Microhyla malang, Matsui, Masafumi, 2011

Matsui, Masafumi, 2011, Taxonomic revision of one of the Old World’s smallest frogs, with description of a new Bornean Microhyla (Amphibia, Microhylidae), Zootaxa 2814, pp. 33-49 : 39-44

Microhyla malang sp. nov.

Synonymy: Microhyla borneensis: Parker 1934 , p. 128 (part); Inger 1966, p. 151 (part); Inger & Stuebing 1997, p. 108; Malkmus et al. 2002, p. 131; Das et al. 2007a, p. 101; Das et al. 2007b, p. 156; Das & Haas, 2010, p. 45.

Holotype. KUHE 17245, an adult male from Gunung Serapi, Matang Range, in the suburbs of Kuching, Kuching Division, Sarawak, Malaysia (01o36'N, 110o11'E, alt. 290 m a.s.l.; now a part of Kubah National Park), collected on 15 August 1993 by Masafumi Matsui.

Paratypes. Eleven adult males: KUHE 17217, 17236, 17658 from the type locality, collected on 12 August, 12 August, and 9 September, 1993, respectively; SM unnumbered (former KUHE 53034), KUHE 53018 from the type locality, collected on 14 August 2008; KUHE 53166, 53176 from the type locality, collected on 26–27 August 2008; Universiti Malaysia Sarawak ( UNIMAS) R2110 from the type locality by Ramlah Zainudin; and KUHE 42549, 42550, 42597 from Kanowit, Sibu Division, collected on 20, 20, and 22, respectively, November 2008 by Daicus M. Berabut, Norhayati Ahmad, Kanto Nishikawa, and Masafumi Matsui.

Referred specimens. Universiti Kebangsaan Malaysia ( UKM) HC 0 0 392 an adult male from Lanjak Entimau Wildlife Sanctuary, Sri Aman Division, Sarawak, collected in 2008 by Daicus M. Berabut and Norhayati Ahmad; KUHE, two unnumbered batches of tadpoles, from the type locality and a stream near the type locality, collected on 27 August 2010 by Masafumi Matsui and Koshiro Eto; KUHE 44228, an adult female from Poring Hot Spring, Pantai Barat Division, Sabah, collected on 21 March 1979 by Masafumi Matsui (Matsui, 1979); KUHE 44229, a juvenile female from Sepilok, Sandakan Division, Sabah, collected in August 1979 by Ryozo Yoshii; Sabah Park Collection (SP) 0 2662 from Imbak, Telupid, Sandakan Division, Sabah, collected on 5 July 2000 by Maklarin Lakim, Paul Yambun, and others. BORNEENSIS 9090, 9210, 9211 from Tawau Hills National Park, Tawau Division, Sabah, collected from 28 July to 1 August 2004 by Masafumi Matsui, Kanto Nishikawa, and Tomohiko Shimada; KUHE, an unnumbered batch of tadpoles, from Tabin Wildlife Reserve, Tawau Division, Sabah, collected on 3 August 2004 by Tomohiko Shimada and Masafumi Matsui.

Etymology. The specific epithet malang is a Malay word denoting unlucky, alluding to the long history of taxonomic confusion in which it was called under the name of its sister species M. borneensis . It is also an allusion of Matang, the type locality of the species in western Sarawak.

Diagnosis. A medium form of Microhyla , adult males about 18–22 mm in SVL; snout obtusely pointed, rounded in profile; first finger short, less than one-fourth of third; tips of three outer fingers weakly dilated, forming weak disks, dorsally with median longitudinal groove; outer palmar tubercle single; tibiotarsal articulation reaching far beyond snout tip; tips of toes distinctly dilated into disks, dorsally with median longitudinal groove; toes on outer side of second 1, inner side of third 2 2/3, outer side of third 1 1/2 – 1 2/3, inner and outer sides of fourth 3, and inner side of fifth 1 phalange(s) free of web; inner and outer metatarsal tubercles present; eyelid without supraciliary spines; top of snout undifferentiated from the brown forehead; vertebral stripe absent; dark dorsal markings usually narrowly outlined in white; a cream stripe below supratympanic fold, not bordered by black above; a narrow, broken, black lateral stripe from above arm to half length of trunk; tail of larvae with two black markings separated by an oblique white marking at middle, and transparent filament at tip.

