Clinotarsus penelope, Grosjean, Stéphane, Bordoloi, Sabitry, Chuaynkern, Yodchaiy, Chakravarty, Paramita & Ohler, Annemarie, 2015

Grosjean, Stéphane, Bordoloi, Sabitry, Chuaynkern, Yodchaiy, Chakravarty, Paramita & Ohler, Annemarie, 2015, When young are more conspicuous than adults: a new ranid species (Anura: Ranidae) revealed by its tadpole, Zootaxa 4058 (4), pp. 471-498 : 484-491

Clinotarsus penelope sp. nov.

Figs. 7 , 8

Holotype. Tadpole MNHN 2000.4630 in stage 36 ( Fig. 7 ) from the Namtok Raman Forest Park (8°27’ N, 98°32’ E, WGS 84, about 30 m asl), Phang Nga Province, Thailand, collected on 13 August 2000 by M. Delorme & A. Ohler. Specimen deposited in the collection of the Muséum national d’Histoire naturelle of Paris, France.

Paratopotypes. 46 tadpoles in stage 25, MNHN 2000.4601–4623 and MNHN 2000.4635–4657; two tadpoles in stage 26, MNHN 2000.4624–4625; one tadpole in stage 27, MNHN 2000.4626; one tadpole in stage 28, MNHN 2000.4627; three tadpoles in stage 34, MNHN 2000.4628 and MNHN 2000.4658–4659; two tadpoles in stage 35, MNHN 2000.4629 and MNHN 2000.4660; two tadpoles in stage 37, MNHN 2000.4631–4632; two tadpoles in stage 38, MNHN 2000.4633–4634; one tadpole in stage 43, MNHN 2000.8402, Namtok Raman Forest Park (8°27’ N, 98°32’ E, WGS 84, about 30 m asl), Phang Nga Province, Thailand, coll. M. Delorme & A. Ohler, on 13 August 2000.

Referred specimens. 34 tadpoles, THNHM 0 0 436, Khlong Ban Krang, Ban Krang Protected Unit, Kaeng Krachon National Park, Phetchaburi Province, Thailand, coll. Y. Chuaynkern, 25 July 2004; 12 tadpoles, THNHM 0 0 553 and 7 tadpoles, THNHM 0 0 546, Khlong Bang Po Ta, Khao Sok National Park, Surat Thani Province, Thailand, coll. T. Chan-ard & Y. Chuaynkern, 4 December 2003 and 26 December 2003, respectively; 3 tadpoles, MNHN 2010.1069–1071, Khlong Palian at junction of streams arising from Nam Tok Ton Tok and Nam Tok Ton Te, Trang Province, Thailand, coll. M. Kottelat, K. Kubota et al., 6 March 2001; 8 tadpoles, THNHM 0 1154, and 41 tadpoles, THNHM 0 1155, Khlong Rang Waterfall, Ngao National Park, Chumphon Province, Thailand, coll. Y. Chuaynkern, 27 November 2004; 9 tadpoles and some eggs, FMNH 206841, Klong Naka Nature Reserve (80 km south Ranong), Phang Nga Province, Thailand, coll. C. B. Frith & D. W. Frith, 6 December 1974; 7 adult males, THNHM 02648–51, THNHM 09647–48, FMNH 206815, and 1 female, FMNH 206814, Khlong Naka Wildlife Sanctuary, Kapoe District, Ranong Province, Thailand; 1 female, THNHM 0 0 487, and 1 male, THNHM 0 0 488, Huay Khayeng, Ban Tha Madeu, Nong Phling Swamp, Thong Pha Phum, Kanchanaburi Province, Thailand; 2 males, FMNH 213995–96, Tung Ma Lai District, Kanchanaburi Province, Thailand; 2 males, THNHM 01082–83, Pha To, Khlong Rang Waterfall, Ngo National Park, Chumphon Province, Thailand.

Two tadpoles ( THNHM 0 1379, Khlong Saeng Wildlife Sanctuary, Surat Thani Province, Thailand, coll. W. Thaksintham) present all the morphological characteristics of C. penelope but are quite small. TOL and BL of the stage 35 are 56.9 mm and 20.1 mm respectively and those of the stage 38 are 58.2 mm and 19.6 mm. They are then only referred to C. penelope here with caution.

