Theloderma annae, Nguyen, Truong Quang, Pham, Cuong The, Nguyen, Tao Thien, Ngo, Hai Ngoc & Ziegler, Thomas, 2016

Nguyen, Truong Quang, Pham, Cuong The, Nguyen, Tao Thien, Ngo, Hai Ngoc & Ziegler, Thomas, 2016, A new species of Theloderma (Amphibia: Anura: Rhacophoridae) from Vietnam, Zootaxa 4168 (1), pp. 171-186 : 176-183

Theloderma annae sp. nov.

( Figs. 2 , 3 )

Holotype. IEBR 3732 (Field number HB 2014.185), adult male, collected by T. Q. Nguyen et al. on 9 October 2010 in karst forest near Cho Village (20o24.909’N, 105o19.102’E, at an elevation of 343 m), Tu Do Commune, Lac Son District, Hoa Binh Province, Vietnam.

Paratypes. Seven specimens collected from Ngoc Son – Ngo Luong Nature Reserve in Lac Son District , Hoa Binh Province, Vietnam: IEBR 3733–3735 (Field numbers HB 2014.92–2014.94), adult males, collected by C. T. Pham et al. on 19 April 2014 in the karst forest near Khu Village (20o27.976’N, 105o18.421’E, at an elevation of 650 m) Ngoc Son Commune ; ZFMK 97289 (Field number HB 2014.121), adult female, collected by T.Q. Nguyen et al. on 2 October 2014 in the karst forest near Khu Village (20o26.862’N, 105o20.144’E, at an elevation of 553 m) Ngoc Son Commune ; ZFMK 97290 (Field number HB 2014.147), adult male, collected by T.Q. Nguyen et al. on 6 October 2014 in the karst forest near Khang Village (20o23.778’N, 105o20.847’E, Vietnam, at an elevation of 219 m) Tu Do Commune ; IEBR 3736 (Field number HB 2014.186), adult female, collected by T.Q. Nguyen et al. on 9 October 2010 in the karst forest near Cho Village (20o24.964’N, 106o19.116’E, at an elevation of 279 m), Tu Do Commune ; VNMN A.2016.5 (Field number HB 2014.211), adult male, collected by T.Q. Nguyen et al. on 10 October 2014 in the karst forest near Khu Village (20o26.517’N, 105o20.147’E, at an elevation of 570 m) Ngoc Son Commune.

Diagnosis. Morphologically, the frog specimens from Hoa Binh Province showed diagnostic characters of the genus Theloderma , for instance a distinct tympanum, round canthus rostralis, bony ridges from canthus rostralis to occiput absent, and skin of head not co-ossified to the skull (see Liem 1970; McLeod & Norhayati 2007; Rowley et al. 2011). However, because no morphological synapomorphy is known for the genus Theloderma , and its monophyly is not certain ( Bain et al. 2009; Li et al. 2009; Rowley et al. 2011) we used molecular evidence to provide independent support of our generic placement.

The new species is distinguished from its congeners and other small rhacophorid species by a combination of the following characters: 1) Size small (SVL 27.1–28.5 mm in males, 30.3–32.6 mm in females); 2) head longer than wide; 3) vomerine teeth absent; 4) snout long (SNL/SVL 0.16–0.19); 5) spines on upper eyelid absent; 6) tibiotarsal projection absent; 7) dorsal skin smooth; 8) dermal fringes on forearm and tarsus absent; 9) dorsal surface greyish green; and 10) throat and ventral surfaces of arms and thighs brown with white spots.

Description of holotype. Adult male, body robust (SVL 27.4 mm), dorsoventrally compressed. Head slightly longer than wide (HL 11.7 mm, HW 10.8 mm), convex above; snout round in dorsal view, slightly protruding, its length longer than horizontal diameter of eye (SNL 5.1 mm, ED 4.1 mm); canthus rostralis round, loreal region oblique, concave; interorbital distance wider than internarial distance and upper eyelid (IOD 3.6 mm, IN 3.3 mm, UEW 2.9 mm); distance between anterior corner of eyes (DAE 6.2 mm) about 68% distance between posterior corner of eyes (DPE 9.2 mm); nostril round, without a lateral flap of skin, closer to tip of snout than to the eye (NS 2.4 mm, EN 3.4 mm); pupil oval, horizontal; tympanum distinct (TYD 2.7 mm), round, smaller than eye diameter (ED 4.1 mm), greater than the distance between tympanum and eye (TYE 1.1 mm); pineal ocellus absent; spinules on upper eyelid absent; vomerine teeth absent; choanae small, oval; tongue cordate, deeply notched posteriorly; vocal sac absent; supratympanic fold distinct, extending from behind the eye to beyond level of axilla.

