Nanorana yunnanensis ( Anderson 1879 )

Thongproh, Prapaiporn, Chunskul, Jidapa, Makchai, Sunchai, Cota, Michael, Safoowong, Mongkol, Duengkae, Prateep, Duangjai, Sutee, Thitichayaporn, Somsak, Chuaynkern, Yodchaiy & Chuaynkern, Chantip, 2023, The identity of Nanorana yunnanensis (Anderson, 1879) from Thailand, with a description of its tadpole (Anura, Dicroglossidae), Zootaxa 5263 (3), pp. 365-388 : 374-381

Nanorana yunnanensis ( Anderson 1879)

Rana yunnanensis Anderson 1879 ‘1878’: 839. Syntypes: BMNH 2 specimens (lost; not mentioned by Boulenger (1882); BMNH 1947.2.3.76 (lectotype of Rana phrynoides Boulenger 1917 ) designated neotype by Dubois (1987 ‘1986’). Type locality: ‘Hotha [= Husa], 5,000 feet above sea level’, Yunnan, China; neotype from Tongchuan Fu [= Dongchuan Shi], Yunnan, China. Huang et al. (2016) invalidly (Art. 74.5) designated a replacement neotype, CIBYN09060612, from ‘Husa (N24°47′, E97°89′), Longchuan County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China’ to avoid the name Rana yunnanensis becoming a senior synonym of Rana phrynoides Boulenger 1917 .

Rana (Paa) bourreti Dubois 1987 ‘1986’: 46. Holotype: MNHNP 1948.128 (= LZUH 3.59 ), by original designation. Type locality: ‘ Chapa [= Sa Pa], Vietnam, 22°20′N, 103°50′E’.

Material examined. Chiang Mai Province: Fang District; ‘ Doi Lang’ ( THNHM 16642 [female]), ‘ Border Patrol Police Company 334, Doi Pha Hom Pok National Park (20°07’57.6”N 99°09’30.2”E, msl 2051 m elev.)’ ( THNHM 30500–1 [males], THNHM 30502.1 –.2 [tadpoles]; Mae Ai District , ‘Doi Lang’ ( THNHM 13029–30 [males], THNHM 20920 [juvenile], THNHM 26897 [male], THNHM 25480-25483 [tadpoles]. The morphometric data of adult and juvenile specimens are shown in Table 6.

Diagnosis. N. yunnanensis is characterised by a combination of the following characters: (1) body stout; (2) SVL of adult males 86.8 ± 3.04 mm (n = 5), adult female 74.8 mm (n = 1); (3) snout dorsally round; (4) tympanum visible; (5) supratympanic fold present; (6) dorsum with longitudinal short fold, small wart present within fold; (7) nuptial spines on chest of male present; (8) spiny nuptial pad present on prepollex and fingers I-III; (9) tip of tongue round, not bifid; (10) vomerine teeth in short, oblique group; (11) inner and outer metacarpal tubercles present; (12) outer metacarpal heart-shaped; (13) inner metatarsal tubercle present; (14) outer metatarsal tubercle absent; (15) dermal flap on outer edge of fifth toe present; (16) toe webbing full.

Description of five adult males. The following description refers to voucher no. THNHM 30500 (field no. PT 02794; Figs. 2–3 ), THNHM 30501 (field no. PT 02803), THNHM 13029–30, and THNHM 26897.

