Leptolalax aereus, Phimmachak, Sompouthone & Sivongxay, Niane, 2010

Phimmachak, Sompouthone & Sivongxay, Niane, 2010, A new species of Leptolalax (Anura: Megophryidae) from Laos, Zootaxa 2681, pp. 35-46 : 36-44

Leptolalax aereus sp. nov.

Holotype: SAMA R64236, adult male, calling on mid-stream rock pile in 6 m wide, swift rocky stream in semi-evergreen forest in the Sepon Mining Tenement, Vilabouli District, Savannakhet Province, Laos (16.96317º N, 106.0466º E, 326 m), collected at 21:36 h on 23 November 2008 by B. L. Stuart, S. J. Richards, S. Phimmachak and N. Sivongxay.

Paratypes: NCSM 76038, SAMA R64234–64235 (three males), same data as holotype but collected near a swift, rocky stream. SAMA R64237 (one male), same locality data as holotype but collected on 25 November 2008. NCSM 76041–76044 (four males) and NCSM 76039–76040, SAMA R64238–63240 (five females), from the Sepon Mining Tenement, Vilabouli District, Savannakhet Province, Laos (16.95653º N, 106.0677º E, 303 m), collected on 26 November 2008; NCSM 76045 (female), and SAMA R64241 (male), collected at same site on 28 November 2008; NCSM 76046 (female) collected at same site on 30 November 2008. NCSM 76047 (male) from the Sepon Mining Tenement, Vilabouli District, Savannakhet Province, Laos (16.03939º N, 106.1567º E, 284 m), collected on 7 December 2008. SAMA R64242 (male) from the Sepon Mining Tenement, Province, Laos (17.011806º N, 106.220139º E, 353 m), collected on 6 December 2008. NCSM 76049–76051 (three males) and NCSM 76048 (female) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.02141º N, 106.2904º E, 474 m), collected on 22 June 2009; NCSM 76053 (male) collected at same site on 23 June 3009; NCSM 76054–76056 (three males) and NCSM 76061 (female) collected at same site on 24 June 2009. NCSM 76052 (male) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.02161° N, 106.2890º E, 450 m), collected on 23 June 2009; NCSM 76065 (male) and NCSM 76066 (female) collected from same site on 29 June, 2009. NCSM 76057 (female) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.0257º N, 106.2944º E, 511 m), collected on 24 June 2009. NCSM 76062 (male) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.01874º N, 106.2973º E, 465 m), collected on 25 June, 2009. NCSM 76063 (female) and NCSM 76064 (male) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.02345º N, 106.2894º E, 438 m), collected on 26 June 2009. NCSM 76067–76069 (three males) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (16.01816º N, 106.2973º E, 470 m), collected on 30 June 2009. NCSM 76070– 76071 (two males) from the Sangi River drainage basin, Vilabouli District, Savannakhet Province, Laos (17.02073º N, 106.2862º E, 454 m), collected on 1 July 2009. Specimens from 2008 were collected by B. L. Stuart, S. J. Richards, S. Phimmachak and N. Sivongxay. Specimens from 2009 were collected by B. L. Stuart, S. Phimmachak and N. Sivongxay.

Etymology. Specific epithet from aereus L., meaning made of copper or bronze; in reference to copper hue evident in life on the dorsal surface of most specimens.

Diagnosis. Assigned to the genus Leptolalax on the basis of the following: small size, rounded finger tips, the presence of an elevated inner palmar tubercle not continuous to the thumb, presence of macroglands on body (including supra-axillary, pectoral, ventrolateral and femoral glands), vomerine teeth absent, tubercles on eyelids, anterior tip of snout with pale, vertical bar (Dubois 1980; Lathrop et al. 1998; Delorme et al. 2006). Leptolalax aereus sp. nov. is distinguished from its congeners by a combination of (1) size (25.1–28.9 mm in 28 adult males, 27.1–38.6 mm in 12 adult females), (2) absence of distinct black or dark brown dorsolateral markings on head, (3) near immaculate white chest and belly, (4) head length greater than head width, (5) no webbing or lateral fringing on fingers, (6) rudimentary webbing between toes I–IV, no webbing between toes IV–V; toes with very weak lateral fringing, (7) a call consisting of an average of 3–4 notes containing 1–2 pulses, and with a dominant frequency of 6187.5–7875 Hz.