Diagnosis (mostly copied from Grosjean et al. 2003). A large-sized tadpole (TL 16.4–92.7 mm, stages 25–38) beige-grey with black spots in tadpoles in stage 25 and uniformly black from stage 26, a large black ocellus with a red halo on caudal muscle at base of tail (followed by two smaller ones of decreasing size often poorly visible); a pair of large parotoid glands behind eyes, a pair of pectoral glands and a pair of ventroposterior ones, a supracaudal and an infracaudal gland; numerous white secretory pores on the ventral surface; a semi-circular snout; KRF 1– 2:(3+3)–(7+7)/1+1:4–8. This tadpole can be distinguished from the tadpole of C. alticola by its greater size at comparable developmental stage, by the presence of a totally differently coloured stage 25 (vs. identical to the other stages in C. alticola ), by its black coloration at stage 26 onwards (vs. beige in C. alticola ), by its semi-circular snout (vs. nearly rounded in C. alticola ), by presence of secretory pores on the ventral surface (vs. absent in C. alticola ), by the presence (often) of several ocelli (vs. only one in C. alticola ) and by elliptical elongate nares with dorsolateral projection (vs. round without projection).

Description of the holotype. The description of the holotype MNHN 2000.4630 in stage 36 is reproduced from Grosjean et al. (2003). For more information about the type series (measurements, variation, description of the buccal cavity) refer to Grosjean et al. (2003).

“ In dorsal view ( Fig. 7 B), body elliptical, widest at the posterior third; snout semi-circular. In profile ( Fig. 7 A), body depressed; body width 1.2 of body height; snout rounded. Eyes slightly bulging, directed almost laterally and positioned dorsolaterally, not visible in ventral view, diameter about 0.1 times snout-vent length. Nares oval, relatively small-sized, rimmed, with one anterolateral projection, positioned almost dorsally and directed slightly anterolaterally, distance between nares about 0.5 times interpupilar distance, closer to snout than to pupils. Spiracle sinistral, bulb-shaped, attached to body wall except at its extremity, positioned ventrolaterally, oriented more horizontally than posterodorsally; snout-spiracle distance 0.6 times snout-vent length. Spiracular opening oval, situated above level of hind limb. Tail musculature robust, gradually tapering, almost reaching tail tip. Tail fins moderately high, not extending onto body, riddled with numerous white pores on whole surface with secreted white mucus. A gland on the ventral fin, posterior to vent, the infracaudal gland; another at the beginning of dorsal fin, the supracaudal gland, slightly extending on body. Upper fin convex, slightly higher than lower; lower fin straight in proximal quarter, then slightly convex. Maximum tail height located 20–30 % from anterior end, tail tip rounded. Vent tube moderately large, roughly conical, opening with bevelled edge hidden by large flap of skin, directed posteriorly, linked to ventral tail fin, opening dextral. Presence of a pair of large parotoid glands behind eyes with pores visible without magnification, a pair of grey pectoral glands ventrally and a pair of ventral glands posteriorly situated at the level of hind limbs. Ventral surface also riddled with numerous white pores. All the pores secrete white mucus (probably produced under the stress of capture), particularly the parotoid glands and the supracaudal gland but also pores of caudal fins and ventral surface. Neuromasts not observed. Oral disk large, anteroventral, slightly emarginated, directed ventrally. Papillae of moderate size, finger-shaped, some bifid. Single row of papillae on median part of lower labium and at extremities of large medial gap of upper labium (five papillae on each side); up to five rows of submarginal papillae laterally; transverse row of submarginal papillae between accessory keratodont rows and lower keratodonts rows; accessory keratodont rows present on submarginal papillae and short ridges oriented at right angle to the keratodont rows. KF 2:6+6/1+1:8; keratodonts about 80 µm long with a curved spatulate apical portion bearing 26-29 (counted from six keratodonts from row P6) marginal denticles. Jaw sheaths slightly serrated, serrations black, distal half of sheaths dark brown, lower part white; upper sheath in wide flat arch slightly convex medially, lower sheath V-shaped.

In life, tadpole entirely brown-black, fins opaque, a black ocellus at the base of tail surrounded by a red halo. In preservative, back and flanks dark grey, ventral surface light grey with white pores; tail fins dark grey with white pores, caudal muscle dark brown with a black ocellus surrounded by a light orange halo.”