Frog of large size (SVL 83.5–85.9 mm), body stout, head of large size, oval in dorsal view; wider than long (HW 33.5–34.6 mm; HL 30.7–34.7 mm; MN 26.6–28.3 mm; MFE 22.8–23.4 mm; MBE 13.7–16.5 mm), flat above. Snout oval in dorsal view, elliptical in lateral view, slightly protruding, its length (SL 9.2–10.9 mm) longer than horizontal diameter of eye (EL 8.1–9.1 mm). Canthus rostralis rounded, loreal region concave, rather vertical in cross-section. Interorbital space flat, wider (IUE 5.1–6.5 mm) than upper eyelid (UEW 6.3–7.3 mm) and wider than internarial distance (IN 6.3–7.5 mm); distance between fronts of eyes (IFE 12.0– 12.9 mm) 1.6-fold greater than distance between backs of eyes (IBE 20.0– 22.7 mm). Nostril oval, directed posterior ventrally, with flap of skin laterally, closer to eye (EN 4.0– 4.8 mm) than to tip of snout (NS 4.0– 5.7 mm). Pupil elliptical, horizontal. Tympanum (TYD 3.6–5.0 mm) distinct, oblique vertical oval, 56.8% of eye diameter; tympanum-eye diameter (TYE 5.1–7.1 mm) 123.9% of tympanum diameter. Pineal ocellus present, in middle point between anterior borders of eyelids. Vomerine ridge present, bearing numerous small teeth (n = 3 in each side); with an angle of 40° to body axis, closer to choanae than to each other, as long as distance between them. Tongue large, cordate; not emarginated, bearing no median lingual process. Tooth-like projections on lower jaw absent.

Forelimbs short and strong; forearm (FLL 19.0–21.0 mm) longer than hand (HAL 20.9–22.0 mm); enlarged. Fingers I, II, and IV short and strong; finger III (TFL 10.2–11.3 mm) long and strong. Relative lengths of fingers: II <I <IV <III. Tips of fingers rounded, not enlarged without lateroventral grooves, first and second narrow compared to finger width, third and fourth slightly wide compared to finger width (fd1 1.1–1.3 mm, fw1 1.3–1.5 mm; fd2 1.0– 1.4 mm, fw2 1.0– 1.8 mm; fd3 1.0– 1.4 mm, fw3 1.0– 1.8 mm; fd4 1.0– 1.5 mm, fw4 1.0– 1.6 mm). Fingers with dermal fringe on inner and outer sides of finger I, and inner sides of fingers II and III; webbing on fingers absent. Subarticular tubercles prominent rounded, single in fingers I and II, double in fingers III and IV. Prepollex distinct, elliptical; single distinct palmar tubercle, elliptical; supernumerary tubercles absent.

Hindlimbs medium long, strong; heels articulate when limbs are folded at right angles to body; tibia 2.8- fold longer (TL 42.1–43.9 mm) than wide (TW 15.0– 16.7 mm), longer than thigh (FL 39.6–44.9 mm) and longer than distance from base of internal metatarsal tubercle to tip of toe IV (FOL 41.8–46.9 mm). Toes medium long and strong, toe IV (FTL 23.3–26.5 mm) 2.6-fold greater than distance from base of tarsus to tip of toe IV (TFOL 61.0– 67.2 mm). Relative lengths of toes: I <II <V <III <IV. Tips of all toes rounded, not enlarged; without lateroventral grooves, rather wide compared to toe width (td1 1.0– 1.6 mm, tw1 1.1–1.2 mm; td2 1.3–1.7 mm, tw2 1.0– 1.2 mm; td3 1.3–1.6 mm, tw3 1.1–1.5 mm; td4 1.2–1.4 mm, tw4 1.1–1.4 mm; td5 1.0– 1.4 mm, tw5 1.2–1.3 mm). Webbing present, full webbing: I 1½-1 II 1-1½ III 1½-1½ IV 2½-1 V (WTF 10.6–12.8 mm, WFF 8.3–10.3 mm; WI 9.7–10.1 mm, WII 7.5–8.9 mm; MTTF 23.5–24.1 mm, MTFF 23.3–25.1 mm, TFTF 8.3–13.4 mm, FFTF 15.6–17.2. mm). Dermal fringe along toe V present: from tip of toe beyond first subarticular tubercle. Subarticular tubercle prominent, oval, simple, all present. Inner metatarsal tubercle distinct, elliptical, its length (IMT 5.6–6.3 mm) 1.6-fold greater than the length of toe I (ITL 10.1–11.8 mm). Tarsal folds present. Outer metatarsal tubercle absent; supernumerary tubercles absent; tarsal tubercle absent.

