Microhyla malcolmi Cochran, 1927

Figures 6 C – D, 7 B, 10 B, 11, 12, 13; Tables 3, 6, S 2

Suggested common name.

Malcolm’s narrow-mouthed frog.

Synonymy and chresonymy.

Microhyla malcolmi Cochran, 1927: 182 . Holotype: USNM 72172 (Fig. 11). Type locality: “ Pak Jong, Siam ”, now Pak Chong District, Nakhon Ratchasima Province, Thailand — Parker (1928: 473–499); Barbour and Loveridge (1929: 235); Bourret (1942: 509); Li et al. (2019: 568).

Microhyla fowleri Taylor, 1934: 284 . Holotype: ANSP 19903 (Fig. 12). Type locality: “ Chieng Mai, Siam ”, now Chiang Mai Province, Thailand — Dubois (1987: 3); Bourret (1942: 509); Taylor (1962: 560); Fei (1999: 292–293); Yang and Rao (2008: 124); Fei et al. (2009: 890–894); Fei et al. (2010: 481); Matsui (2011: 33–49); Matsui et al. (2011: 168, 171, 174, in part); Fei et al. (2012: 567); Poyarkov et al. (2014: 89–148); Pradana et al. (2017: 70-90); Li et al. (2019: 568).

Microhyla (Microhyla) fowleri — Dubois (1987: 3).

Microhyla berdmorei — Bourret (1942: 509, in part); Parker (1928: 473–499, in part); Barbour and Loveridge (1929: 235); Parker (1934: 127, in part); Taylor (1962: 560, in part); Heyer (1971: 64–66, in part); Berry (1975: 118–119, in part); Dubois (1987: 3, in part); Stuart (1999: 49, in part); Orlov et al. (2002: 99, in part); Ohler et al. (2002: 465–481, in part); Chan-ard (2003: 102, in part); Teynié et al. (2004: 35, in part); Nguyen et al. (2005: 44, in part); Stuart (2005: 35); Devi and Shamungou (2006: 317–324, in part); Grismer et al. (2006: 63, in part); Stuart and Emmett (2006: 6); Das and Yaakob (2007: 68, in part); Grismer and Aun (2008: 277, in part); Neang and Holden, (2008: 63, in part); Wogan et al. (2008: 88, in part); Chan et al. (2009: 278, in part); Nguyen et al. (2009: 97, in part); Chan-ard et al. (2011: 131, in part); Thong-aree et al. (2011: 99–106, in part); Grismer et al. (2004: 18, in part); Manthey and Denzer (2014: 3–21, in part); Poyarkov et al. (2014: 89–148, in part); Sumarli et al. (2015: 8, in part); Vassilieva et al. (2016: 72–73, in part); Do et al. (2017: 88–89, in part); Mulcahy et al. (2018: 95, in part); Nguyen et al. (2019: 549-580, in part); Geissler et al. (2019: 40–63); Niyomwan et al. (2019: 222–223, in part); Garg et al. (2019: 15, in part); Poyarkov et al. (2020 b: 136 –163, in part); Gorin et al. (2020: 1–47, in part); Makchai et al. (2020: 116, in part); Poyarkov et al. (2021: 40, in part); Gorin et al. (2021: 97, in part); Zug (2022: 30, in part); Hoang et al. (2022: 35, in part); Frost (2024: page “ Microhyla berdmorei ” in part).

Holotype.

USNM 72172 (adult female), by original designation (not physically examined by us, but see Fig. 11). Type locality: “ Pak Jong, Siam ”, now Pak Chong District, Nakhon Ratchasima Province, Thailand (see Fig. 9).

Revised diagnosis.

Microhyla malcolmi is characterized by the following combination of morphological attributes: (1) large body size (SVL 33.2-41.8 mm in males, 36.0- 43.8 mm in females), with slender and triangular body habitus; (2) head longer than wide; (3) skin on dorsum slightly shagreened, laterally with sparse tiny tubercles; (4) snout obtusely pointed in dorsal, ventral, and lateral views; (5) first finger shorter than half of second finger length; (6) finger tips with weak disks lacking dorsomedial grooves; (7) toes with well-developed disks lacking or bearing rudimentary dorsomedial grooves; (8) tibiotarsal articulation of an adpressed limb extends far beyond snout; (9) toe webbing complete, reaching disks on all toes; webbing formula: i 1-1 ii 1 - 1 iii 1 - 1 iv 1 - 1 v; (10) throat and chin dark-gray to almost black in males; belly bluish-gray anteriorly, yellowish posteriorly; (11) dorsal surfaces of fore- and hind limbs with wide dark crossbars, up to 3–4 crossbars on thighs; (12) brown patch above cloacal opening of variable shape and indistinct edges; (13) dark-brown dorsal “ teddy-bear ” - pattern distinct, usually edged with light-brown or beige anteriorly; (14) black spots and blotches of irregular shape on body flanks; (15) broad grayish-brown lateral band lateral stripe extending from armpit to groin; (16) light postocular stripe beige with black edging; (17) reddish spots on dorsum and dorsal surfaces of hindlimbs absent; (18) iris with black stripe below the pupil.