Forelimbs: Arm short, about half of hand length (FLL 5.8 mm, HAL 14.2 mm), dermal fringe along outer side of forearm absent; fingers free of webbing, relative lengths of fingers I<II≤V<III; tips of fingers with enlarged discs with distinct circummarginal grooves; disc of finger III approximately two times of width of finger III (fd3/ fw3 1.99) but smaller than tympanum diameter (fd3/TYD 0.58); subarticular tubercles distinct, blunt, round, formula 1, 1, 2, 2; nuptial pads prominent, oval; outer palmar tubercle divided into two.

Hindlimbs: Heels overlapping when held at right angles to the body; tibia length about five times greater than tibia width (TbL 16.7 mm, TbW 3.5 mm), longer than thigh length (FeL 14.7 mm) but shorter than foot length (FoL 20.8 mm); relative length of toes I<II<III≤V<IV; tips of toes with enlarged discs with distinct circummarginal grooves, discs slightly smaller than those of fingers; webbing formula I1-1 ½ II1-2III1-2IV2-1 V; subarticular tubercles distinct, blunt, round, formula 1, 1, 2, 3, 2; inner metatarsal tubercle small (IMT 1.7 mm); dermal ridge along outer side of tibia and tarsal fold absent; projection at tibiotarsal articulation absent.

Skin texture in life: Dorsal surface of head and body smooth; posterior part of dorsum, flanks, dorsal surface and lateral sides of limbs with small granules; dorsolateral folds absent; throat and chest smooth, belly and ventral surface of thighs granular; dermal appendage at vent absent.

Coloration in life: Iris greyish green, pupil round; background of dorsal surface greyish green; head with a mossy green blotch between eyes, in triangular shape; tympanum brown; dorsum and upper part of flanks with dark markings and blotches, forming a network; dorsal surface of forelimbs yellowish green with some mossy green spots and bars; throat and chest white with brown marbling; belly immaculate white. The coloration is brighter at night.

Coloration in preservative: Dorsal surface of head, dorsum, and upper part of flanks greyish brown with dark markings and blotches; upper lip and tympanum light brown; forelimb, dorsal surface of thigh, tibia and foot grey with dark bands, posterior part of thigh below the vent greyish brown with small white spots; chin and throat brown with small white spots; belly immaculate cream to white; ventral part of forelimbs white to grey with small white spots; ventral surface of thighs white to grey with small white spots; tibia and webbing dark brown.

Variation and sexual dimorphism. Measurements and morphological characters of the type series are provided in Table 3 . The dorsal markings are indistinct in the specimen IEBR 3735, more prominent in the specimens IEBR 3734, 3736, ZFMK 97289, 97290 and consisting of three dark blotches in the individual IEBR 3733. The males are smaller in size than the females (SVL 27.1–28.6 mm, n = 6 vs. 30.3–32.6 mm, n = 2, respectively).

Etymology. We name this new species in honor of our colleague and friend, Anna Rauhaus, section animal keeper of the terrarium division of the Cologne Zoo, Germany, in recognition of her support of our research and conservation work in Vietnam. As common names we suggest Anna’s Mossy Frog (English), Ếch cây sần an-na (Vietnamese), and Annas Moosfrosch (German).

