Nidirana yeae, Wei & Li & Liu & Cheng & Xu & Wang, 2020

Wei, Gang, Li, Shi-Ze, Liu, Jing, Cheng, Yan-Lin, Xu, Ning & Wang, Bin, 2020, A new species of the Music frog Nidirana (Anura, Ranidae) from Guizhou Province, China, ZooKeys 904, pp. 63-87 : 63

Nidirana yeae sp. nov. Figures 4 , 5A-C , 6 ; Table 1, Suppl. material 1: Table S1

Material examined.

Holotype. CIBTZ20190608004 (Figs 4 , 5 ), adult male, collected by Shi-Ze Li on 6 June 2019 in Huanglian Town (28.44317N, 107.02003E; ca. 1170 m a.s.l.), Tongzi County, Guizhou Province, China.

Paratypes. A total of nine specimens (eight adult males and one adult female) collected by Shi-Ze Li from Huanglian Town in Tongzi County, Guizhou Province, China. Two male specimens: CIBTZ20160714016 and CIBTZ20160714017 collected on 14 July 2016; one female specimen: CIBTZ20190608005 and six male specimens: CIBTZ20190608001, CIBTZ20190608003, CIBTZ20190608006, CIBTZ20190608010, CIBTZ20190608011, CIBTZ20190608013, CIBTZ20190608016 and CIBTZ20190608017 collected on 8 June 2019.

Other material examined.

One tadpole (CIBTZ20190608019) collected by Jing Liu on 8 June 2019.

Diagnosis.

Nidirana yeae sp. nov. is assigned to the genus Nidirana based on molecular data and the following combination of characters: absence of thumb-like structure on finger I; disks of digits dilated, rounded; dorsolateral folds distinct; the presence of large suprabrachial gland in male.

Nidirana yeae sp. nov. could be distinguished from its congeners by a combination of the following characters: (1) body of medium size (SVL 41.2-43.5 mm in males and 44.7 mm in female); (2) lateroventral groove only present on toes; (3) relative finger lengths: II <IV <I <III; (4) three metatarsal tubercles on palm; (5) heels overlapping when hindlimbs flexed at right angles to axis of body; (6) tibiotarsal articulation reaching the level of eye when leg stretched forward; (7) a pair of subgular internal vocal sacs at corners of throat in male; (8) nuptial pad present on the inner side of base of fingers I in male in breeding season; (9) tadpole labial tooth row formula with 1:1+1/1+1:2; (10) in male, the advertisement call containing two kinds of note and the call containing 2-6 repeated regular notes.

Description of holotype.

Body size medium, SVL 40.2 mm; head slightly wider than long (HDW/HDL = 1.03), flat above; snout rounded in dorsal and lateral views, slightly projecting beyond lower jaw; a maxillary gland in posterior corner of mouth from snout to tympanum, behind the gland a shoulder gland present; supratympanic fold absent; interorbital space narrower than internarial distance (IND/IOD = 1.38); eye large and convex, ED 0.76 times of SL; tympanum distinct, large and rounded, 0.76 times of ED, and close to eye; vomerine ridge present, but the outline of vomerine ridges are not sharp and almost connected to the internal nostril; tongue deeply notched posteriorly; paired subgular inner vocal sacs at corners of throat.

Forelimbs moderately robust (LW/SVL = 0.08); lower arm and hand less than a half of body length (LAL/SVL = 0.42); relative finger lengths: II <IV <I <III; tip of fingers weakly dilated, forming elongated and pointed disks; lateroventral grooves on the disks of finger absent; fingers free of webbing, with lateral fringes on fingers III and IV; subarticular tubercles prominent and rounded; week supernumerary tubercles below the base of fingers III and IV; palmar tubercles three, elliptic, distinct.

Hindlimbs relatively robust, tibia 47% of SVL; tibia longer than thigh (TL/THL = 1.04); heels overlapping when hindlimbs held at right angles to axis of body; tibiotarsal articulation reaching the level of mid-eye when hindlimb is stretched forward; toes long and thin, relative toe lengths: I <II <V <III <IV; tip of toes dilated, forming significantly elongated disks; distinct lateroventral grooves on toes; webbing weak, webbing formula:

I2-2II123-312III212-323IV323-2V;

toes with lateral fringes; subarticular tubercles rounded, prominent; inner metatarsal tubercle elliptic, twice as long as its width; outer metatarsal tubercle indistinct, small and rounded.

