Rana tabaca, BAIN & TRUONG, 2004

BAIN, RAOUL H. & TRUONG, NGUYEN QUANG, 2004, Herpetofaunal Diversity of Ha Giang Province in Northeastern Vietnam, with Descriptions of Two New Species, American Museum Novitates 3453, pp. 1-43 : 17-24

Rana tabaca , new species

Figures 6C, D , 10–13

HOLOTYPE: AMNH 163923/IEBR 68 (AMNH Field Series 15217), a mature male from a stream near the Hmong Village of Khau Ria , in Du Gia commune, Yen Minh District, below Mount Muong Cha, Ha Giang Province, Vietnam (22°54̍27̎N, 105°13̍59̎E, ca. 800 m elevation) found on 28 April 2000 by Q.T. Nguyen and R.H. Bain.

PARATYPES: Four mature males (AMNH 163914/IEBR 64; AMNH 163915; AMNH 163916/IEBR 65; AMNH 163917/IEBR 66) and one gravid female (AMNH 163920) collected with holotype by Q.T. Nguyen and R.H. Bain. A subadult female (AMNH 163922/AMNH FS­15258) was also collect­ ed on the same stream as the holotype (above 900 m elevation) by Q.T. Nguyen and R.H. Bain. Two males (AMNH 163918, 163919) and one subadult female (AMNH 163921/ IEBR 67) were collected between 24 and 25 May 2000 from the Bac Trao River , near Tham Ve Village, below Mt. Tay Con Linh II District, Ha Giang Province, Vietnam (22°45̍39̎N, 104°52̍23̎E, 600 m) by R.H. Bain .

DIAGNOSIS: Rana tabaca is characterized by a combination of the following characters: SVL of males 52–60 mm (mean 55.60 mm), adult female 103 mm; upper lip spotted brown between tip of snout and eye, lip stripe golden, extends below eye to insertion of arm; dorsal skin shagreened, dorsolateral folds present on males and subadult females; dorsum varies from dark brown with greengold marbling to olive brown with red­brown spots; web full to disk on all toes except IV, webbing on IV full to distal subarticular tubercle, reaching disk as a fringe, postaxial fringe on V to proximal subarticular tubercles, continuing to the base of metatarsal as a thin ridge; no external metatarsal tubercle; males with paired gular pouches, nuptial spines absent; eggs not pigmented.

DESCRIPTION OF HOLOTYPE: AMNH 163923/IEBR 68, a mature male, SVL 53.40 mm, HDW:HDL 0.93, HDL:SVL 0.40; pupil broadly oval; snout short, rounded in dorsal view, bluntly rounded in profile, protruding beyond margin of lower jaw; eye very prominent, EYE:SNT 1.03; eyelid broader than interorbital distance; top of head flat; canthus rostralis rounded; loreal region concave; lip flared just anterior to orbit; nostril about three­fourths distance from eye to tip of snout; weak supratympanic fold straight posteroventrally from posterior corner of eye to distal portion of tympanum; tympanum round, distinctly visible, separated from eye by distance less than tympanum diameter, TMP:EYE 0.62; choanae ovoid; vomerine dentigerous processes prominent, posteromedial to choanae, each bearing numerous teeth; tongue cordiform, distinctly notched posteriorly, free for approximately two­thirds its length.

Forearms robust; fingers moderately short, slender, HND:SVL 0.21, relative lengths of fingers II ‹ I ‹ IV ‹ III, median callous pads to proximal tubercle on fingers II, III, IV, furrows on either edge of finger III and medial edge of II; disks on tips of fingers expanded (›2× base of phalange), relative pad size I = II ‹ IV ‹ III, pad width of finger III less than TMP, ventral circummarginal grooves present; terminal phalanges T­shaped; subarticular tubercles conical. Hindlimbs moderately robust; TIB:SVL 0.66; FTL:SVL 0.87; relative toe lengths I ‹ II ‹ III = V ‹ IV; inner

TABLE 3 Comparisons of Some Adult Southeast Asian Cascade Ranids tarsal fold absent; web full to base of toe disks, except toe IV, webbing on IV full to distal subarticular tubercle, reaching disk as a fringe, preaxial fringe on toe I and postaxial fringe on V to proximal subarticular tubercles, on V continuing to the base of metatarsal as a thin ridge; toes long, slender, with rounded triangular disks (›2× base of phalange), pad size of all toes equal to each oth­ er, smaller than those of fingers, each with ventral circummarginal grooves; subarticular tubercles prominent and conical; inner metatarsal tubercle ovoid, long; outer metatarsal tubercle absent.