Material examined.

In this study, we used morphological data from 52 specimens of M. malcolmi from Thailand, Laos, and Vietnam (see Table S 2 for details).

Description of the specimen ZMMU A-7973 (Fig. 13).

An adult male specimen in a very good state of preservation. Body size large (SVL 37.1 mm; other measurements are presented in Table S 2). Body habitus slender, triangular, dorsoventrally flattened (Fig. 13 E). Head triangular in dorsal view; longer than wide (HW / HL ratio 0.94). Snout comparatively long and protruding (SL / HL ratio 0.34), obtusely pointed in dorsal view (Fig. 13 A), gently obtusely pointed in profile, and noticeably extending beyond the edge of the lower jaw (Fig. 13 E). Eyes large, protruding in dorsal and lateral views, significantly shorter than the snout (EL / SL ratio 0.75), and longer than the interorbital distance (IOD / EL ratio 0.88). Canthus rostralis distinct, rounded; loreal area notably concave, smooth. Nostrils oval-shaped, with lateral orientation, located below the canthus rostralis; closer to eye than to the tip of snout. Interorbital distance broader than internarial distance (IND / IOD ratio 0.72). Upper eyelid smaller than interorbital distance (UEW / IOD ratio 0.69). Tympanum concealed, faintly developed glandular supratympanic fold extending from the posterior corner of eye to axilla (Fig. 13 E). At the level of mouth corner, supratympanic fold bends posteriorly and extends to the forelimb insertion. Tongue slender, rounded, free behind for half of its length; vomerine teeth absent; gular vocal sac present, single.

Forelimbs short and slender (Fig. 13 A); lower arm elongated and thin (LAL / FLL ratio 0.75), hand less than half of forelimb length (HAL / FLL ratio 0.42). Fingers slender and elongated, webbing or skin fringes on fingers absent. First finger well-developed, subequal to half of the second finger length (Fig. 13 D); the relative finger length formula: I <II ≤ IV <III. Fingertips rounded, slightly expanded, noticeably narrower than the basal phalanges of the respective fingers. Finger tips lacking peripheral grooves, dorsomedial grooves absent, or present as a very shallow rudimentary medial notch (Fig. 6 D). Finger tips almost uniform in width, with the tip of the first finger being slightly narrower. Subarticular tubercles on fingers distinct, large, rounded, and protruding, with the distal subarticular tubercle on the fourth finger being less distinct. Subarticular tubercle formula: 1, 1, 2, 2. Nuptial pad absent (Fig. 13 D). Two metacarpal tubercles: inner metacarpal tubercle distinct, protruding, rounded in shape; outer metacarpal tubercle rounded, flattened, its diameter equal to the diameter of inner metacarpal tubercle (OPTL / IPTL ratio 1.0).

Hindlimbs long and strong, slender, almost four times longer than the forelimbs (HLL / FLL ratio 3.66). Thighs robust and muscular (Fig. 13 B), shanks elongated and slender, comprising approximately one-third of the hindlimb length (TL / HLL ratio 0.37). When the limbs are held at the right angle to the body, the heels significantly overlap. Tibiotarsal articulation of the adpressed limb extends well beyond the tip of the snout. Foot length comprises more than one-third of the hindlimb length, being significantly shorter than tibia (FL / HLL ratio 0.27; TL / FL ratio 1.36). The relative toe lengths: I <II <V ≤ III <IV. Shanks smooth, inner tarsal fold absent. Tips of all toes distinctly widened into small round disks wider than finger tips (4 FDD / 3 FDD ratio 2.05). Dorsomedial longitudinal grooves absent on all toes or present as rudimentary median notch at the medial edge of toe disk (Fig. 6 C). The relative width of toes disks: I <V <II <III ≤ IV. Toe webbing fully developed, web reaching disks on all toes; webbing formula: i 1-1 ii 1 - 1 iii 1 - 1 iv 1 - 1 v (Fig. 6 C). Subarticular tubercles on toes distinct, rounded, slightly protruding, subarticular tubercle formula: 1, 1, 2, 3, 2. Internal metatarsal tubercle of moderate size, oval, slightly elongated, with indistinct margins, less than half the length of the first toe (IMTL / 1 TOEL ratio 0.45). Outer metatarsal tubercle small but very distinct, rounded, prominent with well-defined margins, slightly longer than inner metatarsal tubercle (OMTL / IMTL ratio 1.12, Fig. 13 C).