Skin of snout smooth; between eye area and side of head glandular; anterior and posterior parts of back and upper part of flank glandular warts with black horny spines; lower part of flank glandular without black horny spines. Dorsolateral folds absent; supratympanic fold distinct, prominent; parotoid glands absent; cephalic ridges absent; co-ossified skin absent. Dorsal parts of forelimb, thigh, and tarsus glandular with black spines. Throat, chest, belly, and ventral portion of anterior and posterior parts of thighs smooth. Macroglands: distinct rictal gland in posterior corner of mouth; supra-brachial gland absent; humeral gland absent.

Colour in preservative. Dorsal parts of head and back greyish with dark blotches; upper and lower parts of flank greyish with dark blotches; loreal region greyish with dark stripe running from nostril to anterior eye; tympanic region grey with dark band at posterior edge; tympanum dark grey; upper lip greyish with four dark bands. Dorsal part of thigh greyish with five dark bands; dorsal part of leg greyish with four dark bands; dorsal part of foot greyish with 11 dark bands; posterior part of thigh dark brown blotch. Throat, margin of throat, chest, belly, and ventral portion of thigh creamy mixed with greyish reticulate; webbing dark grey.

Colour in life. Dorsal parts of head and back brownish with black blotches; upper and lower parts of flank brownish with black blotches; loreal region light brown with black stripe running from nostril to anterior eye; tympanic region light brown with black band at posterior edge; tympanum dark brown; upper lip light brown with four black bands; dorsal part of thigh light brown with five black bands; dorsal part of leg light brown with four black bands; dorsal part of foot light brown with 11 dark bands; posterior part of thigh dark brown blotch; throat, margin of throat, chest, belly, and ventral portion of thigh creamy mixed with light brown reticulate; webbing dark brown.

Male secondary characters. Nuptial spines present on prepollex, fingers I and II, chest, and margin of throat; size of spines large; black spines; rounded group on chest. Vocal sacs present, indistinct on throat; pair of oval openings at posterior of jaw. Other secondary sexual characters: enlargement of forearm.

Description of N. yunnanensis tadpole. The following description refers to specimen number THNHM 30502.1 (field no. PT2799.1; Gosner stage 35; Fig. 4 )

Body in dorsal, ventral, and lateral views ovate (BL 15.2 mm, BW 8.5 mm, BH 5.8 mm); snout ovate in lateral view, round in dorsal and ventral views; eyes of moderate size (ED 1.8 mm), not bulging, not visible in ventral view, in dorsolateral position, dorsolateral directed, located at approximately one-quarter of body length; nares opening ovate, small (ND 0.8 mm), bulging rim, lacking flap in anterolateral position, anterolaterally directed, closer to snout than eye (NP 3.0 mm, RN 2.6 mm); single spiracle, sinistral, tubular, moderately long, attached to body wall except margin, located at midpoint of body length, visible in lateral view; spiracle opening with rounded shape, positioned below body axis, in dorsoposterior direction (SS 9.6 mm). Tail musculature moderate (TMH 4.2 mm, TMW 3.8 mm), not reaching to tail tip, gradually tapering; tail fins of moderate size (UF 2.4 mm, LF 1.8 mm), upper fin not extending onto body (SU 13.6 mm), lower fin not extending onto body, reaching its maximum height at 4/6 of tail; tail tip round; vent tube of large size, rectangular in shape, linked to ventral tail fin, vent tube opening directed to right side of lower fin. Oral disc moderate size (ODW 3.5 mm, AL 1.0 mm, PL 1.1 mm), emarginate laterally; upper labium with marginal papillae, wide gap; lower labium with marginal papillae in three continuous rows, tip of papillae pointed; submarginal papillae present; upper jaw sheath black, broad, marginally serrated, medial projection absent; lower jaw sheath black, broad, medial concaved, marginal serrated; labial teeth black, cuspate, single row arrangement; LTRF: 1:3+3/1+1:2. Colour in life dark grey in dorsal and lateral views, light grey in ventral view; tail muscle cream, with irregular black dots; tail fin light cream, translucent, with irregular black dots; intestinal coiled, indistinct in ventral view; hindlimb cream. Colour in alcohol greyish brown in dorsal and lateral views, grey in ventral view; tail muscle light brown, with irregular black dots; tail fin light brown, translucent, with irregular black dots; intestinal coiled, indistinct in ventral view; hindlimb cream.

