Leptolalax fritinniens, Dehling, J. Maximilian & Matsui, Masafumi, 2013

Dehling, J. Maximilian & Matsui, Masafumi, 2013, A new species of Leptolalax (Anura: Megophryidae) from Gunung Mulu National Park, Sarawak, East Malaysia (Borneo), Zootaxa 3670 (1), pp. 33-44 : 35-41

Leptolalax fritinniens sp. n.

Twittering Litter Frog ( Figures 1–4 )

Holotype: NMBE 1056267, adult male, from near Camp 5 (4°08.208' N, 114°53.622' E, ca. 114 m a.s.l.), Gunung Mulu National Park, Miri Division, Sarawak, East Malaysia (Borneo), collected 3 December 2007 by J. M. Dehling.

Paratypes: BMNH 1978.1524, 1978.1525, two adult females, from Batu Pala, a limestone outlier near Camp 5, Gunung Mulu National Park, collected in 1977 by Julian M. C. Dring; NMBE 1056367–1056368, two adult males, from near Camp 5, Gunung Mulu National Park, collected 20 March 2009 by A. Haas, J. M. Dehling, Pui Y.-M., S. T. Hertwig, and A. Jankowski; KUHE 10534, an adult male, from Camp 5, Gunung Mulu National Park, collected 26 December 1989 by M. Matsui and K. Araya; SRC unnumbered (former KUHE 53678), KUHE 53676, 53679–53681, four adult males, from near Camp 5, Gunung Mulu National Park, collected 21 August 2010 by M. Matsui, K. Nishikawa, and K. Eto.

Diagnosis. We allocate the new species to the genus Leptolalax for showing the following diagnostic characters: vomerine teeth absent, finger tips rounded, fingers lacking webbing, with toe webbing basal or rudimentary, limbs relatively long and slender, subarticular tubercles indistinct, inner palmar tubercle elevated and not extending to Finger I, outer metatarsal tubercle absent, nuptial pads absent, tip of snout with vertical white bar (Dubois 1983, 1987; Lathrop et al. 1998, Delorme et al. 2006). The new species can be distinguished from all other members of the genus Leptolalax by the combination of following characters: (1) size large, SVL of males 31.8– 34.0 mm, of females 45.5–47.7 mm; (2) snout rounded in both ventral view and lateral view; (3) interorbital distance smaller than width of upper eyelid; (4) vocal sac of males subgular, bipartite; (5) toe webbing basal; (6) skin on dorsum and dorsal side of head shagreened with tiny tubercles; (7) supratympanic fold angled; (8) pectoral glands small; (9) supraaxillary glands and ventrolateral glandular ridges absent; (10) venter spotted; (11) advertisement call consisting of long series of 8–289 notes, each composed of with three or four pulses, dominant frequency at 7225–9190 Hz, with prominent frequency modulation.

Etymology. The species epithet derives from the Latin fritinniens , meaning “twittering”, in allusion to the species’ high-pitched advertisement call with prominent frequency modulation.

Description of holotype. Habitus moderately slender ( Figures 1 & 2 ); head moderately wide (HW/SVL 0.32), about as wide as long (HW/HL 0.98) and wider than trunk; snout rounded in both ventral view and lateral view, slightly protruding, its length 40 % of head length and 90 % of eye diameter, wider than long (SL/EE 0.84); canthus rostralis distinct, slightly concave between eye and nostril in dorsal view, almost straight-lined in lateral view; loreal region oblique, slightly concave; nostrils oval, directed dorsolaterally, closer to tip of snout than to eye (EN/ NS 1.12); distance between eye and nostril subequal to internarial distance (EN/NN 0.97) and much smaller than eye diameter (EN/ED 0.58); eye very large (ED/HL 0.45); pupil vertical; tympanum distinct, rounded, its diameter half the eye diameter (TD/ED 0.50); interorbital distance smaller than width of upper eyelid (IO/EW 0.65) and smaller than internarial distance (IO/NN 0.90); pineal ocellus absent; symphysial knob on anteriormost part of mandible; vomerine ridge and teeth absent; tongue large, broad, bifid, free for about half its length; median lingual process absent; vocal sac subgular, bipartite, consisting of two lateroventrally situated parts which are fused with each other medially when inflated ( Figure 3 ); apertures of vocal sac slit-like, directed posterolaterally, situated halfway between base of tongue and corners of mouth.

