of the holotype (IEBR 4343, male) of Limnonectes kiziriani sp. nov. in life.

FIGURE 3. Dorsolateral view (A) and ventral view (B) of the holotype (IEBR 4343, male) of Limnonectes kiziriani sp. nov. in preservative.

FIGURE 4. Right foot (A), right hand (B), and underside of finger I (C) of the holotype (IEBR 4343) of Limnonectes kiziriani sp. nov.

FIGURE 5. Lateral view of the head (A) and dorsal view of the tibia (B) of the holotype (IEBR 3907) of Limnonectes kiziriani sp. nov.

FIGURE 6. Habitat of Limnonectes kiziriani sp. nov. (A) and threat to the habitat of the new species in Thua Thien Hue Province, Vietnam: timber logging (B) and road construction (C).

FIGURE 7. Map showing the known distribution of Limnonectes kiziriani sp. nov. in Vietnam: 1) Dong Chau Proposed Nature Reserve in Quang Binh Province, 2) Sao La Nature Reserve in Thua Thien Hue Province (type locality), and 3) Kon Ka Kinh National Park in Gia Lai Province.