Ecological notes. Theloderma annae sp. nov. appears to be closely associated with karstic environment. Specimens were found at night between 19:00–23:30 h near cave entrances and in valleys surrounded by limestone cliffs, relatively far from water sources ( Fig. 4 ). Advertisement calls, eggs and tadpoles of the species have not been recorded during our field surveys. The main habitat at the type locality is secondary karst forest of medium and small hardwoods mixed with shrubs and vines. Most of specimens were found on leaves, about 0.3–1.2 m above the ground but some specimens were collected on a limestone cliff. The air temperatures at the times of collection ranged from 20.4–30.2o C and relative humidity from 59–87%. In Ngoc Son – Ngo Luong Nature Reserve, several species of Theloderma have been recorded, viz. T. albopunctatum (Liu & Hu) , T. corticale (Boulenger) , and T. lateriticum , but they were found in tree holes filled with water or on tree leaves near streams in the valleys. Other species of amphibians and reptiles found at the site were Rhacophorus sp., Raorchestes parvulus (Boulenger) , Cyrtodactylus bobrovi Nguyen, Le, Ngo, Pham, Hoang, Pham & Ziegler , and Gekko cf. palmatus Boulenger.

Distribution. Theloderma annae sp. nov. is currently known only from the type locality in Ngoc Son – Ngo Luong Nature Reserve, Hoa Binh Province, Vietnam. Several field surveys were conducted in the adjacent karst forest of Hang Kia – Pa Co Nature Reserve in Hoa Binh Province but no records of this species have been made so far.

IEBR VNMN IEBR IEBR IEBR ZFMK ZFMK IEBR

3732 A.2016.5 3733 3734 3735 97290 97289 3736 Comparisons. We compared the new species with other members of the genus Theloderma based on morphological specimen examination (see Appendix I) and data obtained from the literature (e.g., Ahl 1927, 1931; Bain & Nguyen 2004; Bain et al. 2009; Boulenger 1903; Bourret 1937, 1942; Chanda 1994, Chan-ard 2003; Chan & Norhayati 2009; Fei et al. 2009, 2012; Inger et al. 1999; Jiang et al. 2009; Kunz et al. 2010; Liu & Hu 1962; McLeod & Norhayati 2007; Nguyen et al. 2014; Orlov et al. 2005, 2006, 2012; Smith 1924; Stuart & Heatwole 2004; Taylor 1962; Tschudi 1838; Rowley et al. 2011).

Theloderma annae sp. nov. differs from T. bicolor (Bourret) , T. corticale , T. gordoni Taylor, T. (Stelladerma in Poyarkov et al. 2015) horridum (Boulenger), T. kwangsiense (Liu & Hu) , T. leporosum Tschudi , T. moloch (Annandale) , T. nagalandense Orlov, Dutta, Ghate & Kent , and T. phrynoderma (Ahl) by having a smaller size (SVL 27.1–28.6 mm in males and 30.3–32.6 mm in females vs. SVL ≥ 40 mm in the other species) and smooth dorsal skin (vs. with large warts in other species).

