Limnonectes lauhachindai, Aowphol, Anchalee, Rujirawan, Attapol, Taksintum, Wut, Chuaynkern, Yodchaiy & Stuart, Bryan L., 2015

Aowphol, Anchalee, Rujirawan, Attapol, Taksintum, Wut, Chuaynkern, Yodchaiy & Stuart, Bryan L., 2015, A new caruncle-bearing Limnonectes (Anura: Dicroglossidae) from northeastern Thailand, Zootaxa 3956 (2), pp. 258-270 : 259-268

Limnonectes lauhachindai sp. nov.

Holotype: NCSM 80222 (field tag AA 01384), adult male ( Fig. 1 ), Thailand, Ubon Ratchathani Province, Sirindhorn District, Kham Khuen Kaew Subdistrict, 15°17’47.6”N 105°28’22.0”E, 131 m elev., coll. 29 August 2012 by Anchalee Aowphol, Siriporn Yodthong, Natee Ampai, and Attapol Rujirawan.

Paratypes: NCSM 81269, ZMKU AM 01104–09 (seven adult males): same data as holotype. ZMKU AM 0 1111 (one adult male): same data as holotype except coll. 30 August 2012. ZMKU AM 00552–53, ZMKU AM 00586–92 (nine adult males; Fig. 2 ): same data as holotype except coll. 19 August 2011 by Attapol Rujirawan, Wut Taksintum, Virayuth Lauhachinda, Anchalee Aowphol, and Siriporn Yodthong.

FMNH 266148/ THNHM 0 5185, FMNH 266154/ THNHM 0 5189 (two adult males), FMNH 266147/ THNHM 0 5184, FMNH 266150/ THNHM 0 5025 (two adult females): Thailand, Ubon Ratchathani Province, Na Chaluai District, Phu Jong-Na Yoi National Park, Huay Luang Noi Stream, 14º26’15.9”N 105º16’48.2”E, 360 m elev., coll. 15 September 2004 by Yodchaiy Chuaynkern, Bryan L. Stuart, Chatchay Chuechat, and Sunchai Makchai. FMNH 266151/ THNHM 0 5026 (one adult female): same data as FMNH 266147/ THNHM 0 5184 except 14°25’43.9"N 105°16’51.0"E, 350 m elev. FMNH 266152/ THNHM 0 5187 (one adult female): same data as FMNH 266147/ THNHM 0 5184 except 14°26’18.6"N 105°16’04.5"E, 325 m elev.

Referred material. ZMKU AM 0 0 593 (one juvenile male), same data as ZMKU AM 0 0 586.

Etymology. The specific epithet is a patronym for Associate Professor Dr. Virayuth Lauhachinda, Kasetsart University, and co-collector of the new species, in recognition of his contributions to herpetology in Thailand.

Suggested common names. Lauhachinda's Fanged Frog (English), Kob Ngon Arjarn Virayuth ( Thai).

Diagnosis. Assigned to the genus Limnonectes on the basis of molecular evidence ( Fig. 3 ), the presence of fanglike odontoid processes on the lower jaw ( Emerson et al. 2000; Lambertz et al. 2014), and males with hypertrophied heads ( Lambertz et al. 2014). A small-sized Limnonectes having males with SVL 30.5–42.0, females with SVL 32.9–37.9; males with low-profiled, U-shaped caruncle with free posterior margin that completely occupies, but does not extend beyond, interobital region; males with hypertrophied heads; both sexes with enlarged odontoid processes on anterior margin of lower jaw; and webbing on toes.

additions of PWRC = Phu Luang Wildlife Research Centre Museum; RMB = Rafe M. Brown field series; and ZNAC = Anhui Normal University.

Description of holotype. Habitus moderately stocky; body tapering to groin. Head broad and depressed; head length and width subequal. Snout obtusely pointed in dorsal view, round in profile, projecting well beyond lower jaw in profile; nostril dorsolateral, much closer to tip of snout than to eye, below canthus, internarial distance subequal to interorbital distance; canthus rostralis indistinct, rounded, slightly constricted behind nostrils; lores concave, oblique; eye diameter 80% snout length, interorbital distance greater than upper eyelid width; pineal ocellus visible; tympanum round, not elevated from side of head, annulus weakly visible, tympanum diameter about 82% eye diameter and greater than distance between tympanum and eye; small, slit-like vocal sac openings on floor of mouth near lateral margin of tongue; vomerine teeth on two oblique ridges, equal in distance to each other as to choanae; two large odontoid processes at front of mandible; median triangular protuberance at mandibular symphisis.