Description of holotype (measurements in mm). SVL 21.4; habitus stocky, body rounded ( Fig. 4 ); head triangular, slightly wider (9.3) than long (9.2); snout obtusely pointed, rounded in profile, projecting beyond lower jaw; eye small, shorter (2.3) than snout (3.2); canthus rostralis rounded, straight; lore sloping, weakly concave; nostril lateral, on canthus rostralis, closer to tip of snout (1.4) than to eye (1.6); interorbital distance (3.0) wider than internarial distance (2.5), the latter twice width of upper eyelid (1.1); pineal spot absent; tympanum hidden; upper jaw edentate; tongue oval, without papillae; slit-like openings to a median subgular vocal sac.

Forelimb short (10.3) and stout; fingers thick, free of web, but with slight skin fringes on both sides of second and third and inner side of fourth; second finger slightly longer (measured from inner side 2.0, outer 1.4) than fourth (inner 1.6), latter much longer than first (outer 0.7); tips of three outer fingers weakly dilated and forming weak disks slightly wider than basal phalanges, dorsally with median longitudinal groove; diameter of first finger (0.3) one-third that of third finger disk (0.9), latter less than two-times width of phalange; a single outer palmar tubercle (1.1) much larger than inner (0.6); distinct, rounded subarticular tubercles, numbering one on first and second fingers, two on third and fourth fingers; nuptial pad absent ( Fig. 5 ).

Hindlimb long (40.0) about three times length of forelimb; tibia long (14.0), heels overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching far beyond snout tip; foot (12.4) shorter than tibia; tips of toes distinctly dilated into disks, much wider than those of fingers (disk diameter of third toe 0.9), dorsally with median longitudinal groove; third toe longer than fifth; webs between toes moderately developed ( Fig. 4 ), formula: I 1– 2 II 1–2 2/ 3 III 1 1/2 – 3 IV 3– 1 V; subarticular tubercles prominent, rounded, numbering one on first and second toes, two on third and fifth toes, and three on fourth toe; inner metatarsal tubercle oval, length (0.7) one-third of first toe (2.2); outer metatarsal tubercle elevated, larger (0.9) than inner one.

Skin above with scattered, low tubercles; eyelid without supraciliary spines; a weak, curved supratympanic fold from eye to axilla; side of body scattered with tubercles or low ridges more densely than dorsum; hindlimb dorsally scattered with few tubercles; ventral side of body and limbs smooth.

Color. Color in life pinkish brown dorsally, with a darker wide interorbital bar, reverse triangle in shape, medially followed by three darker markings narrowly outlined in white, consisting of two wide-limbed reverse Vshaped marks from occiput to sacrum, and a subtriangle mark between sacrum and groin; a narrower and paler line paralleled with each dark marking laterally to flank; a small black spot at middle of two wide-limbed marks, surrounded by dark dots; lips spotted with black; a cream stripe extending from eye to axilla bordered above by supratympanic fold and below by dark labial marks ( Figs. 6 , 7 ); a narrow, broken, black lateral stripe extending from above arm to half length of trunk; limbs dorsally with narrow dark brown bars; median edge of tarsus darkly marked; a dark spot surrounding anus; throat mottled with dark brown and abdomen cream white; underside of limbs scattered with black pigmentation; iris dorsally and ventrally golden with black reticulation, darkly pigmented at anterior and posterior corners. In preservative, pattern has not obviously changed, although color has slightly faded.

Variation. Individuals of the type series are generally similar in morphology. Variation in size and body proportions is given in Table 2. Web formula was stable except for the third toe, which showed slight variation; on the inner side, some had only two phalanges free of web, while on the outer side, many had 1 2/3 phalanges free ( Fig. 1 ).