Skin on dorsum shagreened, becoming more granular on flanks; venter and around anus smooth; dorsolateral folds present; anus unmodified, directed posteriorly, at upper level of thighs.

COLOR IN LIFE (in preservative): Dorsum dark brown with green­gold marbling (livid blue with light gray spots); snout spotted brown (dark brown on light brown); upper lip spotted brown (black) from tip of snout to anterior of eye, lip stripe gold from below eye to insertion of arm (white); iris entirely gold; dorsolateral stripe yellow (light gray); flanks brown (gray) with black and yellow network (dark gray and off­white); dorsal limbs brown (tan) with black spots and transverse bands (brown), fingers I, II tan (offwhite); posterior surface of thighs yellow with black marbling; webbing marbled white on dark brown (light gray on dark gray); venter iridescent gold­white (white), throat mottled brown to anterior third of belly (light brown on creamy white), light brown mottling on thigh.

MALE SECONDARY SEXUAL CHARACTERS: Greatly enlarged forearms and paired subgular vocal pouches; large white, velvety nuptial pad extends along base of finger I; nuptial spines absent.

MEASUREMENTS OF HOLOTYPE (in mm): SVL 53.40, SNT 8.20, HDL 21.44, HDW 19.98, EYE 8.48, IOD 4.90, TMP 5.34, HND 11.29, TIB 35.40, FTL 46.58.

VARIATION OF PARATYPES: Adults exhibit sexual dimorphism: females are larger (SVL female, 103.4 mm; males 53.62–59.38 mm, mean 56.43 mm); females with smaller HDL: HDW (1.10 for female; males 1.14–1.58, median 1.22); females with smaller TMP:

(B) arrows indicate furrows on preaxial side of fingers II, III; (C) foot. Scales equal 5 mm.

EYE (0.50 for female; males 0.62–0.70, mean 0.63); females with smaller EYE:SNT (0.74 in female; males 0.78–0.97, mean 0.85); females with no dorsolateral folds (present in males). Females have unpigment­ ed eggs. The xiphisternum of the adult female is large and deeply notched posteriorly. The subadult female from Du Gia (AMNH 163922) bears a strikingly resemblance to males: dorsolateral folds present and TMP: EYE is 0.63. Male paratypes all have prominent eyes (EYE:SNT 0.78–0.97, mean 0.85), but only the holotype has an eye that is larger than the snout. The supratympanic fold is more strongly developed and curved in paratypes than in the holotype. Dorsum varies from dark brown with various amounts of green­gold marbling to olive brown with redbrown spots (dark brown with light brown marbling in preservative). Cao Bo specimens (AMNH 163918, 163919, 16321) are brown with no green (dark brown in preservative); flanks sometimes with spots, rather than network; mottling on throat to upper one­third of the belly varies among paratypes from faint to very dark (as a network of light brown on creamy white in preservative). All Cao Bo specimens possess subcutaneous masses on each side of the dorsum just above the insertion of the leg (fig. 13).

MEASUREMENTS OF MALE PARATYPES (N = 6, AMNH 163914—163919; mean, ± standard deviation, range in parentheses): SVL 55.97 ± 3.13 (53.62–59.38), SNT 9.12 ± 0.46 (8.52–9.74), HDL 24.03 ± 2.66 (21.64– 26.58), HDW 19.42 ± 0.82 (18.40–20.26), EYE 7.88 ± 0.24 (7.64–8.26), IOD 4.90 ± 0.24 (4.50–5.08), TMP 5.25 ± 0.37 (4.71– 5.76), HND 12.82 ± 1.53 (11.00–15.63), TIB 33.72 ± 2.27 (30.8–36.64), FTL 44.79 ± 3.01 (42.00–48.74). median TIB:SVL 0.62 (0.52–0.68), median SNT:HDL 0.38 (0.33–0.45).