Forelimbs slender, moderately long (ELB/SVL 0.70, ARM/SVL 0.56); hand longer than forearm (HND/ARM 0.55); fingers long and slender, without webbing or lateral fringes of skin ( Figure 4 ); relative length of fingers II<I<IV<III; finger tips rounded and thickened; subarticular tubercles indistinct; large, prominent, rounded tubercle in thenar and metacarpal region of fingers I, II, and III, separated by a distinct groove from much smaller, rounded tubercle in metacarpal region of Finger IV.

Hindlimbs moderately long (LEG/SVL 1.69); tibiofibula long (TFL/SVL 0.54), longer than foot (TFL/FOT 1.12) and longer than thigh (TFL/THL 1.07); heels overlapping each other with knees flexed and thighs being held perpendicularly to median plane of body; toe tips rounded and thickened, smaller than finger tips; toe webbing basal, webbing formula I 2 -2.5 II 2- 3 III 2.75- 4 IV 4+- 3 V ( Figure 4 ); narrow fringes of skin on lateral sides of toes; relative length of toes I<II<V<III<IV; subarticular tubercles indistinct; longitudinal ridges of thickened skin on plantar side of phalanges except distal ones of toes II–V, absent on Toe I; inner metatarsal tubercle large (length 2.0 mm), oval, 44 % of length of first toe; outer metatarsal tubercle absent.

Skin on dorsum and dorsal side of head shagreened with tiny tubercles, weakly wrinkled on dorsal surfaces of the extremities ( Figures 1 , 2 ); wrinkles on extremities forming indistinct, reticulated, predominantly longitudinal, low ridges ( Figures 1 , 2 , 3 ); several enlarged tubercles on lateral surfaces of trunk; ventral side smooth; supratympanic fold thick and conspicuous, angled, running from posterior margin of eye to just behind corner of mouth; pectoral glands small, indistinct, at insertion of forelimbs; supraaxillary glands and ventrolateral glandular ridges absent.

Measurements. SVL 33.1, TFL 17.8, FOT 15.8, TarL 24.9, LEG 55.9, THL 16.5, ELB 23.2, ARM 18.4, HND 10.1, HW 10.7, HL 10.9, IO 2.6, EW 4.0, ED 4.9, TD 2.4, TE 1.1, EN 2.8, NS 2.5, SL 4.4, NN 2.9, EE 5.2.

Colouration in life. Basic colouration of dorsum anthracite with several light brown flecks and large black, irregularly shaped spots; area below canthus rostralis and ventral edge of supratympanic fold black; basic colouration lightened to light grey on lateral surfaces of trunk and almost white on venter; dorsal surfaces of extremities light grey with dark grey, black-edged crossbars; dorsal area at tibio-tarsal articulation cream-coloured; several cream-coloured stripes along edges of jaws and similarly coloured crossbars on upper arm and on dorsal surface of fingers and toes; conspicuous, light grey stripe from between nostrils to anteriormost edge of upper jaw; venter with large light grey spots; throat, anterior portion of breast, ventral side of forelimb moderately densely speckled, ventral surface of thigh, tibia, tarsus, and postaxial sides of forelimbs heavily speckled dark brown; posterolateral portion of the throat where vocal sacs are located largely unpigmented; iris dark grey in ventral twothirds, reddish grey in dorsal third, with inner edge around pupil ruby-red.

Colouration in preservative. Colours generally darker; contrast reduced; pattern still distinct; iris colour faded to bluish-grey.