Tadpoles. A total of ten tadpoles from St. 25 (TOTL = 9.0 mm, HBL = 2.9 mm) to 41 (15.9 mm, 5.1 mm) from near the type locality of M. malang and identified as that species by DNA analyses (see above) were closely examined ( Table 3 ). Head and body flattened above, spheroidal below; HBW maximum at level of eye 58–64% (median = 61%) of HBL; HBD 84–100% (median = 89%) of HBW; snout broadly rounded, almost truncate in profile; eyes lateral, visible from below, eyeball 14–17% (median = 15%) of HBL; interorbital wide, 180–256% (median = 223%) of eyeball diameter; eye-snout distance 27–30% (median = 30%) of HBL. Oral disk dorso-terminal; lower lip moderately expanded with width 33–48% (median = 43%) of HBW, with a prominent lateral papilla (sensu Das and Haas, 2010) on each side; labial teeth and jaw sheaths entirely absent, but lower labium scattered with small papillae on lateral margin. Spiracle opening median, without free flap, opening 79–90% (median = 84%) of distance from tip of snout to end of body; vent median, in form of long tube directed obliquely backward, small opening at edge of ventral fin; gut in form of two, thick loops visible ventrally. Tail long and lanceolate, abruptly tapering in posterior half and drawn out into a long filament in posterior one-fourth; tail length 176–211% (median = 205%) of HBL, maximum depth 19–28% (median = 25%) of length; dorsal fin originating at end of head-body, with a straight margin, sub-parallel with much deeper ventral fin in anterior half of tail; ventral fin deeper than dorsal throughout anterior to tail filament; caudal muscle moderately strong, maximum tail width 28–36% (median = 32%) of HBW; muscle depth maximum at origin, 41–55% (median = 48%) of maximum tail depth, but steadily narrowed posteriorly, with depth at middle of tail shallower than upper fin depth. Color in life ( Fig. 8 ) light brown on dorsum and laterally, with a pair of paler interorbital markings and darker bands on middle and end of body; venter grey and belly translucent in young stages; tail at middle with two black markings separated by an oblique white marking; tail tip transparent.

characters to SVL, followed by ranges in parenthesis. See text for character abbreviations.

SVL RHL RSL REL RN-EL RHW

Mean/Median 20.5+1.2 39.5 15.8 12.1 7.0 41.0

Range (18.7–22.2) (37.9–42.9) 14.4–17.6) 10.9–12.8) (6.2–8.0) (38.3–43.6)

RIND RIOD RUEW RFLL RLAL RHAL

Median 11.4 13.5 6.2 52.2 38.4 22.8

Range (10.5–11.7) (12.3–15.3) (5.2–6.9) (48.2–54.1) (37.1–42.0) (22.2–23.7)

R1FL RIPTL ROPTL RHLL RTL RFL

Median 5.4 2.8 4.3 193.8 65.9 58.2

Range (5.2–6.3) (2.2–3.2) (3.6–5.5) (182.1–199.7) (62.3–68.8) (53.2–61.0)

R1TOEL RIMTL ROMTL R1FW R2FDW R3FDW

Median 10.4 4.0 5.8 1.6 3.0 3.6

Range (9.2–11.7) (3.1–4.5) (4.2–7.0) (1.1–2.8) (2.3–3.4) (2.7–4.5) R4FDW R1TDW R2TDW R3TDW R4TDW R5TDW

Median 3.1 3.7 5.6 6.2 5.8 4.8

Range (2.7–3.6) (2.9–4.7) (4.2–6.3) (4.6–6.7) (4.6–6.7) (4.1–5.7) R1FLO R2FLI R2FLO R3FLI R3FLO R4FLI

Median 2.9 9.6 6.6 13.6 13.2 7.3

Range (2.4–4.1) (7.7–10.6) (5.8–7.1) (12.7–14.9) (11.7–13.8) (5.6–8.2) Range. The new species is so far known from western Sarawak and eastern Sabah, Malaysian Borneo. Sarawak: Gunung Serapi, Matang, (the type locality), Kanowit, and Lanjak Entimau; Sabah: Poring Hot Spring, Sepilok ( Matsui 1979 as M. borneensis ), Tabin, and Tawau. The species ranges in altitude from 50 to 555 m a.s.l. Das & Haas (2010) reported Gunung Poing, Bau ( Sarawak), Batu Apoi Forest Reserve, Temburong ( Brunei Darussalam), and Kalimantan ( Indonesia) as the range of their M. borneensis (= M. malang ).