MEASUREMENTS OF FEMALE ADULT PARA­ TYPE (AMNH 163920): SVL 103.40, SNT 15.98, HDL 40.00, HDW 36.36, EYE 11.80, IOD 9.72, TMP 5.96, HND 28.16, FPL 2.88, TIB 68.66, FTL 86.52.

COMPARISONS: Rana tabaca superficially resembles several other Asian cascade ranids, but can be differentiated from them by a combination of characters. Rana tabaca has an upper lip that is spotted brown from tip of snout to anterior of eye, lip stripe gold from below eye to insertion of arm: Amolops chunganensis , Huia nasica , Rana archotaphus , R. chloronota , R. daorum , R. graminea , R. hosii , R. leporipes , R. livida (white lip stripe from tip of snout, snout not spotted); R. chalconota , R. exiliversabilis , R. hmongorum , R. iriodes , R. morafkai , and R. nasuta (yellow lip stripe from tip of snout, snout not spotted); R. hejiangensis and R. junlianensis (yellow lip stripe from tip of snout with brown lip bars); R. versabilis (yellowish­brown lip stripe, snout with white asperities); R. grahami , R. jingdongensis , and R. kwangwuensis (yellow­green marbling from tip of snout, some with brown marks); R. andersonii , R. bacboensis , R. hainanensis , R. margaretae , R. schmackeri , R. sinica , R. tiannanensis , and R. trankieni (no lip stripe). The postaxial fringe on toe V that extends to the base of the metatarsal as a thin ridge separates R. tabaca from Huia nasica , R. bacboensis , R. banaorum , R. chalconota , R. chloronota R. daorum , R. hosii , R. graminea , R. hmongorum , R. iriodes , R. margaretae , R. morafkai , R. megatympanum , and R. sinica (if present, fringe ends at the proximal subarticular tubercle); A. chunganensis , R. grahami , R. kwangwuensis (fringe ends at proximal subarticular tubercle or half­way to base of metatarsal); R. hejiangensis , R. sinica (no lateral fringe or ridge on toe V). Rana tabaca most closely resembles R. bacboensis , R. megatympanum , and R. tiannanensis . Rana tabaca further differs from R. bacboensis by its dorsolateral folds (absent in R. bacboensis ) and unpigmented eggs (completely melanic in R. bacboensis ). Rana tabaca further differs from R. tiannanensis by its shagreened dorsum (rough in R. tiannanensis ). Rana tabaca further differs from R. megatympanum by its slightly larger males ( R. tabaca SVL mean 55.60 mm, maximum 59.38 mm; 52.3 mm, maximum 55.2 mm for R. megatympanum ), and its more moderate TMP: EYE (0.59–0.79 [mean 0.66] in R. tabaca males, 0.96–1.54 [mean 1.20] for R. megatympanum ).

Character states for the condition of finger furrows and lateral fringes on the toes were obtained by direct observation of specimens (appendix 1) and from the original description of R. trankieni (Orlov et al., 2003) . Character information on R. exiliversabilis and R. nasuta is from Fei et al. (2001), on R. trankieni from Orlov et al. (2003), and on R. versabilis from Liu and Hu (1962). Refer to table 3 and Bain et al. (2003: table 12) for detailed comparisons of regional cascade ranids.

ETYMOLOGY: The specific name is derived from the Latin tabacum, meaning tobacco. The dark brown of R. tabaca is close to the color of thuoc lao, a tobacco common in northern Vietnam.

DISTRIBUTION: This species is currently known only from Ha Giang Province in northern Vietnam: Mt. Tay Con Linh II, Cao Bo Commune, Vi Xuyen District, and Mt. Muong Cha, Du Gia commune, Yen Minh District.

REMARKS: Males were calling a single, loud, high birdlike chirp. They were found on streamside rock ledges and low­lying foliage and on branches 1–3 m over the stream. A female was seen in a small crevice under rocks. Males and females easily scale the rocks among the cascades they inhabit. Tadpoles remain unknown.

RHACOPHORIDAE

Chirixalus gracilipes ( Bourret, 1937)

Figures 14 , 15

Philautus gracilipes Bourret, 1937 : ‘‘Chapa’’, Tonkin [ Vietnam].

Chirixalus gracilipes is known from the Hoang Lien Mountains in northwestern Vietnam ( Bourret, 1937) and southern Yunnan Province ( Fei, 1999), but this is the first record of it east of the Red River. These specimens match the original description exactly, however Bourret (1937) describes the hands as ‘‘less than two­thirds webbed’’, whereas we prefer to describe the fingers as fleshy with lateral flaps, but not webbing.