Internal oral anatomy of N. yunnanensis tadpole. The following description refers to specimen number THNHM 30502.2 (field no. PT 02799.2; Gosner stage 35).

Buccal roof triangular, longer than wide. Prenarial arena with papillae, triangle-shaped; prenarial arena protrusion present, on central position. Prenarial papillae present, rising on anterior narial wall. Choanae elliptical, slightly oblique; narial valve projection long, lanceolate, directed anteromedially; postnarial arena with papillae; medial ridge flat trapezoid. Buccal roof arena same length and wide, with papillae; lateral roof papillae present. Glandular zone not evident. Dorsal velum smooth margin, without papillae ( Fig. 5A, C–D ).

Buccal floor triangular, slightly expanded. Infralabial papillae three pairs, smooth edge, arising at base of both sides of lower labium, directed medially; tongue anlage conspicuous, depressed in dorsal view; two long lingual papillae in central position, oriented anteriorly. Buccal floor arena oval, with papillae. Buccal pockets elliptical, transverse, slightly curved backward, closer to tongue anlage than medial end of central velum; ventral velum without spicular support, with marginal projections; branchial baskets oblique, much wider than long; bearing three evident filter cavities ( Fig. 5B, E–F ).

Natural history. Adult males and tadpoles were found in a small temporary pond in the tropical evergreen forest of Doi Pha Hom Pok National Park ( Fig. 6 ). N. yunnanensis tadpoles inhabited the same pond as another tadpole species, presumably Rhacophorus or Zhangixalus .

Distribution. Thailand: Chiang Mai Province [Doi Lang, Mae Ai (this study), Doi Lang, Fang (this study)]; China: Yunnan Province, Sichuan Province, Guizhou Province ( Zhang et al. 2010); Vietnam: Lao Cai Province [Sa Pa vicinity ( Zhang et al. 2010)], Son La Province [Ngoc Chien, Xim Vang ( Pham & Nguyen 2018)].

Conservation Status. N. yunnanensis has been designated as EN (endangered) by the IUCN (2021). The Office of Natural Resources and Environmental Policy and Planning (2017) of Thailand has designated this species as VU (vulnerable).

Figures

FIGURE 2. Live adult male N. yunnanensis (PT 02794). (A) General aspect, (B) ventral view.

FIGURE 3. Adult male specimen of N. yunnanensis (PT 02794). (A) Dorsal view of body, (B) ventral view of body, (C) lateral side of head, (D) ventral view of hand, (E) ventral view of foot.

FIGURE 4. External morphology of N. yunnanensis tadpole.(A–C) Specimen no. PT 02799.1 (Gosner stage 35)in lateral, dorsal, and ventral views; (D) specimen no. THNHM 25480 (Gosner stage 30); (E) oral disc of tadpole (specimen no. PT02799.2), (F) upper labial tooth row (specimen no. PT02799.2), (G) upper jaw sheath (specimen no. PT02799.2).

FIGURE 5. Buccal cavity of N. yunnanensis tadpole (PT02799.2). (A) Buccal roof, (B) buccal floor, (C) prenarial arena protrusion, (D) narial valve projection, (E) lingual papillae, (F) buccal floor arena papillae. 1 = upper labium, 2 = prenarial arena protrusion, 3 = choanae, 4 = prenarial papillae, 5 = narial valve projection, 6 = median ridge, 7 = buccal roof arena, 8 = lower labium, 9 = infralabial papillae, 10 = lingual papillae, 11 = buccal floor arena papillae, 12 = filter rows.

FIGURE 6. Distribution map and habitat of N.yunnanensis in Thailand. (A) Map showing current distribution of N. yunnanensis in Thailand. Red circle indicates locality where this species is found in Thailand. Map was generated using SimpleMappr (www. simplemappr.net). (B) Habitat of N. yunnanensis at Doi Pha Hom Pok National Park, Chiang Mai, Thailand.