Forelimb moderately robust. Fingers moderately slender, without webbing; tip of fingers rounded, weakly expanded into discs; relative finger lengths II <IV <I <III; moveable flap of skin on preaxial sides of Fingers II– IV; distinct subarticular tubercles, one on Fingers I–II, two on Fingers III–IV; distinct palmar tubercles, one at base of Finger I, two in contact as base of Fingers II–IV; nuptial pad absent.

Hindlimb moderately robust. Toes moderately slender; tips of toes rounded, expanded into small discs; relative toe lengths I<II<V<III<IV; webbing on Toe I to base of disc, on preaxial side of Toe II to midway between subarticular tubercle and tip and continuing as a fringe to base of tip, on postaxial side of Toe II to base of tip, on preaxial side of Toe III to level of distal subarticular tubercle continuing as a fringe to base of tip, on postaxial side of Toe III to base of tip, on preaxial and postaxial sides of Toe IV to level of distal subarticular tubercle and continuing as a fringe to base of tip, and on Toe V to base of tip; moveable flap of skin on outer margins of Toes I and V; distinct fold on distal half of tarsus; distinct, elongate, oval, inner metatarsal tubercle, length about 44% distance between tip of toe I and tubercle; no outer metatarsal tubercle.

Skin above shagreened with irregular rows of large oval warts, most concentrated near flank and lower back; low-profiled, U-shaped caruncle with free posterior margin that fully occupies, but does not extend beyond, the interorbital region; distinct supratympanic ridge from posterior corner of eye to axilla; large rictal gland; no dorsolateral fold; skin on venter smooth.

Measurements of holotype given in Table 2 .

Color of holotype in preservative. Dorsum dark brown; tips of dorsal warts white, warts encircled with black. Venter cream, chin dark brown, throat with large brown spots, belly and ventral surfaces of limbs with very small dark spots.

Color of paratype ZMKU AM 0 0 586 in life. Dorsum brown, with irregular black spots, becoming brassy on dorsal surfaces of limbs and upper flank; continuous black streak under canthus and supratympanic fold, extending from nostril to upper half of tympanum; lips brown with broad black bars; iris bronze; broad cream-yellow vertebral stripe from anterior margin of upper jaw to vent; upper surfaces of hindlimb with broad black bands; lower flank beige and gray ( Fig. 2 ).

Variation. Females lack caruncles and have narrower heads in dorsal view than males. The largest male paratype (ZMKU AM 01111; SVL 42.0 mm) is noticeably larger than the second largest (NCSM 81269; SVL 37.7 mm). Seven (NCSM 81269, ZMKU AM 0 1106, ZMKU AM 00552–53, ZMKU AM 00586–87, ZMKU AM 00593) of 25 (28%) specimens have a pale vertebral stripe, a polymorphic character seen in other Limnonectes , including L. dabanus and L. kohchangae ( Stuart & Emmett 2006; Stuart et al. 2006b). Measurements are summarized in Table 2 .

Molecules. The aligned dataset contained 1,624 characters. The new species was recovered as sister to a clade containing L. dabanus and L. gyldenstolpei ( Fig. 3 ). The holotype and six paratypes (NCSM 81269, ZMKU AM 01104–07, ZMKU AM 01109) are identical in the 16S gene fragment, but have an uncorrected pairwise divergence of 5.98–6.72% from L. dabanus (n =2) and 4.25–8.40% from L. gyldenstolpei (n =3).

Calls. Paratype male ZMKU AM 0 0 589 had two different advertisement call types, referred to here as Type 1 and Type 2 ( Fig. 4 ). Type 1 (n = 30) had 1–10, one-pulsed notes lasting 27.44 to 4342.91 ms; note duration of 10.29–34.50 ms; interval between notes 182.50–972.41 ms; note repetition rate of 0.98–4.00 notes per second; and dominant frequency of 1.12–2.33 kHz. Type 2 (n = 3) was a single, multi-pulsed note lasting 1749.06–2148.03 ms with 31–37 pulses; pulse duration of 21.24–25.00 ms; interval between pulses 33.74–35.36 ms; pulse rate 16.98– 17.49 pulses per second; and dominant frequency of 2.15–2.24 kHz ( Table 3 ). The advertisement calls were repeated at a rate of approximately 0.12 calls per second and intercall interval varied from 0.36 to 30.26 s. These calls showed frequency modulation with or without weak harmonics.