Measurements of the holotype (in mm). TL 77.7; BL 27.1; TAL 50.6; BH 13.8; BW 12.6; ED 3.1; IOD 9.7; NN 4.4; RN 3.1; NP 5.1; SS 16.6; SU 29.7; UF 4.3; LF 2.9; MTH 13.5; TMH 12.9; ODW 8.9; DG 4.8.

Variation. In addition to the variation described in Grosjean et al. (2003), observation of specimens of additional populations show the following differences: the tadpole of C. penelope can have from one to four ocelli, the fourth one being close to the middle one (three being the prevailing state). Number of ocelli can be asymmetrical on opposite sides of the tail. The posteroventral glands can be obscured by coloration. The acini opening of the caudal fins are surrounded by black halo in some specimens. The parotoid glands can be very protruding in some cases. Two out of the three specimens from Trang Province have only 6 lower uninterrupted keratodonts rows at stages 38 and 40. The largest size, 104.2 mm, is reached by a specimen in stage 37 from lot THNHM 0 1154.

Potential diagnosis of referred adult specimens (14 specimens listed in detail in the “Referred specimens” section above). These specimens are only referred to this species because they come from Museum collections and no tissue is available for barcoding them, precluding a definitive specific allocation. Nevertheless they are the only alticola -like frog found in this well-collected area. Moderate sized elongate frogs with head longer than broad, snout pointed, protruding, tympanum larger than half eye diameter but not nearly eye length, distance between upper eyelids larger than distance between nares, hand and fingers relatively short, finger and toe pads relatively narrow, webbing relatively more incurved; black band between nostril and eye absent, underside light brown, limbs with indistinct bands.

Description of adult voucher referred to Clinotarsus penelope (THNHM 0 2651, male from Khlong Naka Wildlife Sanctuary, Kapoe District, Ranong Province, Thailand) ( Fig. 8 ). (A) Size and general aspect. (1) Specimen of rather small size (SVL 37.7 mm), body slender.

(B) Head. (2) Head narrow, longer (HL 16.3 mm) than wide (HW 12.7 mm; MN 13.8 mm; MFE 10.1 mm; MBE 5.5 mm), flat above. (3) Snout pointed, protruding; its length (SL 7.11 mm) longer than horizontal diameter of eye (EL 4.64 mm). (4) Canthus rostralis rounded, loreal region concave; obtuse in cross section (5) Interorbital space flat, about as large (IUE 3.92 mm) as upper eyelid (UEW 3.19 mm) and as internarial distance (IN 3.19 mm); distance between front of eyes (IFE 7.1 mm) about three-quarters of distance between back of eyes (IBE 10.0 mm). (6) Nostrils oval, without flap of skin; closer to tip of snout (NS 2.92 mm) than to eye (EN 3.63 mm). (7) Pupil indistinct. (8) Tympanum ( TYD 3.48 mm) very distinct, rounded; tympanum-eye distance (TYE 0.73 mm) one fifth its diameter. (9) Pineal ocellus present, between anterior border of eyes. (10) Vomerine ridge present, bearing four small teeth; between choanae, with an angle of 45° to body axis, closer to choanae than from each other, shorter than distance between them. (11) Tongue large, spatulate, emarginate; median lingual process absent. Tooth-like projection on maxilla absent.

(C) Forelimbs. (12) Arm short, thin, fore-arm (FLL 9.4 mm) shorter than hand (HAL 10.8 mm), not enlarged. (13) Fingers I to IV rather long and thin (TFL 6.7 mm). (14) Relative length, shortest to longest: II <I <IV <III. (15) Tips of fingers I to IV pointed, enlarged; latero-ventral grooves on fingers I to IV, very wide compared to finger width (pad width of finger III 0.86 mm; width of finger III 0.61 mm). (16) Fingers without webbing. (17) Subarticular tubercles all present, distinct, oval, single. (18) Prepollex oval, prominent; two oval, flat palmar tubercles present; supernumerary tubercles absent.