Natural history. As already reported by Das and Haas (2010), M. malang is sympatric with M. borneensis around the type locality, in Kubah National Park. They are actually syntopic and can be found very close to each other near the Frog Pond of the park. Chorus of male M. malang was heard in August, September, and December in the park, and also reported from there in April ( Dehling 2010). Calls were heard also in August in Kanowit and Tawau. Tadpoles of two different stages were found in August in Kubah, and older ones in Sepilok, Tabin, and Tawau in August. Matsui (1979) reported a female (now KUHE 44228) from Poring, Sabah with enlarged ova in March. Thus M. malang seems to have a prolonged breeding season. Tadpoles were found in ponds and in shallow, muddy pools in drying stream beds.

Call characteristics. Characteristics of calls recorded at the type locality did not differ from those already reported by Dehling (2010) from records of the same locality at air temperatures of 23.5−24.7°C. They consisted of notes each emitted at an interval of ca. 830 ms. Each note was composed of 5.7 ± 1.1 (4−8) short pulses and lasted for 169 ± 37 (104−242) ms. Frequency bands spread over the 1400–2900 hz range, and the dominant one was 2404 ± 94 (2250−2530) hz. Frequency modulation was not marked but weak intensity modulation was present ( Dehling 2010).

Comparisons. As noted above, the new species closely resembles, but can be differentiated from M. borneensis by larger body size (male SVL 19.4–21.3 mm vs.11.0– 13.2 mm in M. borneensis ), more developed toe web (fifth toe with one phalange free of web vs. two phalanges free), possession of (vs. usually lacking) a mid-dorsal black spot and light lines at the edge of dorsal dark markings. They are remarkably different in tadpole morphology and ecology. The new species breeds in ponds and pools of slowly flowing streams, while M. borneensis utilizes small amount of the water in the cups of pitcher plants. Tadpoles of the new species reach larger size (15.9 mm in total length vs. 11.5 mm in M. borneensis ), and have darker body color with dorsal and tail markings (nearly transparent and without marking in M. borneensis ). The new species is morphologically similar to M. mantheyi , with which it has long been confused (as M. borneensis ). However, M. malang is distinguishable from M. manthey by its uniformly brown snout and forehead (vs. top of snout cream colored in M. mantheyi ), shorter dark, lateral stripe covering anterior half of flank (vs. longer stripe covering entire flank), pale supratympanic stripe lacking dark margin (vs. pale stripe with a dark dorsal edge), absence of light vertebral line (vs. presence of a thin line), rounded snout (vs. snout tapering), and fourth toe three phalanges free of web (vs. fourth toe more than three phalanges free). In tadpoles, M. malang with a light interorbital bar and without dark terminal filament of tail also differs from M. mantheyi , in which interorbital bar and tail filament are dark. Although Das & Haas (2010: 45) noted absence in M. mantheyi of finger disks, the species has disks like those of M. malang and M. borneensis as clearly stated in the original description ( Das et al. 2007a). The new species differs from all the other congeners in the same manner as was reported for M. borneensis by Das & Haas (2010, as M. nepenthicola ).

Calls of M. malang and M. borneensis are basically similar in temporal structure, but clearly differ in frequency properties with the new species emitting a lower voice than M. borneensis . Calls of sympatric M. borneensis recorded on 22 January 1990 at an air temperature 21.7 C included two types. The first call type consisted of a series of pulsed notes lasting 50–140 ms and containing 2–4 pulses. The second call type consisted of the first call type and additional notes including longer series of pulsed notes, and lasted 420–510 ms. The additional note was composed of 6–8 pulses. The pulse rate in the first call type ranged from 39.2–41.6 per second. The dominant frequency was spread over the 3460–3750 hz range. A well-defined harmonic was seen at about 4625 hz and frequency or intensity modulations were absent.