Distribution and natural history. Limnonectes lauhachindai sp. nov. is only known from Na Chaluai and Sirindhorn Districts, Ubon Ratachathani Province, Thailand ( Fig. 5 ), from 131–360 m elevation. Those from Na Chaluai District were taken on the bank or in the water of a shallow stream flowing over bedrock in semi-evergreen forest on a single day between 1400–2140 h. Those from Sirindhorn District were taken on the ground in deciduous dipterocarp forest with wet grassy understory ( Fig. 6 ). Eggs and larvae are unknown.

Comparisons. Limnonectes lauhachindai sp. nov. differs from all other species of Limnonectes except L. dabanus , L. gyldenstolpei , L. macrognathus and L. plicatellus by having mature males with a caruncle on top of the head. Limnonectes lauhachindai sp. nov. further differs from these four species by having males with a lowprofiled, U-shaped caruncle with free posterior margin that fully occupies, but does not extend beyond, the interorbital region (caruncle high-profiled and domed in L. dabanus ; caruncle extending beyond interorbital region in L. gyldenstolpei ; caruncle lacking U-shape and free posterior margin in L. macrognathus ; caruncle high-profiled and horned in L. plicatellus ; Fig. 7 ). Limnonectes lauhachindai sp. nov. further differs from L. dabanus , L. gyldenstolpei , and L. macrognathus by having much smaller males [SVL 52.9–65.5 (mean ± SD 59.8 ± 4.0, n = 15) in L. dabanus ; SVL 51.1–68.4 (mean ± SD 62.0 ± 5.7, n = 14) in L. gyldenstolpei ; SVL 43.2–48.8 (mean ± SD 45.5 ± 3.0, n = 3, this study), types SVL 47–57 (n = 2; Boulenger 1920) in L. macrognathus ], and from L. plicatellus by lacking dorsal rugosities arranged in distinct, longitudinal rows parallel to the body axis (present in L. plicatellus ).

Limnonectes lauhachindai sp. nov. superficially resembles L. hascheanus ( Stoliczka 1870) , L. limborgi ( Sclater 1892) , and L. kohchangae ( Smith 1922) , but differs from all of them by having cephalic caruncles in males (absent in L. hascheanus , L. limborgi , and L. kohchangae ). Limnonectes lauhachindai sp. nov. further differs from L. hascheanus by having larger body size [males with SVL 18.8–25.4, mean ± SD 22.1 ± 1.9, n = 9, females with SVL 20.5–25.0, mean ± SD 23.0 ± 1.6, n = 9, in L. hascheanus ( Inger & Stuart 2010) ], and from L. hascheanus and L. limborgi by having fully webbed toes (greatly reduced toe webbing in L. hascheanus and L. limborgi ).

Male secondary sexual characters are unknown in L. khammonensis ( Smith 1929) , which is known only from the female holotype, but females of L. lauhachindai sp. nov. differ by having a distinct tympanum (indistinct in L. khammonensis ) and less toe webbing (Toe IV webbed to distal subarticular tubercle, continuing as fringe to base of disc, and all remaining toes webbed to base of disc in L. khammonensis ).

Figures

FIGURE 1. Holotype (NCSM 80222) of Limnonectes lauhachindai sp. nov. in preservative. (A) Dorsal view. (B) Ventral view. (C) Plantar view of right foot. (D) Profile view of head.

FIGURE 2. Paratype male (ZMKU AM 00586) of Limnonectes lauhachindai sp. nov. in life.

FIGURE 3. Fifty percent majority-rule consensus phylogram resulting from Bayesian analysis of the mitochondrial 16 S gene from dicroglossid frogs. Numbers at nodes are Bayesian posterior probabilities. Numbers in parentheses are GenBank accession numbers. The source of sequences are given in Table 1.