Description of holotype. Head longer than wide; snout rounded in profile, projecting slightly over lower jaw; nostril closer to tip of snout than eye; canthus rostralis rounded; lores sloping; vertical pupil; eye diameter approximately equal to snout length; tympanum distinct, round, diameter 56% that of the eye, tympanic annulus not elevated relative to skin of temporal region; vomerine teeth absent; pineal ocellus absent; vocal sac openings large, oval, located laterally on floor of mouth; paired internal subgular vocal sac; tongue large, broad, with small notch at narrowed, posterior tip; distinct, raised supratympanic ridge running from eye towards axillary gland. Tips of fingers rounded, not broader than phalanges; finger I almost as long as finger II, relative finger lengths I <II = IV <III; nuptial pads absent; subarticular tubercles absent; a large, laterally compressed inner palmar tubercle distinctly separated from smaller, laterally compressed outer palmar tubercle; no finger webbing or lateral fringes. Tips of toes like fingers; relative toe length I <II <V <III <IV; subarticular tubercles absent, replaced by dermal ridges, distinct on second, third, fourth and fifth toes; small, oval inner metatarsal tubercle pronounced, outer metatarsal tubercle absent; webbing rudimentary between toes I–IV, absent between toes IV–V; toes with very weak lateral fringing. Tibia approximately half that of snout-vent length; tibiotarsal articulation reaches to tip of snout. Skin on entire dorsum with low, round or laterally compressed tubercles, more frequent and larger on posteriodorsal and dorsolateral surfaces, forming faint ridges on dorsal surface of thighs and upper arms; ventral skin smooth; pectoral gland laterally compressed, 1.0 mm diameter; femoral gland oval, 0.9 mm diameter, on posteroventral surface of thigh, closer to knee than to vent; supra-axillary gland raised, 0.8 mm diameter; many small glands around cloacal opening. Ventrolateral glands present, dorsolaterally compressed, forming an incomplete line.

Colour of holotype in life. Dorsum brown with copper/orange wash, axilla to elbows and heel orange. Dorsal surface of head pale copper. Darker greyish-brown interorbital bar, W-shaped marking between axillae, inverted V-shaped marking between sacrum, darkening towards inguinal region; pale greyish-brown bars on background of pale orange on upper lip; loreal and tympanic region with no distinct dark brown or black markings; diffuse, transverse greyish-brown bars on dorsal surface of limbs; ventral surface of elbow and upper arm without dark bars; fingers and toes with faint transverse barring. Small greyish-brown flecks along flanks. Ventral surface of chest and belly opaque white; throat transparent pale pink; outer edges of chin, and thighs, arms and all of tibiotarsus brownish grey with small whitish spots. Supra-axillary gland orange; femoral, pectoral and dorsolateral glands white. Iris bronze with minute, black reticulations.

Colour of holotype in preservative. Dorsal surface brown; ventral surface, including throat, white. Ventrolateral margins of chest and belly and margins of throat with brown speckling. Ventral surfaces of thighs and arms cream to pale brown with white speckling. Dark greyish brown and white flecks on flanks. White macroglands and pectoral glands have become indistinct in preservative.

Measurements. Holotype: SVL 28.7, HDL 11.0, HDW 10.2, SNT 4.2, EYE 3.6, IOD 3.2, TMP 2.0, TEY 1.0, TIB 14.6, ML 7.5, PL 14.1, F1L 3.1, F2L 3.5, F3L 5.9.

