Nasutixalus yingjiangensis, Yang & Chan, 2018

Yang, Jian-Huan & Chan, Bosco Pui-Lok, 2018, A new phytotelm-breeding treefrog of the genus Nasutixalus (Rhacophoridae) from western Yunnan of China, Zootaxa 4388 (2), pp. 191-206 : 194-204

Nasutixalus yingjiangensis sp. nov.

Holotype. SYS a005802, adult male, calling from inside a small tree hole on a small tree (Tetradium glabrifolium, ca. 13 cm in diameter at breast height) in a montane evergreen broadleaf forest at Tongbiguan Town, Yingjiang County, Yunnan Province, China (24°37'21.59'' N, 97°37'13.29'' E, 1610 m above sea level), collected on 20 April 2017 by J.H. Yang.

Paratypes. SYS a005803, adult male; SYS a005804, adult female, both from the same locality as holotype, collected on 10 June 2017 by J.H. Yang, Shen-Pin Yang, Li-Yan Wang and Rong-Jia Li.

Etymology. The specific name “ yingjiangensis ”, is a Latinized toponymic adjective in reference to the type locality of the new species, Yingjiang County of Yunnan Province, China. For the common names, we suggest “Yingjiang Tree-hole Frog” (English) and “Yíng jiāng léng bí shÙ wā” (Chinese).

Diagnosis. The new species is assigned to the genus Nasutixalus by the possession of the following morphological characters considered to be diagnostic for the genus: medium body size; outline of snout truncate in dorsal view, semi-circular in ventral view, slightly vertical in lateral view; snout not protruding; canthus rostralis obtuse and raised prominently, forming a ridge from nostril to anterior corner of eyes; webbing rudimentary on fingers and well developed on toes; dorsal skin relatively smooth, scattered with small tubercles; iris with a weak “X”-shaped, light colored marking (Biju et al. 2016; Jiang et al. 2016), and on the basis of molecular analyses (see above and Fig. 2 ).

Nasutixalus yingjiangensis sp. nov. can be distinguished from its congeners by a combination of following morphological characters: medium body size (SVL 39.5–40.0 mm in adult males, 47.5 mm in a single female); tympanum indistinct and covered with tubercles; disc diameter of third finger greater than tympanum diameter; dorsal skin relatively smooth, scattered with small tubercles, those on head and anterior dorsum of body more dense and more prominent; light brown above with a dark brown marking between eyes and two broad dark brown lateral strips on the dorsum; iris with a weak “X”-shaped, light colored marking; interorbital distance shorter than the upper eyelid width; comparatively short foot (mean TFL/SVL ratio 67.0% and 62.9% in males and a single female respectively).

Description of holotype (measurements in mm). SYS a005802 ( Fig. 3 & 4 ), adult male, medium body size (SVL 40.0), body habitus moderate; head width (HW 15.4) slightly greater that head length (HL 13.8); snout length (SL 5.8) nearly equal to horizontal diameter of the eye (ED 5.4); snout truncated in dorsal view, semi-circular in ventral view, and nearly slightly vertical in lateral view, not protruding; canthus rostralis rounded and raised noticeably, forming a ridge from nostril to anterior corner of eye; loreal region slightly concave; interorbital distance (IOD 3.7), slightly shorter than width of the upper eyelid (UEW 4.0), and internasal distance (IND 4.0); nostrils notably anterolaterally protuberant, oval, slightly closer to tip of snout (NS 2.4) than to eye (EN 2.6); tympanum barely distinct and circular (TD 2.2), 0.42 times of eye diameter, distance from eye (TED 0.7) by about one third of its own diameter; vomerine ridge distinct, obtuse, closer to choanae than each other; vomerine teeth absent; tongue deeply emarginated without median lingual process; supratympanic fold distinct and gently curved ventrally, extending from behind the eye, over the tympanum to axilla.

Forelimbs moderately long, robust, lower arm and hand length (LAHL 20.6) about half of body length; relative length of fingers I<II<IV<III; all finger tips dilated with well-developed disks with distinct circummarginal grooves (FDWI 1.6, FWI 1.3; FDWII 2.3, FWII 1.3; FDWIII 2.5, FWIII 1.3; FDWIV 2.2, FWIV 1.4), third finger disk width slightly larger than tympanum diameter; all fingers with distinct lateral fringes on the inner and outer sides, webbing on fingers rudimentary (I2 +–2+II2– 3III 2 2/3–2 1/ 2IV); subarticular tubercles prominently domed, rounded, formula 1, 1, 2, 2; thenar tubercles well developed; inner and outer metacarpal tubercles distinct, oval and long, inner one greater than outer one; distinct small supernumerary tubercles present on the base of all fingers; distinct nuptial pad present, surface microgranular, covering the dorsal surface of the basal phalange of finger I.