The new species differs from T. andersoni (Ahl) by having smooth dorsal skin (vs. with small tubercles in T. andersoni ), in dorsal color pattern (greyish green vs. dark olive with two yellow spots on middle of flanks and a large black spot on groin in T. andersoni ) and ventral color (white vs. yellow with fine brown spots anteriorly in T. andersoni ); from T. albopunctatum (Liu & Hu) and T. asperum (Boulenger) by having smooth dorsal skin (vs. with small tubercles in latter species), in dorsal color pattern (greyish green vs. greyish brown with large conspicuous white pattern in latter species), in ventral color pattern (white vs. marbled black and bluish grey in latter species), and iris color (greyish green vs. reddish brown in latter species); from T. baibengense Jiang, Fei & Huang by having smooth dorsal skin (vs. with small tubercles in T. baibengense ), in dorsal color pattern (greyish green vs. back with large conspicuous white pattern in T. baibengense ), and ventral color pattern (white vs. dark with white pattern in T. baibengense ); from T. lateriticum in dorsal color pattern (greyish green vs. brick red with single black mid-dorsal spots in T. lateriticum ), in ventral color pattern (white vs. uniform grey-brown with white spots in T. lateriticum ), and iris color (greyish green vs. brick-red in T. lateriticum ); from T. laeve (Smith) in dorsal color pattern (greyish green vs. golden beige to light brown above with small dark brown spots and blotches forming an x-shaped figure, and dark longitudinal streaks on flanks in T. laeve ), in ventral color pattern (white vs. light greyish pink to violet), and iris color (greyish green vs. grey above and dark brown below in T. laeve ); from T. licin McLeod & Ahmad by having dorsal skin smooth (vs. with small tubercles in T. licin ), in dorsal color pattern (greyish green vs. white to pale brown in T. licin ), in ventral color pattern (white vs. white with brown reticulations in T. licin ), and iris color (greyish green vs. red in T. licin ); from T. nebulosum by having smooth dorsal skin (vs. with small tubercles in T. nebulosum ), in dorsal color pattern (greyish green vs. brown with dark marking in T. nebulosum ), in ventral color pattern (white vs. dark brownish black with pale blue in T. nebulosum ), and iris color (greyish green vs. pale gold above, reddish brown below in T. nebulosum ); from T. palliatum by having smooth dorsal skin (vs. with small tubercles in T. palliatum ), in dorsal color pattern (greyish green vs. pale brown or pale yellow to light straw brown with dark blotches forming an x-shaped figure in T. palliatum ), in ventral color pattern (white vs. dark brownish black with pale blue or greyish with light bluish and dark spots and blotches in T. palliatum ), and iris color (greyish green vs. pale gold above, reddish brown below in T. palliatum ); from T. petilum (Stuart & Heatwole) in dorsal color pattern (greyish green vs. light brown with dark brown reticulations and scattered black spots in T. petilum ), and the iris color (greyish green vs. upper part reddish brown, lower part grey in T. petilum ); from T. rhododiscus (Liu & Hu) in dorsal color pattern (greyish green vs. brown in T. rhododiscus ), in ventral color pattern (white vs. brown black scattered with grey white network in T. rhododiscus ), and iris color (greyish green vs. red brown in T. rhododiscus ); from T. ryabovi Orlov, Dutta, Ghate & Kent by having a smaller size (SVL 27–33 mm vs. 44 mm in T. ryabovi ), in dorsal color pattern (greyish green vs. light beige with lilac pattern and black spots in T. ryabovi ), in ventral color pattern (white vs. dark grey in T. ryabovi ), and iris color (greyish green vs. dark brown in T. ryabovi ); from T. (Stelladerma in Poyarkov et al. 2015) stellatum Taylor and T. (Stelladerma in Poyarkov et al. 2015) vietnamense in dorsal color pattern (greyish green vs. brown with light markings in the latter), in ventral color pattern (white vs. dark brown reticulated with cream in in the latter), and iris color (greyish green vs. brown with black reticulations in the latter); and from T. truongsonense (Orlov & Ho) in dorsal color pattern (greyish green vs. pale brown with small, distinct darker brown markings in T. truongsonense ), in ventral color pattern (white vs. dark grey with black round speckles in T. truongsonense ), and iris color (greyish green vs. pale gold above, reddish brown below in T. truongsonense ).

In terms of dorsal color pattern Theloderma annae sp. nov. is similar to Gracixalus quyeti (Nguyen, Hendrix, Böhme, Vu & Ziegler) from Quang Binh Province and G. w a z a Nguyen, Le, Pham, Nguyen, Bonkowski & Ziegler from Cao Bang Province. In addition, Theloderma annae sp. nov. and the two afore mentioned Gracixalus species also have similar life histories, all inhabiting limestone karst forest far from water sources. However, Theloderma annae differs from G. quyeti by having dorsal skin smooth (vs. with small sharp tubercles in G. quyeti ), the absence of a dark inverse Y-marking on dorsum (vs. present in G. quyeti ), and the outer palmar tubercle prominent (vs. indistinct in G. quyeti ). Theloderma annae sp. nov. differs from G. w a z a in the ratio of TYD/TDE (0.39 in males and 0.32 in females vs. 0.87 in males and 0.98 in females in G. w a z a), and the absence of a dark inverse Y-marking on dorsum (vs. present in G. waza ) ( Nguyen et al. 2008, 2012).

Figures

FIGURE 2. Dorsal and ventral views of the holotype (IEBR 3732, adult male) of Theloderma annae sp. nov. from Hoa Binh Province, Vietnam.

FIGURE 3. Ventral side of hand (A) and foot (B) of the holotype (IEBR 3732) of Theloderma annae sp. nov. in preservative.

FIGURE 4. Theloderma annae sp. nov. (IEBR 3734) in situ on vegetation in Ngoc Son – Ngo Luong Nature Reserve, Hoa Binh Province, Vietnam.