Variation. Colour of paratypes varied slightly in life. NCSM 76065 and SAMA R64242 had more extensive dusting or spotting on throat and lateral margins of belly than holotype. Colour of NCSM 76054 appears aberrant among the type series, exhibiting large black patches on ventral surfaces of legs, chest and throat. Some individuals have slightly more extensive webbing (NCSM 76039, NCSM 76043, NCSM 76045, NCSM 76064, SAMA R64239, SAMA R64242) or lateral fringing (NCSM 64242) on feet. Ventrolateral glandular lines vary in degree of completeness and distinctiveness, and are indistinct in SAMA R64242, NCSM 76048, NCSM 76046, NCSM 76049, NCSM 76057, NCSM 76062, and NCSM 76065. Glands around cloacal opening vary in size and number. Skin less tuberculate in preservative than in life. In preservative dorsal skin texture varies from finely tuberculate (NCSM 76040, NCSM 76044–76045, NCSM 76048, NCSM 76066, NCSM 76068, SAMA R64239) to almost smooth (NCSM 76038, NCSM 76041–76043, NCSM 76047, NCSM 76049–76050, NCSM 76052, NCSM 76054, NCSM 76056–76057, NCSM 76061–76063, NCSM 76069–76071, SAMA R64234–64238, 64240–64242). Females are significantly larger than males (Mann-Whitney U -test, Z= -4.460, p <0.001; N=40), and in life, have opaque whitish throats, compared to transparent pale pink throats of males. Measurements of the type series are shown in Table 1.

Range; Mean ± S. D. (N=26) Range; Mean ± S. D. (N=12)

SVL 25.1–28.9; 27.3 ± 0.9 27.1–38.6; 34.7 ± 2.9 HDL 9.6–11.0; 10.2 ± 0.3 10.2–13.7; 12.8 ± 0.9 HDW 8.8–10.2; 9.5 ± 0.3 9.6–13.1; 12.1 ± 0.9 SNT 3.3–4.2; 3.8 ± 0.2 3.7–5.3; 4.5 ± 0.4

EYE 3.0–3.9; 3.4 ± 0.2 3.1–5.1; 4.1 ± 0.5

IOD 2.2–3.5; 2.8 ± 0.3 2.9–3.6; 3.2 ± 0.2

TMP 1.6–2.0; 1.8 ± 0.1 1.9-2.4; 2.2 ± 0.1

TEY 0.6–1.2; 0.9 ± 0.1 0.9–1.6; 1.3 ± 0.2

TIB 12.8–14.7; 13.8 ± 0.5 13.1–18.6; 16.9 ± 1.3 ML 6.3–7.5; 7.0 ± 0.3 6.6–9.2; 8.3 ± 0.7

PL 12.1–14.1; 13.0 ± 0.6 12.8–17.7; 15.8 ± 1.3 F1L 2.3–3.1; 2.7 ± 0.2 2.5–3.9; 3.4 ± 0.4

F2L 2.6–3.5; 3.0 ± 0.2 2.9–4.3; 3.7 ± 0.3

F3L 4.6–6.8; 5.7 ± 0.4 5.3–7.5; 6.9 ± 0.6

Range; Median (N=26) Range; Median (N=12) TIB:SVL 0.48–0.53; 0.50 0.46–0.53; 0.49