Variation. The male paratypes are generally very similar to the holotype in size and proportions. SVL of males varies between 31.8 mm (NMBE 1056367) and 34.0 mm (NMBE 1056368). Females are considerably larger than males with an SVL of 45.5 mm (BMNH 1978.1524) and 47.7 mm (BMNH 1978.1525). Males have vocal sacs but lack nuptial pads or asperities.

TFL/SVL ratio is 0.53–0.56 (males) and 0.47–0.50 (females), HW/HL 0.96–1.03 (males) and 1.13–1.14 (females), IO/EW 0.65–0.87 (males) and 0.70–0.75 (females), and EN/NN 0.97–1.08 (males) and 1.05–1.06 (females).

Advertisement call. Advertisement calls of four males including the holotype were recorded and analysed ( Table 1 ). Values are given as mean ± SD followed by range. Air temperatures during recordings ranged between 24.3 and 24.9 °C. The advertisement consisted of long series of notes ( Figure 5 ). Number of notes within a series was 58.7 ± 36.3 (8–289). Note repetition rate was 11.7 ± 0.3 (10.6–12.8) per second. Depending on the number of notes, calls lasted 4.9 ± 2.5 (0.6–17.4) s. Individual notes lasted 34.0 ± 4.2 (14–50) ms and were separated from each other by an interval of 51.3 ± 4.7 (36–61) ms. Each note was composed of 3.3 ± 0.5 (3–4, n = 30) rather indistinct pulses ( Figure 5 C). Pulse length varied considerably between 3 and 17 ms (8.8 ± 3.7, n = 37). When pulses were discrete, the interval between individual pulses was about 2 ms. Marked frequency modulation was always observed within a note. The dominant frequency at the beginning was 8266 ± 250 (7750–9200) Hz and decreased towards the end of the note to 7622 ± 154 (7250–8100) Hz. The frequency difference between the beginning and the end of the note was 650 ± 150 (200–1200) Hz. Usually, the first note or the first two notes of a series were higher in frequency (9142 ± 90 Hz, n = 129 calls from 2 males) than the subsequent ones ( Figure 5 B, C). Irregular intensity modulation was observed within a single call and a note ( Figure 5 ). Only in the recording of one male, weak harmonics were present between 9500–9800 Hz. In phases of few calls of this male, only these harmonics were audible and the corresponding notes were only about half the length of regular notes. During the recording, this male sometimes continued the vocal sac motions between two calls but no sound was audible or traceable between 20 and 44,000 Hz in the recordings.

Ecological notes and distribution. The type specimens were found in alluvial forest perching on leaves in low vegetation in the vicinity of small, slow-flowing streams. All males were encountered while calling. Most specimens were found at night, but a few were heard calling between 0 930 h and 1130 h. Tadpoles of the species remain unknown. The species occurs sympatrically with Leptolalax pictus and Leptolalax cf. gracilis .

Although the type series contains only specimen from Camp 5 in Gunung Mulu National Park, we are aware that the species is also distributed in Brunei and Sabah (unpublished molecular and bioacoustic data of MM and JMD). However, most voucher specimens in herpetological collections are mislabelled as either L. dringi or L. gracilis . In addition, preliminary genetic and bioacoustic analyses of specimens and their calls from several locations in Sabah (Matsui, unpubl. data; Dehling, unpubl. data) indicate that at least one further, yet unrecognized species is present. Before the relationships between the populations from Sabah have been resolved, we therefore refrain from describing the geographic range of the new species.

(0.6–15.4, n = 111) (1.1–7.2, n = 11) (1.8–3.5, n = 5) (0.9–17.4, n = 18)

call interval [s] 2.7 ± 2.1 1.3 ± 0.5 8.7 ± 4.4 1.6 ± 0.4

(1.3–19.7, n = 111) (0.4–1.9, n = 10) (5.0–14.5, n = 4) (1.2–2.5, n = 16)

number of notes/call 49.0 ± 32.0 55.8 ± 24.1 28.2 ± 7.3 98.9 ± 89.4

(8–186, n = 111) (14–87, n = 11) (21–38, n = 5) (12–289, n = 18)