Dorsal skin of head and anterior part of body smooth, posterior part and flanks with several tubercles, some tubercles with black spot; a large suprabrachial gland behind base of forelimb; dorsolateral fold extending from posterior margin of upper eyelid to above groin; several granules on the dorsal surfaces of thigh, tibia, and tarsus; ventral surface of head, body, and limbs smooth, several flattened tubercles densely arranged on the rear of thigh and around vent.

Colouration of holotype in life.

In life, dorsal surface and suprabrachial gland pale brown; flank relatively smooth with dense tubercles on region nearly the dorsolateral fold; several black spots on flank, dorsum, and head; a discontinuous light yellow streak from posterior head to cloacae; dorsal forelimbs light brown and one brown stripe in front of the base of forelimb; dorsal hindlimb grey-brown with dense tubercles, three brown bands on the thigh, four on the tibia and the tarsus; tympanum and temporal region black; maxillary gland white; ventral surface smooth, throat and ventral of thigh and forelimbs incarnadine, belly and chest light yellow (Fig. 4 ).

Preserved holotype colouration.

Dorsal surface faded to brown; black spots on dorsum and flank more distinct; limbs faded light brown and the crossbars becoming clearer; ventral surface faded to pale cream and throat fade to brownness (Fig. 5 ).

Variations.

All adult specimens were similar in morphology but some individuals differed from the holotype in colour pattern. In some adult males, the colour of tympanum and temporal region pinkish red (Fig. 6A ); in some adult males, the colour of dorsum is reddish brown (Fig. 6B ); in the adult female, the colour of dorsum was brownish red and the flank was brownish under the dorsolateral fold (Fig. 6C ); in some adult males, the colour of dorsum brick-red and the tubercles on flank were obvious (Fig. 6D ); in some adult males, the throat was creamy and ventral surface of body was white with brown patches (Fig. 6E ); in the adult female, the throat was brown and there were some patchiness on the ventral surface of the body and thigh (Fig. 6F ).

Tadpole description.

Measurements of specimen CIBTZ20190608019 (in mm): TOL 35.2, SVL 14.0, BW 6.1, BH 5.1, SL 3.1, SS 8.1, IOD 3.3, TAL 20.7, TAH 4.0, TBW 3.0. Body oval, body and tail yellowish brown, flattened above; several brown spots on dorsum and tail; maximum depth near posterior part of tail and more than body depth; body width longer than body height (BW/ BH = 1.53); eyes lateral, nostril near snout; spiracle on left side of body, directed dorsoposteriorly; keratodont formula: 1:1+1/1+1:2; ventral of body oval, creamy white with dense brown spots on flank of body; both upper and lower lips with labial papillae; some additional tubercles at the angles of the mouth, usually with small keratodonts; tail fusiform, approximately 1.5 times as long as snout-vent length, tail height 19.3 % of tail length; dorsal fin arising behind the origin of the tail (Fig. 7 ).

Advertisement call.

Eleven advertisement calls of Nidirana yeae sp. nov. were recorded from the holotype CIBTZ20190608004 on the ridge of a paddy field in Huanglian Town, Tongzi County, Guizhou Province, China on 8 June 2019 between 21:00-22:00. The call has two kinds of notes (Fig. 3 ; Table 5 ). Call duration was 728-2082 ms (mean 1199 ± 174 ms, N = 11). Call interval was 2000-9435 ms (mean 4586 ± 2659 ms, N = 10). The first type of note is the start note in each call and the other notes in each call are termed the second type. Amplitude modulation within strophe is apparent, beginning with moderate energy pulses, decreasing slightly to a minimum then increasing approximately to the midnote, subsequently increasing to a peak then decreasing rapidly towards the end of each note in the first type; in the second type amplitude beginning with highest pulses and decreasing towards approximately the midnote then increasing slightly then decreasing towards the end of each note. The first type of note has a longer duration than the second type (308-440 ms, N = 10 vs.135-240 ms, N = 23).The two-note call (N = 5) has a duration of 728-825 ms, and dominant frequency is 4200-5040 Hz, three-note call (N = 2) has a duration of 988-1135 ms and dominant frequency is 4620-5040 Hz, four-note call (N = 3) has a duration of 1400-1563 ms and dominant frequency is 4680-5160 Hz, six-note call (N = 1) has a duration of 2082 ms and dominant frequency is 5280 Hz (Table 5 ).

Secondary sexual characteristics.