HDL:SVL 0.36–0.39; 0.37 0.34–0.38; 0.37

HDL:HDW 1.03–1.14; 1.07 1.05–1.08; 1.06

Advertisement call. Call descriptions are based on the calls of the holotype (SAMA R64236), recorded at 22.4°C ambient temperature ( Table 2, Figures 5 A–D). Calls were approximately 30 ms in duration, and repeated at a variable rate, averaging approximately six calls per second. Each call consisted of three, or occasionally four notes of 6–9 ms duration, and each note contained 1–2 pulses. Within each call, notes were repeated at a rate of approximately 40–45 notes per second. The dominant frequency of the calls was 6187.5– 6375 Hz, however energy was spread over a fairly wide band (5500–7000 Hz). Faint harmonics were detected at approximately 12750 Hz, and the fundamental frequency was absent ( Figure 5 C). Frequency modulation was weak or absent, with successive notes often declining slightly in frequency in the order of 100–200 Hz. Amplitude modulation was present, with calls tending to decline in intensity with successive notes. The advertisement call of paratype NCSM 76068, taken at 25.5ºC ambient temperature, had a higher note repetition rate and was more variable than that of SAMA R64236 ( Figures 5 E–H). Call interval, call rate and the number of notes within each call were highly variable both within and among individuals (N=6, Table 2). Although the intensity and rate of calling increased and decreased during bouts of calling in all recordings, calls did not form distinct call groups (in up to 204 s of calling). The dominant frequency was positively correlated with temperature ( Figure 6 ). To the human ear, the advertisement call of L. aereus is a high-pitched, rapid chirping, sounding similar to an orthopteran.

Ecology. Leptolalax aereus was abundant at rocky streams in closed evergreen or semi-evergreen forest. All known locations are between 284–511 m elevation, and animals were collected at night between 20:25– 23:15 h. Males were observed calling from crevices between boulders, on rocks, and on stream banks. Females were found on rocks mid-stream, and up to 1 m from the streams. Leptolalax aereus was heard calling in both June and November, suggesting that breeding may occur throughout the year.

Conservation status. To date, the new species is only known from Vilabouli District, Savannakhet Province, Laos, but it probably occurs in other suitable habitats in adjoining areas of Laos and Vietnam. Although it appears to require closed evergreen or semi-evergreen forest along the streams where it occurs, several of the streams where we documented this species run through severely degraded habitats, suggesting means (and ranges).

SAMA NCSM 76054 NCSM 76064 NCSM 76065 NCSM 76067 NCSM 76068 R64236*

Number of notes 59 102 189 62 62 70

measured

at least some ability for populations to persist in substantially modified habitats as long as sufficient riparian evergreen forest is retained. Until the distribution and habitat requirements of this species are more adequately documented, we suggest the species should be considered Data Deficient following IUCN’s Red List categories ( IUCN 2001).

Comparisons. Leptolalax aereus is a medium-sized species of Leptolalax (25.1–28.9 mm in 28 adult males, 27.1–38.6 mm in 12 adult females), and can be distinguished on the basis of size from the smaller L. applebyi (males 19.6–20.8 mm, female 21.7 mm), L. kecil (males 19.3–20.5 mm, female 25 mm), L. melicus (males 19.5–22.7 mm) and L. pluvialis (males 21.3–22.3 mm), and the larger L. bourreti (male 36.2 mm), L. gracilis (males 30–36 mm), L. kajangensis (males 34–35 mm), L. nahangensis (male 40.8 mm), L. sungi (males 48.3–52.7 mm, females 56.7–58.9), and L. tamdil (male 32.3 mm, female 31.8 mm).

In lacking distinct dark dorsolateral markings on the head, L. aereus can be distinguished from L. alpinis , L. applebyi , L. bourreti , L. dringi , L. fulignosus , L. hamidi , L. heteropus , L. kajangensis , L. khasiorum , L. kecil , L. melanoleucus , L. melicus , L. nahangensis , L. oshanensis , L. pelodytoides , L. pictus , L. pluvialis , L. solus , L. sungi and L. tamdil , all of which have dark canthal and/or temporal streaks.

In having an immaculate white chest and belly with only slight darker specking at margins, L. aereus can be distinguished from L. alpinis , L. applebyi , L. croceus , L. dringi , L. fulignosus , L. gracilis , L. heteropus , L. kajangensis , L. kecil , L. maurus , L. melanoleucus , L. melicus , L. nahangensis , L. pluvialis , L. solus , L. tuberosus and L. ventripunctatus , all of which have dark or otherwise maculate chests and/or bellies.