note repetition rate [/s] 11.8 ± 0.2 11.9 ± 0.5 11.3 ± 0.4 11.8 ± 0.2

(11.2–12.1, n = 111) (10.62–12.79, n = 11) (10.87–11.76, n = 5) (11.3–12.1, n = 18)

note duration [ms] 34.7 ± 4.5 35.0 ± 3.2 38.0 ± 5.8 28.1 ± 3.4

(28–44, n = 90) (29–44, n = 30) (24–50, n = 31) (14–35, n = 90)

note interval [ms] 47.9 ± 4.8 47.0 ± 3.8 54.6 ± 5.2 54.6 ± 3.8 (550–750, n = 90) (200–1200, n = 30) (400–950, n = 31) (500–1100, n = 90) Comparisons. By the absence of both a ventrolateral glandular ridge and a supraaxillary macrogland, Leptolalax fritinniens differs from species of the genus occurring north of the Isthmus of Kra (in most parts corresponding to the subgenus Lalos Dubois, Grosjean, Ohler, Adler & Zhao, 2010), all of which have a ventrolateral glandular ridge and/or a supraaxillary gland, i.e. Leptolalax aereus Rowley, Stuart, Richards, Phimmachak & Sivongxay, 2010 , L. alpinus Fei, Ye & Li, 1990, L. applebyi Rowley & Cao, 2009 , L. bidoupensis Rowley, Le, Tran & Hoang, 2011 , L. bourreti Dubois, 1983 , L. croceus Rowley, Hoang, Le, Dau & Cao, 2010 , L. eos Ohler, Wollenberg, Grosjean, Hendrix, Vences, Ziegler & Dubois, 2011 , L. firthi Rowley, Hoang, Dau, Le & Cao, 2012 , L. fuliginosus Matsui, 2006 , L. khasiorum Das, Tron, Rangad & Hooroo, 2010 , L. lateralis (Anderson, 1871) , L. liui Fei & Ye, 1990, L. melanoleucus Matsui, 2006 , L. melicus Rowley, Stuart, Thy & Emmett, 2010 , L. nahangensis Lathrop, Murphy, Orlov & Ho, 1998, L. nyx Ohler, Wollenberg, Grosjean, Hendrix, Vences, Ziegler & Dubois, 2011 , L. oshanensis (Liu, 1950) , L. pelodytoides (Boulenger, 1893) , L. pluvialis Ohler, Marquis, Swan & Grosjean, 2000 , L. sungi Lathrop, Murphy, Orlov & Ho, 1998, L. tamdil Sengupta, Sailo, Lalremsanga, Das & Das, 2010 , L. tuberosus Inger, Orlov & Darevsky, 1999 , and L. ventripunctatus Fei, Ye & Li, 1990.