A pair of subgular inner vocal sacs, a pair of slit-like openings at posterior of jaw; a single light brown nuptial pad on the inner side of dorsal surface of finger I (Fig. 4C ); nuptial spicules invisible; suprabrachial gland present.

Morphological comparisons.

Nidirana yeae sp. nov. differs from N. leishanensis and N. lini by having smaller body size (SVL <45 mm in the new species vs. SVL> 49 mm in males of N. leishanensis and SVL> 57 mm in females of N. lini ).

Nidirana yeae sp. nov. differs from N. daunchina , N. hainanensis and N. leishanens by the presence of lateroventral groove only on toes (vs. both fingers and toes present in the latter).

Nidirana yeae sp. nov. differs from N. pleuraden by the presence of lateroventral groove only on toes (vs. both fingers and toes absent in the latter).

Nidirana yeae sp. nov. differs from N. adenopleura , N. hainanensis , N. lini , N. nankunensis , N. okinavana , and N. pleuraden by the relative finger lengths II <IV <I <III (vs. II <I <IV <III or II <I = IV <III in the latter).

Nidirana yeae sp. nov. differs from N. hainanensis , N. lini , and N. nankunensis by tibiotarsal articulation reaching the level of eye when leg stretched forward (vs. reaching nostril or beyond snout in the latter).

Nidirana yeae sp. nov. differs from N. okinavana by having subgular internal vocal sacs (vs. gular vocal sacs absent in the latter).

Nidirana yeae sp. nov. differs from N. hainanensis and N. leishanensi by having nuptial pad on the inner side of base of fingers I in males in breeding season (vs. nuptial pad absent in N. hainanensis and nuptial pads on both fingers I and II in N. leishanensis ).

Nidirana yeae sp. nov. differs from N. nankunensis and N. okinavana by the call containing 2-6 notes (vs. 13-15 notes in N. nankunensis and 17-25 notes in N. okinavana ).

Nidirana yeae sp. nov. is genetically closer to N. chapaensis , N. daunchina , and N. yaoica . It differs from N. chapaensis by the following characters: the relative finger lengths II <IV <I <III (vs. II <I = IV <III), tibiotarsal articulation reaching the level of eye when leg stretched forward (vs. reaching nostril), having nuptial pad on the inner side base of finger I in males in breeding season (vs. having two nuptial pads on finger I), tadpole labial tooth row formula of 1:1+1/1+1:2 (vs. 1:1+2/1+1:2); differs from N. daunchina by the presence of lateroventral groove only on toes (vs. both fingers and toes present), heels overlapping when hindlimbs flexed at right angles to axis of body (vs. heels meeting), tibiotarsal articulation reaching the level of eye when leg stretched forward (vs. reaching nostril), having significantly lower value of SVL in males and having significantly lower ratios of HDL, ED, TED, HLL, TW, TFL, and FL to SVL in males, the outline of vomerine ridges not sharp and almost connected to the internal nostril (vs. outline of vomerine ridges sharp and distinctly separated from the internal nostril; Fig. 5G, H ), having longer call duration in two-note call and three-note call, having shorter note interval in the two-note call and three-note call (Table 4 ); differs from N. yaoica by the presence of lateroventral groove only on toes (vs. both fingers and toes present), relative finger lengths II <IV <I <III (vs. II <I <IV <III), tibiotarsal articulation reaching the level of eye when leg stretched forward (vs. reaching nostril), having significantly lower ratios of HDL, HDW, ED, TED, RAD, TL, and FL of SVL in males, having longer call duration and longer note duration in two-note call and three-note call, having shorter note interval in two-note call and three-note call, and having higher dominant frequency in call (Table 5 ).

Remarks.