Calling males, gravid females, and several aerial clutches of eggs and larvae were found at 1700 m. Clutches were deposited on leaves overhanging forest pools, which varied from rocky to muddy bottomed. Clutches were found from ground level up to 4 m. One clutch was found on leaves, but directly in the pool. Clutch size varies from two to eight. Initial identification of eggs was based on proximity to calling males, as well as egg size and shape, visible through gravid females (fig. 14). Comparison of DNA sequence data confirmed that the eggs and larvae are conspecific with adult specimens of C. gracilipes (J. Faivovich, unpubl.). The right ovary of one female (AMNH 163900) holds more than 20 eggs (complete count not possible in order to keep specimen intact).

Eggs are creamy yellow with brown melanic pole, each encased in a gelatinous capsule that sticks the eggs to the leaf and each other (fig. 14). Eggs are between 2.5 and 2.8 mm in diameter, whereas the gelatinous casings range from 4.5 to 10 mm in diameter. Larvae within the gelatinous egg­mass clutches were found between stage 1 and stage 24 of development ( Gosner, 1960). Tadpoles beyond stage 20 were large and active, causing the casings to droop to the edge of the leaf (fig. 15). At stage 24, tadpoles are depressed, oval in dorsal view; snout round in dorsal and lateral views; eyes in dorsal position, dorsolateral orientation; nares threefourths to tip of snout, aperture oval, directed anterodorsally; oral disk ventral, elliptical, emarginated at the corners and appears suctorial; at this stage the labial teeth are still forming, although the jaw sheath is present and strongly keratinized in a typical shape (see Altig and McDiarmid, 1999: fig. 3.9A); tail is moderately high, originates near dorsal tail­body junction, tip weakly pointed. In preservative, body gray with light brown, irregular dusting, tail fin almost totally without pigment.

MEASUREMENTS (in mm) OF ONE TADPOLE AT STAGE 24: body length 4.08, lateral height 2.04; dorsal height 2.37; interorbital distance 1.42; internares distance 1.26; tail length 8.38; maximum tail muscle height 1.02; tail muscle width 0.67 (all tadpole measurements follow Altig and McDiarmid, 1999).

The generic placement of this small, distinct species is problematic. Philautus is a large (177 species), widely distributed (south and southeast Asia) genus with historically ambiguous diagnosable characters. This has made it a taxonomically confusing group, as assignment of small rhacophorid species has been scattered among Philautus , Chirixalus (21 species), and Rhacophorus (56 species) ( Bossuyt and Dubois, 2001; Frost, 2002). At the time of its description, the placement of gracilipes into Philautus rather than Chirixalus was based on the following characters: digit tips dilated into ‘‘regular­sized’’ disks for Philautus , ‘‘large­sized’’ disks for Chirixalus ; external metatarsals separated by a furrow or by a narrow web in Philautus , absent in Chirixalus ; ‘‘webbing’’ of two external fingers gives the appearance that they are opposable to the internal fingers in Chirixalus , not in Philautus ( Bourret, 1937, 1942; Liem, 1970). Although no phylogeny for Philautus has been proposed, Dring (1979) described the direct aerial development of the type species, Philautus aurifasciatus , and it has since been recognized as the diagnosable character for the genus ( Bossuyt and Dubois, 2001). Even in the absence of larval data, workers continue to assign small rhacophorid species to Philautus if they are not diagnosable as Chirixalus (i.e., do not have two external fingers ‘‘opposable’’ to the internal digits) ( Bossuyt and Dubois, 2001). Assignment of species to Chirixalus is also problematic, as it has been shown to be paraphyletic (Wilkinson et al., 2002).