Leptolalax aereus , with a head longer than wide, can be further distinguished from L. bourreti , L. croceus , L. khasiorum , L. lateralis , L. tamdil and L. tuberosus , all of which have heads wider than long. In having rudimentary webbing between toes I–IV, no webbing between toes IV–V; and toes with weak lateral fringing, L. aereas can be differentiated from L. alpinis and L. liui , which have wide lateral fringing on toes, and from L. pelodytoides , which has more extensive webbing and wide lateral fringes between toes. The advertisement call of L. aereas appears structurally unique among Leptolalax in terms of the degree of variability in call interval, call rate and number of notes per call within and among recorded calls. In lacking strong frequency modulation, the call of L. aereus differs from L. dringi and L. hamidi . In having an extremely high frequency (6000–7000 Hz) the call of L. aereus can be distinguished from that of L. applebyi (3962–4306.6 Hz, 21.5ºC), L. croceus (2625–3000 Hz, 21.6–25.1ºC), L. fuliginosus (2250–2430 Hz, 19.3–19.6 ºC), L. gracilis (2540– 2650 Hz, 20ºC), L. heteropus (2833 Hz, 21ºC), L. kecil (3200 Hz, 21.4ºC), L. melanoleucus (3050–3200 Hz, 23.9ºC), L. melicus (3560–3610 Hz, 26.1–26.2 ºC), L. oshanensis (4402–4633 Hz, 14ºC; recorded from c. 40 km from type locality of L. oshanensis ), L. solus (3100–3200 Hz, 24.2–24.3ºC), and L. tuberosus (2584– 2756.2 Hz, 22.5-24.5 ºC). Although frequency can vary with temperature, differences among species of the scale reported here are extremely unlikely to be attributed to temperature differences.

Leptolalax aereus is morphologically most similar to L. oshanensis , but differs from it by its call (above), and by lacking a distinct black line under the supratympanic fold and distinct black inter-orbital blotches that abut the inner margins of the orbital bulge (present in all L. oshanensis examined). Leptolalax aereas is also grey in preservative (compared to brown for L. oshanensis ). Male L. aereus and male L. oshanensis do not differ in SVL (male L. aereus mean SVL 27.3 ± 0.9 S. D., male L. oshanensis mean SVL 27.2 ± 0.7 S. D.; Mann-Whitney U -test, Z= -0.641, p = 0.522; N=42), but L. aereus males have a greater head length (male L. aereus mean HDL 10.2 mm ± 0.4 S. D., male L. oshanensis mean HDL 9.7 mm ± 0.3 S. D.; Mann-Whitney U -test, Z= -3.910, p <0.001; N=42), shorter snout length (male L. aereus mean SNT 3.8 mm ± 0.2 S. D., male L. oshanensis mean SNT 4.0 mm ± 0.2 S. D.; Mann-Whitney U -test, Z= 2.069, p = 0.039; N=42), and greater tibia length (male L. aereus mean TIB 13.7 mm ± 0.5 S. D., male L. oshanensis mean TIB 13.2 mm ± 0.4 S. D.; Mann-Whitney U -test, Z= -3.216, p = 0.001; N=42) than L. oshanensis .

Figures

FIGURE 5. The advertisement call of Leptolalax aereus sp. nov. holotype SAMA R 64236, recorded at ambient air temperature of 22.4 ºC (A) 25 s waveform of relative amplitude, (B) an expanded 0.7 s waveform, and (C) corresponding 0.7 s spectrogram showing two representative calls, and (D) a power spectrum (relative amplitude vs. frequency). The advertisement call of Leptolalax aereus sp. nov. paratype NCMS 76068, recorded at 25.5 ºC. (E) 25 s waveform of relative amplitude, (F) an expanded 0.7 s waveform, and (G) corresponding 0.7 s spectrogram showing three representative calls, and (H) power spectrum (relative amplitude vs. frequency).

FIGURE 6. Temperature-dependence of the average dominant frequency of the advertisement call of Leptolalax aereus sp. nov.