Hindlimbs long and slender (HLL 61.0), 171% of SVL; tibiotarsal articulation reaching the posterior corner of eye when adpressed along the body; shank (TIB 18.4) slightly longer than thigh (FML 18.0), and slightly shorter than foot (FL 18.9, LFT 26.6); toes moderately long and thick, relative lengths I<II<III<V<IV; tips of toes with well-developed disks with distinct circummarginal grooves, disks slightly smaller than those of fingers; relative width of discs I<II=III<V<IV (TDWI 1.5, TWI 1.0, TDWII 2.0, TWII 1.5, TDWIII 2.0, TWIII 1.4, TDWIV 2.4, TWIV 1.5, TDWV 2.1, TWV 1.3); all toes with distinct lateral fringes on the inner and outer sides, toe webbing moderate (I1 1/3– 2II 1–2+ III1–2 +IV2– 1V); subarticular tubercles distinctly domed, and rounded formula 1, 1, 2, 3, 2; inner metatarsal tubercle prominent, oval and long (2.1 in length); outer metatarsal tubercle absent; small supernumerary tubercles presents on the base of all toes; tarsal glandular ridge absent.

Dorsal surfaces of head, body and limbs smooth and scattered with small tubercles, those on dorsal head, eyelids and anterior body relatively prominent and dense whilst those on posterior body, lower flanks and limbs relatively weak and scarce; lateral surfaces of head covered with small tubercles, those on temporal region and supratympanic fold relatively prominent and dense; tympanum finely covered with tubercles; ventral surfaces of throat, chest, belly and basal thighs densely covered with distinct flat tubercles, those on throat and chest relatively smaller; ventral surfaces of the forelimbs, shanks and tarsus scattered with small tubercles.

Coloration of holotype in life. Dorsal surface pale brown with a moderate-sized dark inverted triangular- shaped blotch between the eyes extending to the upper eyelids, and two relatively broad dark lateral stripes that extend from above scapular region to groin; the two dark stripes on dorsum not in contact and anteriorly separated from the dark interorbital blotch between eyes; dark brownish broad transverse bands present on dorsal surface of fore and hind limbs: three on the lower arm, three on the thigh and tibia; a dark line extends from snout, through nostril and along canthus rostralis to the anterior corner of eye; a short and narrow light yellow stripe present on tip of snout; a dark blotch present on upper lip under the eye; a distinct small dark spot present on between anterior corners of eyes; supratympanic fold and tympanic region slightly darker; a relatively large dark blotch present on above axilla; lower flanks scattered with irregular dark marbling. Ventral surface immaculate, violet-grey in color. Iris dark blackish, with light golden pigmentation relatively scarce on anterior, posterior, upper and lower corners, forming an indistinct X-shaped golden marking ( Fig.3D ).

……continued on the next page Coloration of holotype in preservative. Greyish brown above, dark patterns on dorsum and bandings on limbs still visible; venter uniform grey, without distinct dark spots or marking; throat greyish white ( Fig. 4 ). Light golden pigmentation of iris coloration fades to greyish white.

Variation. The male paratype SYS a005803 and female paratype SYS a005804 match the overall characters of the holotype (for measurements of the type series see Table 3). The two broad dark stripes in contact with each other anteriorly and separated from the dark marking on head in male paratype SYS a005803, while the female paratype SYS a005804 has the two broad dark stripes extend anteriorly and connect with the dark marking on head (see Fig. 5 ). A narrow, light yellowish stripe borders the anterior edge of the dark interorbital blotch in the female paratype SYS a005804 ( Fig. 5C ). In preservative, the ventral surfaces of body, thigh and tibia of male paratype SYS a005803 are dull white and scattered with distinct, small dark brown spots and marbling, while the female paratype SYS a005804 has an immaculate, dark brown venter.

Comparisons. For the two known members of the genus Nasutixalus , N. yingjiangensis sp. nov. differs from N. medogensis by having a relatively smaller body size (males SVL 39.5–40.0 mm vs. 45.0 mm), interorbital distance shorter than the upper eyelid width (mean male IOD/UEW ratio 87.9% in the new species vs. 110.3% in N. medogensis ), a relatively shorter foot (mean male TFL/SVL ratio 67.5% in Nasutixalus yingjiangensis sp. nov. vs. 72.7% in N. medogensis ), dorsal surfaces of head and the anterior part of body with dense and prominent tubercles (vs. relatively smooth in N. medogensis ), and a different coloration pattern in life (dorsum of body and limbs without light green patterns in the new species vs. light green patterns present in N. medogensis ). Nasutixalus yingjiangensis sp. nov. can be distinguished from N. jerdonii by having interorbital distance shorter than the upper eyelid width (mean male IOD/UEW ratio 87.9% in the new species vs. 121.2% in N. jerdonii ), a relatively shorter foot (mean TFL/SVL ratio 67.0% and 62.9% in males and female respectively in the new species. vs. 70.6% (N=11) and 66.5% (N=1) in N. jerdonii ), tympanum indistinct and covered with tubercles (vs. tympanum fully exposed and smooth in N. jerdonii ), and nuptial pads only present on dorsal surface of finger I (vs. present on dorsal surface of finger I and finger II in male paratype of N. jerdonii , refers to Biju et al. 2016). Finally, the new species is distinct from all currently recognized species of Nasutixalus in the fragments of the 12S and 16S rRNA mt DNA genes examined (p> 7.1%).