Skin texture is generally similar to that described for M. berdmorei (see above, Fig. 7 A, B). Skin on dorsum slightly shagreened, with sparse small tubercles getting denser on the lateral sides of dorsum (Fig. 7 B). Dorsal surfaces of forelimbs almost smooth, few tiny tubercles present on forearms. Dorsal surfaces of hindlimbs with sparse tubercles scattered across thighs and shanks; these tubercles are noticeably smaller than those on dorsum (Fig. 13 A). Upper eyelid smooth. Body flanks smooth, numerous small warts present around the tympanal region. Ventral surfaces of body and limbs completely smooth (Fig. 13 B). Cloacal opening unmodified, with posterior orientation.

Coloration in life.

Dorsal background coloration gray-brown with a bronze tinge on the sides of the back, with a faint brown “ teddy-bear ” pattern medially (Fig. 7 B). “ Teddy-bear ” marking with more distinct borders and beige edging anteriorly; the pattern becoming less distinct posteriorly, beige edging not discernible posteriorly. Interorbital dark bar incomplete, present as two indistinct dark-brown blotches between posterior parts of upper eyelids. Indistinct gray-brown marking in the shape of an inverted triangle between interorbital blotches and the “ teddy-bear ” pattern on dorsum (Fig. 13 A). Posterior part of dorsum brownish with indistinct gray blotches. A wide beige light postocular stripe running under the supratympanic fold from the posterior corner of eye to axilla, dorsally edged with black (Fig. 7 B).

The lateral surfaces of the body and head slightly lighter than the dorsum. Snout, canthus rostralis and loreal area uniformly light olive-brown; dark-gray mottling present on the upper jaw; a few irregular black or brownish spots present below the eye. A broad grayish-brown band running from the posterior margin of the eye along the supratympanic fold. A narrow blackish-brown interrupted stripe running from the posterior corner of the eye to the axilla. A series of irregular black blotches and spots on body flanks between the axilla and groin. Except for the upper arm, limbs dorsally bearing indistinct dark-gray crossbars with indistinct edges; two crossbars visible on the lower arms; three crossbars present on each thigh and shank. Fingers and toes dorsally with narrow blackish transverse crossbars.

Belly lightly colored; anterior part of the belly bluish-gray, posterior portion of the belly, groin, ventral surfaces of upper arms, and thighs yellow to yellowish-gray with indistinct gray mottling on thighs (Fig. 7 B). Gular area dark-gray; chin covered with dense gray mottling which gets darker at the edges of the mandible, mouth corners and gradually fades to bluish-gray towards the chest. Shanks ventrally light yellowish-gray, small black spots present on the ventral surfaces of the limbs. Fore- and hindlimbs ventrally grayish-yellow to yellowish. Ventral surfaces of hands (Fig. 13 D) show no distinct pattern; feet ventrally with dark blackish-brown marking extending from the tibiotarsal joint to the ventral surfaces of toes and toe webbing (Fig. 13 C). Iris bronze with black reticulations and a distinct black vertical stripe ventrally (Fig. 7 B). Pupil round, black, outlined with a thin golden circle.

Coloration in preservative.

After two years in preservative, the pattern described above generally remains unchanged, though light colors, like the yellowish coloration of the ventral surfaces and the olive-bronze coloration of dorsum faded to off-white and light gray, respectively. The dark dorsal pattern have become slightly less discernible. The characteristic dark spot above the cloacal opening, black spots and blotches on flanks, and dark markings on feet remain visible, they have turned dark grayish-brown. The limbs have turned yellowish-gray, and the dark crossbars still visible as indistinct dark-gray patterns. The ventral surfaces have faded to light beige; however, the dark markings on the chin have turned dark-gray but are still well discernible.

Variation.

The examined individuals are overall quite similar in appearance. Differences in size and body proportions of the examined specimens are provided in Tables 4 and 5. In females, the body length (SVL) ranges from 33.1 to 43.8 mm (n = 17); in males, the SVL ranges 25.4–41.8 mm (n = 35). The dorsal background coloration varies from gray-brown to gray. Some male specimens demonstrate a darker and more contrasting dorsal “ teddy-bear ” - pattern (ZMMU A-5073, ZMMU A-4710). Breeding males have a darker-colored chin (dark-gray to blackish) than females (gray).

Etymology.

The species was named after Dr. Malcolm Arthur Smith (1875–1958), a famous British herpetologist and physician, who collected many specimens in the early 20 th century across Thailand, Vietnam and Malaysia. Recommended common names: “ Malcolm’s narrow-mouthed frog ” (English); “ Nhái b ầu Mao-com ” (Vietnamese); “ uzkorot Malkolma ” (узкорот Малькольма, Russian); “ Eung mae nao ” (อ ึ ่ งแม ่ หนาว, Thai).