From the species occurring on the Malay Peninsular and Borneo, L. fritinniens (characters in parentheses) differs in the following morphological characters: Leptolalax arayai Matsui, 1997 has a tuberculate dorsum (vs. smooth) without conspicuous markings (vs. present in L. fritinniens ), has an unspotted, yellow venter (vs. venter white with black spots), orange groin and ventral sides of legs (vs. white to cream-coloured ventral side of legs and groin), and a single, medially arranged vocal sac in males (vs. bipartite; Figure 3 ). Leptolalax dringi Dubois, 1987 differs by a smaller size with SVL 26.6–31.3 mm in males and 36.6–38.1 mm in females (vs. SVL 31.8–34.0 mm in males and 45.5–47.7 mm in females); iris bright red in upper third (vs. reddish grey); a relatively wider interorbital space with IO/EW 0.80–1.04 in males and 0.74–0.79 in females (vs. 0.65–0.87 and 0.70–0.75, respectively); angle of supratympanic fold being wider (vs. angle narrow); heads of males being wider than long with HW/HL 1.11–1.22 (vs. as long as wide HW/HL 0.96–1.03); and a relatively greater eye-to-nostril distance with EN/NN 0.81–0.90 in females and 0.76–0.89 in males (vs. 1.05–1.06 in females and 0.97–1.08 in males). Leptolalax gracilis (Günther, 1872) differs in having a curved supratympanic fold (vs. angular); a single medially arranged subgular vocal sac in males (vs. bipartite; Figure 3 ); relatively greater interorbital distance with IO/EW 0.78–0.99 in females and 0.71–0.89 in males (vs. 0.70–0.75 and 0.65–0.87, respectively); iris bright red in the upper two-fifths and dull greyish red, with a narrow ring of bright red along the pupil in the lower three-fifths (vs. iris dark-grey in ventral two-thirds, reddish grey in dorsal third, with inner edge around pupil ruby-red); male SVL 34.3–39.0 (vs. 31.8–34.0). Leptolalax hamidi Matsui, 1997 differs in having the venter unspotted (vs. spotted); large dark brown dorsal markings with light outlines (vs. dorsal markings small without light outlines); and a smaller size with SVL 28.0–31.0 mm in males, 36.0–43.0 mm in females (vs. 31.8–34.0 mm in males and 45.5– 47.7 mm in females). Leptolalax heteropus (Boulenger, 1900) is much smaller with SVL of males 24.6–26.0 mm and of female 31.7 mm (vs. 31.8–34.0 mm in males and 45.5–47.7 mm in females) and has more developed toe webbing and distinct lateral fringes on the toes (vs. toe webbing basal, lateral fringes indistinct). Leptolalax kajangensis Grismer, Grismer & Youmans, 2004 has shorter legs with TFL/SVL 0.42 in males (vs. 0.53–0.56); a curved supratympanic fold (vs. angular); a black spot on the tympanum (vs. absent); an unpatterned venter (vs. venter spotted); and a dark brown dorsum with black pattern (vs. grey dorsum). Leptolalax kecil Matsui, Belabut, Ahmad & Yong, 2009 is much smaller with SVL of males 19.3–20.5 mm and female 25.0 mm (vs. 31.8–34.0 mm in males and 45.5–47.7 mm in females), has a light brown dorsum with dark brown pattern (vs. grey dorsum with black spots); a black spot on the tympanum (vs. absent); a red iris (vs. iris dark grey in ventral two-thirds, reddish grey in dorsal third); and has large, conspicuous, orange pectoral glands (vs. pectoral glands hardly discernible). Leptolalax maurus Inger, Lakim, Biun & Yambun, 1997 is much smaller with SVL of the female holotype being 31.8 mm (vs. 43.5–47.7 mm in females) and SVL of the male paratype 26.1 mm (vs. 31.8–34.0 mm in males), has a dark brown to black dorsal and ventral colouration (vs. grey dorsally and white with black spots ventrally); and a dark red iris (vs. dark grey in ventral two-thirds, reddish grey in dorsal third). Leptolalax pictus Malkmus, 1992 has an immaculate venter (vs. spotted) and has a light brown dorsum with dark brown markings with conspicuous thin light outlines (vs. dorsum grey with black pattern without distinct light outlines). Leptolalax platycephalus Dehling, 2012 has an immaculate venter (vs. spotted); a skin flap above the vent; a wider head with HW/SVL 0.37–0.38 (vs. 0.31–0.32); a greater interorbital distance with IO/EW 1.14–1.27 (vs. 0.65–0.87), rudimentary toe webbing (vs. basal), large pectoral glands (vs. hardly discernible), and different dorsal and ventral colouration. Leptolalax solus Matsui, 2006 is smaller with the only specimen, a male, having an SVL of 27.6 mm (vs. 31.8–34.0 mm in males); has a larger pectoral gland; and a chocolate-brown, largely unpatterned dorsum (vs. dorsum grey with dark pattern).