Distribution and natural history. Nasutixalus yingjiangensis is currently only known from its type locality in Yingjiang County, western Yunnan, China. The type locality is a small, isolated patch of mature montane evergreen forest with an average canopy height of 30 m ( Fig. 6 ); this forest remnant is surrounded by a mosaic of farmland, orchards, Betula alnoides timber plantation, and recently-cleared forest land.

The male holotype SYS a005803 was found calling inside a small tree hole on a Tetradium glabrifolium tree at 21:30 h on 20 April 2017 (Fig, 6B); it has rained during the day. The tree hole was about 4.5 m above the ground; the opening was small and oval in shape (ca. 18 mm in width and 25 mm in length), and the tree hole cavity had conical shape and was about 100 mm in depth, 30 mm at the widest and 15 mm at its narrow end. The single female paratype SYS a005804 was found and collected from inside a large tree hole which was about ca. 5 m above ground during the day survey on 11 June 2017; the opening was about ca. 80 mm in diameter, while the tree hole cavity was about ca. 120 mm in depth. The other male paratype SYS a005803 was also found and collected from inside a small tree hole which was about ca. 2 m above ground during the day survey; the opening was about ca. 40 mm in diameter, while the tree hole cavity was about ca. 80 mm in depth. These observations suggest that the new species is a phytotelm-breeder, similar to N. jerdonii (Biju et al. 2016).

We conducted four field surveys at the type locality between July 2016 and June 2017. Many males were heard calling from the canopy (mostly ca. 4 m above ground) during summer surveys on 5 May 2016, 20 April and 10 June 2017; no male calls were detected during the winter survey on 8 December 2016. This indicates the new species breeds during the rainy season starting from mid-April. Calling activity was highest from dusk until midnight. Sympatric rhacophorid treefrogs recorded in the forest fragment during the surveys include Rhacophorus maximus Günther, Rhacophorus rhodopus Liu & Hu, Raorchestes longchuanensis (Yang & Li) , Kurixalus odontotarsus (Ye & Fei) and Polypedates cf. braueri (Vogt). No eggs and tadpoles of Nasutixalus yingjiangensis were found during the survey.

Advertisement call. The call series contains a single, pulsed call of 0.297– 0.391 s duration (mean 0.344 ± 0.035 s, N=12). The intercall-interval is of 3.527– 6.150 s (mean 4.195 ± 0.770 s, N=11). Calls are repeated in series at a rate of 13.3 times per minute on average. All calls contain a fundamental frequency and a dominant frequency. The dominant frequency range is of 1.56–1.64 kHz, whereas the fundamental frequency is of 0.76 kHz. A third harmonic is weakly present at 2.32–2.41 kHz ( Fig. 7 ). To the human ear, the advertisement call of the new species is a short and low-pitched “uh”.

Remarks: measurements of N. jerdonii and N. medogensis obtained from Biju et al. 2016 and Jiang et al. 2016 respectively.

Figures

FIGURE 2. Bayesian inference (BI) tree derived from 1266 bp sequences of the mitochondrial 12S and 16S rRNA genes. Numbers above branches are Bayesian posterior probabilities (> 70% retained) and numbers below branches indicate bootstrap support values for maximum likelihood analyses (>70% retained).

FIGURE 4. Types of Nasutixalus yingjiangensis sp. nov. in preservative:(A–B) holotype SYS a005802; (C–D) male paratype SYS a005803; (E–F) femaleparatype SYS a005804.Photos by J.H. Yang.

FIGURE 6. Habitat of Nasutixalus yingjiangensis sp. nov.: (A) type locality—mature evergreen montane forest fragment surrounded by farmland, cleared forest and Betula alnoides timber plantation; (B) microhabitat of the male holotype SYS a005802, red arrow denotes location of the tree hole, where the calling male holotype was found; (C) close-up of the tree hole opening located ca.4.5 m above the forest floor.Photos by Joanne Li (A, B) and Zhi-Hua Zhang (C).

FIGURE 7. Advertisement call of an unvouchered male individual of Nasutixalus yingjiangensis sp. nov.: (A) waveform and spectrogram showing a two note portion of a call group;(B) waveform and spectrogram showing a single call.

FIGURE3. Holotype of Nasutixalus yingjiangensis sp. nov. (SYS a005802) in life:(A) anterolateral view of right head,noted the X-shaped iris pattern and raised canthus rostralis;(B) general view, dorsolateral aspect; (C) dorsal view; (D) ventral view; (E)thenar view of hand;(F) volar view of foot;(G) schematic illustration of foot webbing.Photos by J.H.Yang.

FIGURE5. Nasutixalus yingjiangensis sp. nov.: (A–B) adultmale paratype SYS a005803 in life;(C–D) adult female paratype SYS a005804 in life.Photos by J.H.Yang.