Because tadpoles of C. gracilipes exhibit characters not seen in direct aerial developers (i.e., strongly keratinized jaw sheath, expand­ ed oral disk, and coiled gut), the species cannot be considered part of Philautus . Bossuyt and Dubois (2001) followed Inger et al. (1999: 23–24) in removing C. palbebralis from Philautus when faced with the same situation. In the absence of a known phylogeny of the two genera, we follow the provisional taxonomy of Bossuyt and Dubois (2001) and place gracilipes in Chirixalus , since it is not a member of Philautus , but we recognize that this is a provisional arrangement pending major revisionary work. This is consistent with Bossuyt and Dubois’ (2001) placement of gracilipes in the C. palbebralis group (sensu Fei, 1999). The need for these taxonomic stop­gap measures highlights the necessity for a rigorous systematic study of Rhacophorus , Chirixalus , and Philautus , the latter of which is also suspected to be paraphyletic ( Bossuyt and Dubois, 2001).

MEASUREMENTS OF FEMALES (in mm, N = 3, AMNH 163893, 163899, 163900; mean,

± standard deviation, range in parentheses): SVL 27.75 ± 1.24 (26.37, 28.08, 28.79), HDL 10.05 ± 0.83 (9.44, 9.72, 10.99), HDW 9.23 ± 0.81 (8.30, 9.56, 9.82), SNT 4.22 ± 0.31 (3.93, 4.55, 4.17), TIB 15.35 ± 0.29 (15.54, 15.49, 15.02), FTL 21.01 ± 0.45 (20.50, 21.18, 21.35), HND 9.46 ± 0.46 (9.51, 8.98, 9.89), EYE 3.48 ± 0.30 (3.14, 3.56, 3.73), TMP 1.44 ± 0.21 (1.20, 1.58, 1.55), IOD 4.36 ± 0.36 (4.33, 4.74, 4.02); median HDL:HDW 1.11 (1.14, 1.12, 1.14), median TIB:SVL 0.55 (0.55, 0.52, 0.59), median TMP:EYE 0.41 (0.44, 0.42, 0.38), median SNT:HDL 0.42 (0.47, 0.38, 0.42).

MEASUREMENTS OF MALES (in mm, N = 5, AMNH 163894–163898; mean, ± standard deviation, range in parentheses): SVL 22.76 ± 0.97 (21.66–23.80), HDL 8.89 ± 0.65 (8.06–9.66), HDW 7.73 ± 0.54 (7.16–8.56), SNT 3.67 ± 0.19 (3.38–3.86), TIB 13.06 ± 0.22 (12.80–13.41), FTL 17.56 ± 0.55 (16.96–18.04), HND 8.11 ± 0.71 (7.51– 9.28), EYE 3.34 ± 0.25 (3.11–3.74), TMP 1.26 ± 0.24 (0.95–1.49), IOD 3.62 ± 0.21 (3.50–3.99); median HDL:HDW 1.15 (1.08– 1.24), median TIB:SVL 0.58 (0.55–0.62), median TMP:EYE 0.38 (0.30–0.48), median SNT:HDL 0.41 (0.36–0.47).

Figures

Fig. 6. Three frog species from Ha Giang Province, Vietnam: (A) paratype of Rana iriodes, new species (AMNH 163928), adult male, SVL 42.80 mm; (B) paratype of Rana iriodes, new species; (C) paratype of Rana tabaca, new species (AMNH 163915), adult male, SVL 59.18 mm; (D) paratype of Rana tabaca, new species (AMNH 163920), adult female, SVL 103.40 mm; (E) Polypedates dugritei (AMNH 163910), adult male, in profile; and (F) posterior view showing transmedial white line, SVL 40.50 mm.

Fig. 10. Holotype of Rana tabaca, new species (AMNH 163923/IEBR 68), a male from Mt. Muong Cha, Ha Giang Province, Vietnam: dorsal view (left), ventral view (right). Scales equal 10 mm.

Fig. 11. Head of Rana tabaca, new species, holotype (AMNH 163923/IEBR 68), in profile. Scale equals 5 mm.

Fig. 12. Hand and foot of Rana tabaca, new species (AMNH 163923/IEBR 68), holotype: (A) hand;

Fig. 13. Dorsal view of posterior pelvic region of a female Rana tabaca, new species (AMNH 163921/ IEBR 67), paratype. Arrows point to groups of cutaneous masses on posterior part of the dorsum.

Fig. 14. Chirixalus gracilipes: dorsal view of gravid female (AMNH 163899) (left), SVL 29.50 mm; egg clutch (right). Individual eggs vary from 2.5–2.8 mm in diameter.

Fig. 15. Chirixalus gracilipes clutch with tadpoles visible.