Wu et al. (1986) reported that the populations from Kuankuoshui Nature Reserve of Suiyang County, Fanjiang Mountain of Jiangkou County and Leigong Mountain of Leishan County, Guizhou Province, China belonged to N. adenopleura . Fei et al. (1990, 2009) suggesting that populations from Kuankuoshui Nature Reserve of Suiyang County together with the populations from north-eastern part of Guizhou Province, China should be N. daunchina , and the populations from Fanjiang Mountain of Jiangkou County and Leigong Mountain of Leishan County, Guizhou Province, China should be N. adenopleura . Li et al. (2019a) proved that the population from Leigong Mountain of Leishan County should be a new species, which they named N. leishanensis . From the morphological description and morphometric data of the population from Kuankuoshui Nature Reserve of Suiyang County, some characters is very similar to Nidirana yeae sp. nov.: body of medium size (SVL 39.0-46 mm in males and 44-48 mm in females); lateroventral groove on toes present; relative finger lengths II <IV <I <III; three metatarsal tubercles on palm; a pair of subgular internal vocal sacs at corners of throat in males; nuptial pad present on the inner side of base of fingers I in males in breading season; tadpole labial tooth row formula with 1:1+1/1+1:2. This population was probably Nidirana yeae sp. nov., and detailed comparisons especially with molecular data should be conducted to establish its identity. The phylogenetic trees in our work and Lyu et al. (2019a) all supported that the population from Hejiang County, Sichuan Province, China was the closest to topotypes of N. daunchina but separated from Nidirana yeae sp. nov. and other relatives, and so this population in the south-eastern part of Sichuan Province should be N. daunchina and not Nidirana yeae sp. nov. Although the morphometric data (large body size) of the population from Fanjiang Mountain of Jiangkou County in Wu et al. (1986) indicated that it was similar to N. leishanensis , we still need detailed comparisons and molecular data to clarify its taxonomic status.

Ecology.

Nidirana yeae sp. nov. is currently found from the paddy field (28.44317N, 107.02003E; ca. 1170 m a. s. l.) in Huanglian Town, Tongzi County, Guizhou Province, China. The individuals were found on the paddy field near an evergreen broad-leaved forest (Fig. 8 ). Tadpoles of the species could be found in the water. Two sympatric amphibians, Zhangixalus omeimontis (Stejneger, 1924) and Polypedates braueri (Vogt, 1911) were also found in the type locality.

Etymology.

The specific name yeae is in homage to the famous taxonomist Ye Chang-Yuan for her great contributions to Chinese amphibian research. For the common name, we suggest Ye’s Music Frog (English) and Ye Shi Qin Wa (Chinese).

Figures

Figure 3. Advertisement calls of Nidirana yeae sp. nov. (holotype CIBTZ 20190608004), N. daunchina (specimen CIB 2011081603) and N. yaoica (specimen SYS a 007009). A Waveform showing two-note call of Nidirana yeae sp. nov B sonogram showing two-note call of Nidirana yeae sp. nov C waveform showing two-note call of N. daunchina D sonogram showing two-note call of N. daunchina E waveform showing two-note call of N. yaoica F sonogram showing two-note call of N. yaoica.

Figure 4. Photos of the holotype CIBTZ 20190608004 of Nidirana yeae sp. nov. in life. A Dorsal view B ventral view C dorsal view of hand D ventral view of hand E ventral view of foot. Key: 1 indicates nuptial pad on the inner side of finger I.

Figure 5. The holotype specimen CIBTZ 20190608004 of Nidirana yeae sp. nov. and topotype specimen CIB 2011081603 of N. daunchina. A-C Dorsal view, ventral view and dorsolateral view of CIBTZ 20190608004 D-F dorsal view, ventral view and dorsolateral view of CIB 2011081603 G, H oral cavity of CIBTZ 20190608004 and CIB 2011081603 (arrow point to vomerine ridge) I, J dorsal view of hand of CIBTZ 20190608004 and CIB 2011081603 K, L ventral view of hand of CIBTZ 20190608004 and CIB 2011081603 M, N ventral view of foot of CIBTZ 20190608004 and CIB 2011081603.

Figure 6. Colour variation in Nidirana yeae sp. nov. A Dorsal view of male specimen CIBTZ 20190608003 B dorsal view of male specimen CIBTZ 20190608016 C dorsal view of female specimen CIBTZ 20190608005 D dorsal view of male specimen CIBTZ 20190608006 E ventral view of male specimen CIBTZ 20190608006 F ventral view of female specimen CIBTZ 20190608005.

Figure 7. The tadpole CIBTZ 20190608019 of Nidirana yeae sp. nov. in life. A Dorsal view B lateral view C ventral view D mouth structure. Key: 1, spiracle; 2, lower keratodonts; 3, additional tubercles at the angles of mouth; 4, upper keratodonts; 5, labial papillae on upper lips; 6, labial papillae on lower lips.

Figure 8. Habitats of Nidirana yeae sp. nov. in the type locality, Huanglian Town, Tongzi County, Guizhou Province, China. A Landscape of montane forests in the type locality B a paddy field occupied by the species in its type locality. insert: a male of Nidirana yeae sp. nov. in the paddy field.