(D) Hind limbs. (19) Shanks thin, seven times longer (TL 20.7 mm) than wide (TW 2.6 mm), shorter than thigh (FL 21.4 mm) but longer than distance from base of internal metatarsal tubercle to tip of toe IV (FOL 18.4 mm). (20) Toes long, thin, toe IV (FTL 10.6 mm) longer than third of distance from base of tarsus to tip of toe IV (TFOL 27.1 mm). (21) Relative length of toes, shortest to longest: I <II <III <V <IV. (22) Tips of toes pointed, enlarged, ventrolateral grooves on toes I to V (pad width of toe IV 0.86 mm, width of toe IV 0.61 mm). (23) Webbing rather large: I 0—1 ½ II 0— 2 III 0— 2 IV 2—0 V (MTTF 10.1 mm; MTFF 10.8 mm; FTFT 7.6 mm; FFTF 7.8 mm). (24) Dermal ridge along toe V from tip of toe to proximal subarticular tubercle absent. (25) Subarticular tubercles all present, prominent, oval, simple. (26) Inner metatarsal tubercle rather short, prominent, its length (IMT 1.23 mm) 3.5 times in length of toe I (ITL 4.30 mm). (27) Tarsal fold absent. (28) Outer metatarsal tubercle present, rounded; supernumerary tubercles and tarsal tubercle absent.

(E) Skin. (29) Dorsal and lateral parts of head and body: snout, upper head and back shagreened; side of head smooth; flank with poorly distinct glandular warts. (30) Latero-dorsal folds flat, narrow, from eye to groin; “Fejervaryan” line absent; lateral line system absent; supratympanic fold poorly distinct, from eye to above shoulder; cephalic ridges absent; co-ossified skin absent. (31) Dorsal parts of limbs smooth. (32) Ventral parts of head, body and limbs: throat, chest, belly and ventral part of thigh smooth; posterior part of thigh near vent with treefrog belly skin. (33) Macroglands: a flat rectal gland present.

(F) Coloration in alcohol. (34) Dorsal and lateral parts of head and body: dorsal parts of head and body light brown; flanks brown getting clearer ventrally; loreal region clear, tympanic region brown, tympanum light brown, transparent; upper lip with a brown band, larger on snout, and a white glandular line. (35) Dorsal parts of limbs light brown with indistinct darker bands; posterior part of thigh brown. (36) Ventral parts of head, body and limbs: throat light brown with a beige band in the center; margin of throat light brown; chest, belly and thigh light brown, with white spots on chest and belly; webbing brown.

(G) Male secondary sexual characters. (37) Nuptial spines on first finger; with small white spinules forming small round pad on the articulation of phalanges two and three. (38) Vocal sacs present, indistinct on throat, with rounded openings posterior on mouth floor. (39) No other secondary sexual characters known.

(H) Female sexual characters (FMNH 206814). (40) Oviduct not observed. (41) Ovary with small entirely dark brown oocytes.

Variation and comparison of adult specimens of C. alticola and C. penelope . The morphological measurements are given in Table 4 and a multivariate analysis of measurements is presented in Fig. 9 and Table 5. Under univariate analysis there are few statistically significant measurements that distinguish the two species. Nevertheless they have minute differences in head, hand and foot morphology: Clinotarsus alticola have a larger head, as expressed by significant higher values of IFE (larger distance between anterior border of eyes) and IN (larger distance between nostrils) than C. penelope . Clinotarsus penelope has significantly longer inner metatarsal tubercle and a more incurved webbing (larger value of TFTF). On the other hand the first two factors of Principal Component Analysis ( Fig. 9 , Table 5) do not allow to separate the two species.

Clinotarsus alticola Clinotarsus penelope Mann Whitney

Males

Measurement adult males (n = 3) adult males (n = 12) adult females (n = 2)

SVL 35.4 ± 3.9 (31.3–39.1) 38.5 ± 3.2 (34–45.8) 45.3–45.4 U = 10, p = 0.295 n.s. rhw 316 ± 27.9 (284–332) 325 ± 18.4 (298–352) 303–313 U = 14, p = 0.633 n.s. rhl 403 ± 25.3 (384–431) 418 ± 17.3 (385–439) 409–410 U = 10, p = 0.295 n.s. rmn 341 ± 16.5 (325–358) 360 ± 9.5 (340–374) 349–353 U = 5, p = 0.07 n.s. rmfe 254 ± 24.1 (235–281) 247 ± 22.5 (182–267) 250–253 U = 16, p = 0.84 n.s. rmbe 140 ± 12.7 (125–148) 156 ± 40.5 (126–281) 161–164 U = 14, p = 0.633 n.s. rife 197 ± 1.5 (195–198) 182 ± 6.8 (166–191) 154–168 U = 0, p = 0.004 ** ribe 268 ± 14.1 (258–284) 262 ± 14.1 (237–281) 252–255 U = 14, p = 0.633 n.s. rin 99 ± 11.6 (90–112) 87 ± 3.8 (81–93) 77–77 U = 3, p = 0.031 *