Tables

TABLE 3. Measurements (in mm) and proportions of the type series of Theloderma annae sp. nov. (H = holotype, P = paratype, other abbreviations defined in text).

Sex ♂ Type status H	♂ P	♂ P	♂ P	♂ P	♂ P	Min-Max Mean±SD ♀ (n=6) (n=6) P	♀ P
SVL 27.4 HW 10.8	27.7 10.2	28.0 10.2	28.5 10.9	27.8 10.4	27.1 10.3	27.1–28.5 27.7±0.34 30.3 10.2–10.9 10.5±0.26 11.8	32.6 12.7
HL 11.7 MN 2.2	11.2 2.3	11.1 2.1	11.2 2.3	11.6 2.0	11.6 2.1	11.1–11.7 11.4±0.23 12.4 2.0–2.3 2.2±0.08 2.0	13.0 2.5
MFE 5.2 MBE 7.8	4.8 8.0	4.9 8.4	4.8 8.6	4.8 9.7	4.6 8.7	4.6–5.2 4.8±0.13 4.2 7.8–9.7 8.4±0.27 8.2	5.2 8.9
SNL 5.1 ED 4.1	4.9 4.2	4.6 4.2	5.0 4.5	4.6 4.2	5.0 4.4	4.6–5.1 4.9±0.16 5.0 4.1–4.5 4.3±0.11 4.8	5.4 4.9
UEW 2.9 IN 3.3	2.8 3.4	2.9 3.1	2.8 3.2	2.7 3.2	2.6 3.0	2.6–2.9 2.8±0.07 2.9 3.0–3.4 3.1±0.18 3.4	3.2 3.5
IOD 3.6	3.8	3.8	3.4	3.7	3.7	3.4–3.8 3.7±0.09 3.8	4.0
DAE 6.2 DPE 9.2	6.1 8.8	5.8 8.5	5.8 8.9	6.3 8.8	6.1 8.6	5.8–6.2 6.0±0.16 6.4 8.5–9.2 8.8±0.16 9.4	6.6 10.2
NS 2.4 EN 3.4	2.1 3.3	2.2 3.1	2.1 3.2	2.2 3.2	2.3 3.0	2.1–2.4 2.2±0.08 2.4 3.0–3.4 3.2±0.11 3.1	2.5 3.4
TYD 2.9 TYE 1.1	2.6 1.2	2.4 0.9	2.5 0.9	2.6 1.0	2.7 1.1	2.4–2.9 2.6±0.12 3.1 0.9–1.2 01.0±0.10 0.9	3.2 1.0
FLL 5.8	5.1	4.4	4.8	4.7	4.	4.4–5.8 4.9±0.36 5.5	6.3
HAL 14.2 TFL 6.2 fd3 1.7	13.3 5.6 1.5	13.6 5.7 1.6	13.9 5.8 1.6	13.8 5.8 1.7	13.4 5.3 1.5	13.3–14.2 13.7± 0.26 14.3 5.3–6.2 5.7±0.20 5.9 1.5–1.7 1.6± 0.06 1.5	15.8 6.3 1.6
FeL 14.7 TbL 16.7	15.1 16.2	13.8 15.8	14.8 15.7	14.1 16.4	13.8 17.0	13.8–15.1 14.4 ±0.48 15.0 15.7–17.0 16.3±0.38 17.4	15.8 18.9
TbW 3.5	3.0	3.1	3.0	3.1	2.9	2.9–3.5 3.1± 0.14 3.1	3.5
FoL 20.8 FTL 12.9	21.1 12.3	19.7 12.1	20.2 11.7	20.0 10.7	20.7 11.0	19.7–20.8 20.3± 0.33 22.0 10.7–12.9 11.8 ±0.63 13.5	23.4 13.3
SNL/SVL 0.19 ED/SNL 0.80	0.18 0.87	0.18 0.91	0.17 0.90	0.17 0.90	0.18 0.88	0.17–0.19 0.18± 0.01 0.16 0.80–0.91 0.88± 0.03 0.97	0.17 0.90
TYE/TYD 0.40 fd3/TYD 0.58	0.45 0.60	0.38 0.66	0.34 0.62	0.37 0.67	0.39 0.55	0.34–0.45 0.30±0.03 0.33 0.55–0.67 0.61± 0.04 0.52	0.30 0.48