Figures

FIGURE 1. Ventral views of feet of the large form (A-D: males from Gunung Serapi, Sarawak [A: KUHE 17217; B: KUHE 17245; C: KUHE 17658; D: KUHE 53176], E: female from Poring, Sabah [KUHE 44228]) and the small form of Microhyla (F-J: males [F: KUHE 10693; G: KUHE 10695; H: KUHE 10743; I: KUHE 53241; J: KUHE 53938]; K-O: females [K: KUHE 12067; L: KUHE 26419; M: KUHE 53020; N: KUHE 53165; O: KUHE 53582], all from Gunung Serapi, Sarawak). Not to scale.

FIGURE 4. Dorsal (A) and ventral (C) views of male holotype of Microhyla malang sp. nov. (KUHE 17245) and dorsal view (B) of syntopic male Microhyla borneensis (KUHE 53814) from Gunung Serapi, Sarawak. Scale bar = 10 mm.

FIGURE 5. Ventral views of right hands (A, C) and feet (B, D) of syntopic Microhyla borneensis (A, B: KUHE 53814) and Microhyla malang sp. nov. (C, D: KUHE 53018) from Gunung Serapi, Sarawak. Scale bar = 5 mm.

FIGURE 6. Dorsolateral view of a male paratype of Microhyla malang sp. nov. (KUHE 53018) from Gunung Serapi, Sarawak.

FIGURE 7. Dorsolateral view of head of Microhyla borneensis (A – B, males [A: KUHE 53938; B: KUHE 10692]: C – F, females [C: holotype, BM 1947. 2.11.82; D: KUHE 53020; E: KUHE 12067; F: KUHE 53165] and Microhyla malang sp. nov. (G – H, males [G: holotype, KUHE 17245; H: KUHE 17217]; I, female [KUHE 44228]).

FIGURE 8. Larval Microhyla malang sp. nov. from Gunung Serapi, Sarawak (A – C: stage 32, total length = 13.9 mm) and Tawau, Sabah (D – F: stage 41, total length = 16.4 mm, from photos taken by T. Shimada); dorsal (A, D), lateral (B, E), and ventral views (C, F). Scale bar = 5 mm.

Tables

TABLE 3. Measurements in mm of larval Microhyla malang sp. nov. from Serapi. See text for character abbreviations.

Stage	25	27	30	31	31	32	34	35	40	41
TotL	9.02	12.90	13.11	13.66	14.42	13.86	13.67	14.90	15.94	15.85
HBL	2.93	4.15	4.28	4.78	5.11	4.89	4.96	4.88	5.14	5.09
HBW	1.86	2.48	2.75	2.85	3.12	3.03	2.88	3.11	3.09	3.14
HBD	1.66	2.31	2.31	2.47	2.88	2.80	2.88	2.75	2.69	2.75
Eye-Snout	0.90	1.27	1.22	1.35	1.50	1.47	1.36	1.51	1.49	1.54
Eye Diameter	0.50	0.58	0.68	0.71	0.72	0.69	0.69	0.77	0.80	0.79
Inter-orbital	0.90	1.21	1.54	1.56	1.73	1.77	1.67	1.76	1.60	1.65
Snout-Spiracle	2.48	3.68	3.52	4.30	4.15	4.00	3.92	4.14	4.34	4.29
Oral disk W	0.66	1.04	1.15	1.29	1.56	1.35	1.38	1.27	1.02	1.38
TailL	6.09	8.75	8.83	8.88	9.31	8.97	8.71	10.02	10.80	10.76
Max tail D	1.51	2.04	2.20	2.15	2.65	2.34	2.48	2.42	2.06	2.31
Max tail W	0.62	0.89	0.79	0.86	1.04	1.04	0.87	1.05	0.86	0.94
Max muscle D	0.83	0.92	1.10	1.02	1.15	1.09	1.04	1.16	1.14	1.21