ren 107 ± 7.8 (100–115) 102 ± 9.7 (80–117) 96–102 U = 15, p = 0.734 n.s. rel 132 ± 10.9 (123–144) 121 ± 12.7 (104–150) 99–109 U = 10, p = 0.295 n.s. rtyd 93 ± 5.3 (89–99) 88 ± 10.9 (62–105) 51–64 U = 13, p = 0.536 n.s. rtye 19 ± 3.7 (16–23) 26 ± 6.4 (17–37) 35–38 U = 7, p = 0.136 n.s. riue 107 ± 7.6 (100–115) 104 ± 4.4 (96–111) 90–99 U = 14, p = 0.633 n.s. ruew 82 ± 17.9 (64–100) 84 ± 6.7 (66–93) 74–77 U = 15, p = 0.734 n.s. rfll 230 ± 15.3 (220–248) 239 ± 15.4 (210–274) 242–247 U = 13, p = 0.536 n.s. rhal 265 ± 25.1 (240–290) 288 ± 17.3 (259–315) 291–303 U = 11, p = 0.365 n.s. rtfl 167 ± 14.3 (159–184) 181 ± 13.5 (155–202) 184–197 U = 9, p = 0.233 n.s. rfd3 32 ± 2.1 (30.7–34.8) 28 ± 3.8 (22–34) 28–39 U = 5, p = 0.07 n.s. rfw3 14 ± 1.3 (12.8–15.4) 16 ± 2.4 (11–19) 18–19 U = 9, p = 0.233 n.s. rtl 570 ± 38 (540–613) 551 ± 19.4 (521–581) 544–568 U = 12, p = 0.448 n.s. rfol 456 ± 31.1 (422–482) 475 ± 25.2 (442–523) 478–493 U = 11, p = 0.365 n.s. rftl 259 ± 33.6 (220–279) 276 ± 22 (230–320) 268–289 U = 12, p = 0.448 n.s. rimt 29 ± 3.2 (26–32) 40 ± 4 (33–46) 41–43 U = 0, p = 0.004 ** ritl 111 ± 15.2 (96–126) 112 ± 6.9 (103–127) 115–127 U = 15, p = 0.734 n.s. rmttf 252 ± 34.1 (224–290) 254 ± 14 (231–273) 255–264 U = 14, p = 0.633 n.s. rmtff 280 ± 35 (252–319) 280 ± 20.6 (234–307) 273–284 U = 16, p = 0.84 n.s. rtftf 179 ± 25 (150–197) 203 ± 12.9 (178–227) 206–212 U = 4, p = 0.048 *

rfftf 178 ± 17.2 (163–197) 198 ± 13.9 (178–223) 203–206 U = 6, p = 0.101 n.s. rtd4 30 ± 3.7 (25.6–32) 28 ± 3.3 (23–32) 30–34 U = 15, p = 0.734

rtw4 16 ± 2.6 (14.2–19.2) 15 ± 1.7 (12–18) 16–18 U = 13, p = 0.536 n.s.

Distribution limited to the tadpole data ( Fig. 10 ). Thailand: Namtok Raman Forest Park (8°27’N, 98°32’E, about 30 m above sea level), Phang Nga Province (type locality). Localities of referred specimens: Kaeng Krachon National Park, Phetchaburi Province; Khao Sok National Park, Surat Thani Province; Khlong Palian at junction of streams arising from Nam Tok Ton Tok and Nam Tok Ton Te, Trang Province, Khlong Rang Waterfall, Ngao National Park, Pha To, Chumphon Province. Smith (1930) mentioned the presence of “ Rana alticola ” in the province of Nakhon Si Thammarat which fills a gap between the provinces of Surat Thani and of Trang.

Etymology. This species is dedicated to the daughter of the first author, Pénélope . The nomen is used as a noun in apposition to generic substantive.