FIGURE 4. Advertisement call of paratype male (ZMKU AM 00589) of Limnonectes lauhachindai sp. nov. recorded at an ambient air temperature of 24.0 ° C. (A) 26 s waveform showing five representative calls with two different call types: a) Type 1 and b) Type 2, (B) waveform of Type 1 call, (C) spectrogram of Type 1 call, (D) waveform of Type 2 call, and (E) spectrogram of Type 2 call.

FIGURE 5. Map illustrating the type (star) and paratype (circle) localities of Limnonectes lauhachindai sp. nov. in Ubon Ratchathani Province, Thailand.

FIGURE 6. Type locality of Limnonectes lauhachindai sp. nov. in Kham Khuen Kaew Subdistrict, Sirindhorn District, Ubon Ratchathani Province, Thailand.

FIGURE 7. Dorsal view of caruncle on top of head (above), with approximate margin of caruncle indicated in red (below). (A) Limnonectes lauhachindai sp. nov. (holotype). (B) L. dabanus (FMNH 262745). (C) L. gyldenstolpei (NCSM 79550).

Tables

TABLE 2. Measurements (mm) of types of Limnonectes lauhachindai sp. nov. Abbreviations defined in the text.

Measurement	Holotype male n =1	All males n =20 Range; Mean ± SD	Paratype females n =4 Range; Mean ± SD
SVL	35.9	30.5–42.0; 33.8 ± 2.8	32.9–37.9; 35.4 ± 2.6
HDL	16.8	13.7–20.6; 15.8 ± 1.5	13.8–15.8; 14.8 ± 0.9
HDW	16.6	13.6–20.0; 15.3 ± 1.4	13.1–15.3; 14.2 ± 1.0
SNT	6.3	4.7–6.8; 5.6 ± 0.6	5.2–5.8; 5.5 ± 0.3
EYE	5.0	4.0–5.7; 4.5 ± 0.4	4.7–5.1; 4.9 ± 0.2
IOD	3.6	2.9–4.2; 3.6 ± 0.3	2.1–3.6; 2.9 ± 0.6
TMP	4.2	3.0–5.0; 3.7 ± 0.4	2.9–3.4; 3.1 ± 0.2
IND	3.5	3.0–4.0; 3.4 ± 0.2	2.8–3.7; 3.3 ± 0.4
SHK	17.0	13.9–19.1; 15.8 ± 1.2	17.1–18.6; 17.7 ± 0.8
TGH	17.8	14.2–20.4; 16.7 ± 1.4	15.3–19.0; 17.3 ± 1.8
LAL	7.5	6.3–8.7; 7.0 ± 0.6	6.9–8.2; 7.5 ± 0.6
HND	8.5	6.9–9.8; 7.9 ± 0.7	6.8–9.0; 8.1 ± 1.0
FTL	16.7	14.1–19.2; 15.9 ± 1.1	16.6–19.0; 17.9 ± 1.1
IML	2.0	1.6–2.5; 2.0 ± 0.2	1.7–2.7; 2.2 ± 0.4
IMW	0.9	0.9–1.2; 1.0 ± 0.1	0.8–1.1; 1.0 ± 0.1

TABLE 3. Measurements of advertisement call parameters of paratype male (ZMKU AM 00589) of Limnonectes lauhachindai sp. nov. Parameter values are given as mean ± SD (and ranges).

Call parameter	Call type (number	of calls)
	Type 1 (n = 30)	Type 2 (n = 3)
Note description	1 note = 1 pulse	1 note = multi-pulses
Call duration (ms)	1807.15±1216.01; (27.44–4342.91)	1981.08±207.29; (1749.06–2148.03)
Intercall interval (ms)	7063.43±6180.57; (361.37–30262.46)
Call rate (calls/s)	0.12	0.12
Note	4.63±2.59; (1–10)	1
Note duration (ms)	18.37±6.80; (10.29–34.50)	1981.08±207.29; (1749.06–2148.03)
Internote interval (ms)	464.13±189.90; (182.50–972.41)	-
Note rate (notes/s)	2.16±0.78; (0.98–4.00)	-
Pulse	-	34.67±3.21; (31–37)
Pulse duration (ms)	-	22.78±1.97; (21.24–25.00)
Interpulse interval (ms)	-	34.47±0.82; (33.74–35.36)
Pulse rate (pulses/s)	-	17.25±0.26; (16.98–17.49)
Dominant frequency (kHz)	2.1±0.29; (1.12–2.33)	2.2±0.05; (2.15–2.24)