In addition to the morphological differences, Leptolalax fritinniens can be distinguished by its unique advertisement call from 20 of the 35 species of the genus, of which call characteristics are known (Malkmus & Riede 1993; Matsui 1997; Jiang et al. 2002; Malkmus et al. 2002; Xu et al. 2005; Matsui 2006; Matsui et al. 2009; Rowley & Cao 2009; Sukumaran et al. 2010; Rowley et al. 2010a, 2010b, 2010c, 2011, 2012; Matsui & Dehling 2012). The advertisement call of L. fritinniens , as described by Matsui (1997), was compared to calls of recently described species (as L. dringi ; Matsui 1997, 2006; Matsui et al. 2009; Rowley & Cao 2009; Rowley et al. 2010a, 2010b, 2010c, 2011, 2012), and therefore, we compare the advertisement call only to those of the other Bornean species in the following: The call of L. fritinniens has a dominant frequency of 7250–9200 Hz at 24.3–24.9°C. Although dominant frequency is known to vary over temperature (e.g. Rowley et al. 2010c) the frequency of the call of L. fritinniens is likely to be higher than the dominant frequency of the calls of L. arayai (5400–5900 Hz, 17.4 °C), L. dringi (6050–6400 Hz, temperature unknown), L. gracilis (2600–2800 Hz, 20.0–26.2°C), L. hamidi (6700–7300 Hz, 22.9–24.1 °C), L. maurus (5150 Hz, temperature unknown), and L. pictus (6800–7150 Hz, 19–22 °C). Call length and number of notes within a call is very variable (0.6– 17.4 s, 8–289 notes), but on average (4.9 s, 59 notes), the calls recorded in L. fritinniens are longer and contain more notes than reported in the call of L. dringi (0.1– 1.0 s, 2–11 notes), L. maurus (4.1 s, 15 notes), and L. pictus (1.9– 4.9 s, 12–31 notes). Marked frequency modulation like in the calls of L. fritinniens is absent in the calls of L. dringi , L. gracilis , and L. maurus . Note repetition rate is temperature-dependent but at 10.6–12.8 per second recorded for L. fritinniens at 24.3–24.9 °C it appears to be higher than in the advertisement calls of all other Bornean species ( L. arayai 9.0–9.3/s; L. dringi 8.2– 10.3; L. gracilis 6.9–10.4; L. hamidi 9.0–9.3; L. maurus 3.5) except L. pictus (11–13).

Figures

FIGURE 1. Lateral (left), ventral (middle) and dorsal (right) views of the holotype of Leptolalax fritinniens (NMBE 1056267) in life.

FIGURE 2. Dorsal (left) and ventral (right) view of a male paratype (KUHE 53676) of anesthetized Leptolalax fritinniens. Scale bar represents 10 mm.

FIGURE 3. Calling males of (A) Leptolalax fritinniens, (B) L. gracilis, (C) L. hamidi, and (D) L. arayai. Note the bipartite vocal sacs in L. fritinniens and L. hamidi and the single, median vocal sacs in L. gracilis and L. arayai.

FIGURE 4. Volar view of right hand (left) and plantar view of right foot (right) of a male paratype (KUHE 53676) of anesthetized Leptolalax fritinniens. Scale bar represents 5 mm.

FIGURE 5. Advertisement call of a male paratype (KUHE 53676) of Leptolalax fritinniens recorded at an air temperature of 24.5 C. (A) 25 s spectrogram (top) and corresponding oscillogram of relative amplitude over time (bottom) for 3.5 calls. (B) Spectrogram (top) and corresponding oscillogram (bottom) of a part of a call containing 28 notes, expanded from A. (C) Spectrogram (top) and corresponding oscillogram (bottom) of the first four notes, expanded from B; each note consisting of three, four, three, and three pulses, respectively.

Tables

TABLE 1. Parameters of the advertisement call of four males of Leptolalax fritinniens, recorded near Camp 5, Gunung Mulu National Park. Parameter values are given as means ± SD, followed by ranges and n in parentheses.

Vo u c h e r N o. status	NMBE 1056267 KUHE 53676 holotype paratype	KUHE 10534 paratype	uncollected male
air temperature [°C]	24.3 24.5	24.3	24.9
call duration [s]	4.1 ± 2.7 4.7 ± 2.0	2.5 ± 0.7	8.4 ± 7.6