Conservation status. DD, Data Deficient as the distribution range and the specific threats of the new species have not been properly assessed.

Component Initial Eigenvalues / Extraction sum of squared loadings

Total % of Variance Cumulative %

1 9.617 31.023 31.023 2 5.300 17.097 48.120 3 3.053 9.849 57.969 4 2.716 8.760 66.729 5 2.294 7.400 74.129 6 1.917 6.184 80.313 7 1.523 4.911 85.224 8 1.271 4.099 89.323 continued.

Components

1 2 3 4 5 6 7 8

svl 0.523 0.155 0.003 0.327 -0.101 -0.608 -0.337 0.125 rhw 0.642 -0.264 0.487 0.228 -0.094 0.055 0.058 0.046 rhl -0.494 0.368 0.454 0.433 -0.004 0.348 -0.009 0.271 rmn -0.653 0.374 0.137 0.392 0.227 0.176 -0.106 0.241 rmfe 0.244 -0.098 -0.187 0.430 -0.276 0.472 -0.585 0.157 rmbe -0.321 0.119 0.502 -0.108 0.374 -0.194 0.607 0.149 rife -0.062 -0.324 0.088 0.574 -0.484 0.243 0.337 -0.336 ribe -0.169 -0.247 0.814 0.043 0.198 0.357 -0.050 -0.130 rin 0.725 -0.626 0.160 0.003 0.000 0.104 0.100 0.125 ren -0.690 0.149 0.328 0.151 -0.343 0.070 0.023 0.315 rel 0.408 -0.684 -0.271 0.300 0.258 0.136 0.050 -0.063 rtyd -0.085 -0.494 -0.154 0.705 0.132 -0.056 0.343 0.069 rtye 0.284 0.473 0.570 -0.079 -0.169 -0.136 -0.273 0.332 riue -0.898 -0.026 0.287 0.039 -0.073 0.202 -0.031 -0.179 ruew 0.474 -0.203 0.357 0.197 0.643 -0.160 -0.187 -0.019 rfll -0.041 0.309 0.450 -0.287 -0.506 -0.245 -0.007 -0.265 rhal -0.269 0.817 -0.084 0.065 0.113 0.261 0.169 -0.019 rtfl -0.404 0.563 -0.521 0.173 0.365 0.236 0.089 0.055 rtl 0.717 0.172 -0.046 0.272 -0.285 0.100 -0.074 -0.276 rfol 0.843 0.390 0.019 0.136 -0.174 0.128 0.170 0.086 rftl 0.828 0.427 -0.016 0.124 -0.171 0.018 0.249 0.021 rimt 0.604 0.206 -0.006 0.021 0.449 0.088 -0.050 -0.028 ritl 0.618 0.629 -0.299 0.140 -0.027 0.128 0.119 -0.003 rmttf 0.942 0.133 0.056 0.102 -0.012 -0.059 0.136 0.156 rmtff 0.862 0.235 0.046 0.161 -0.032 0.016 0.100 0.203 rtftf -0.055 0.789 -0.003 0.057 0.295 0.031 -0.117 -0.349 rfftf 0.419 0.637 0.288 0.105 0.255 0.058 -0.151 -0.428 rfd3 0.124 -0.115 -0.193 -0.597 -0.173 0.617 0.003 0.079 rfw3 0.655 0.347 0.076 -0.409 -0.158 0.195 0.302 0.111 rtd4 0.545 -0.276 0.027 -0.446 0.333 0.294 -0.124 0.231 rtw4 0.578 -0.394 0.405 -0.115 0.145 0.273 -0.071 -0.278

Figures

FIGURE 7. Pictures of the holotype of Clinotarsus penelope sp. nov., MNHN 2000.4630 in stage 36; lateral (A) and dorsal (B) views.

FIGURE 8. Clinotarsus penelope sp. nov. THNHM 0 2651, potential adult male, described voucher, SVL 37.7 mm.

FIGURE 9. Scatter plot of Factor 1 and 2 of Principal Component Analysis including potential adult males and females of Clinotarsus penelope sp. nov. and Clinotarsus alticola based on 31 measurements.

FIGURE 10. Distribution map of Clinotarsus penelope sp. nov. limited to the tadpole data. Red star indicates the type locality.