Distribution.

Based on our revalidation and definition of M. malcolmi, we define the range of this species as follows (Fig. 1): China (extreme south of Yunnan Province: Jinghong, Mengla, and Mengyang counties), Vietnam (northwestern, central, and southern parts of the country), Laos (entire country), Cambodia (entire country), and Thailand (entire country). The southernmost record is known from Perlis State in Peninsular Malaysia (Fig. 1, locality 32). Microhyla malcolmi is also expected to occur in eastern Myanmar, though further studies are needed to clarify the extent of its distribution.

Natural history notes.

Microhyla malcolmi inhabits various habitats, including primary and secondary forests as well as human-modified rural landscapes in lowland and hilly areas at elevations up to 2200 m a. s. l. In the lowland monsoon forests of southern Vietnam, this species appears to be associated with bamboo tangles (Vassilieva et al. 2016) and is also often recorded along forest streams. Microhyla malcolmi is active both day and night; according to Vassilieva et al. (2016), its diet consists mainly of ants. Breeding was observed in Vietnam and Cambodia and usually had two peaks of reproductive activity: in May-June and October-December (Neang and Holden 2008; Vassilieva et al. 2016). The noisy rasping call of breeding males can be heard at night from beside forest pools (Neang and Holden 2008). Breeding mainly takes place in slowly-flowing forest streams, ponds, rain pools, puddles and other similar still waterbodies; the reproductive activity usually starts after heavy rains. Clutches include hundreds of small (1.6–1.7 mm) pigmented floating eggs. In Thailand, the species prefers waterbodies with dead leaves and branches on silty bottoms for breeding (Meewattana 2022).

Tadpole.

A detailed description of the larval morphology of M. malcolmi from Thailand was presented by Meewattana (2022) (referred to as M. berdmorei in his work). Tadpoles at late developmental stages reach 20–30 mm in length with large body, oval-shaped in dorsal view; interorbital distance ca. five times greater than internarial distance; mouth-snout distance equal to snout-eye distance; anal tube with vertical orientation reaching the edge of ventral fin; ventral tail fin less than twice as deep as dorsal tail fin; both fins deeper than tail musculature at the level of fourth proximal segment; tail tip tapering (Meewattana 2022). Oral disc terminal, comprising a half of interorbital distance in width; lacking papillae, jaw sheaths, or labial teeth (Meewattana 2022). In life, head, body, and caudal musculature pale grayish; posterior part of body dark-gray or black; dorsally with a weak dark marking between the eyes; tail fins transparent. Tadpoles of M. malcolmi are lentic suspension feeders.

Advertisement call.

The male advertisement call of M. malcolmi represents a series of noisy rasping sounds that resemble the sound of a ratchet to the human ear. Heyer (1971) provided a brief description of an advertisement call for a M. malcolmi population from Sakaerat Experimental Station, Nakhon Ratchasima Prov., Thailand (referred to as M. berdmorei in his work). The duration of the call was 0.09– 0.26 s, with each call consisting of 3–9 pulses at a pulse rate of 33–35 pulses per second, and the peak frequency of the call estimated at 1500–1800 Hz.

Our recording of M. malcolmi advertisement calls taken in Song Hinh Forest Reserve, Phu Yen Province, Vietnam, included call series, each of them consisting of several calls (4–6; average 5.2 ± 1.4) emitted at a 2.3 ± 1.5 s (0.97– 3.79 s) interval; a single call lasted for 0.22 ± 0.04 s (0.16–0.31) on average. Each call consisted of 9 ± 1.1 (8–10) pulses. The call’s amplitude increased sharply, reached its peak in the first 0.05– 0.10 s of call duration, and then gradually decreased towards the call’s end; the last half of the call duration had a notably lower amplitude (491 ± 57 Hz) than the first half (Fig. 10 B). We estimated the call peak frequency to be 1631 ± 93 Hz (1507–1809 Hz), which agrees well with the estimates of Heyer (1971).

Comparisons.

Microhyla malcolmi was previously considered as a junior synonym of M. berdmorei, but this species can be differentiated from M. berdmorei sensu stricto by having: fully-developed foot webbing (I 1-1 II 1 - 1 III 1 - 1 IV 1 - 1 V vs. I 1-1 II 1 - 2 III 1 - 2 IV 2 - 1 V); supratympanic fold distinct (vs. indistinct); comparativey shorter snout (SL / HL ratio 0.31-0.39 [avg. 0.34, n = 21] in males, 0.32-0.37 [avg. 0.35, n = 9] in females of M. malcolmi vs. 0.46 in male [n = 1], 0.45-0.46 [avg. 0.45, n = 3] in females of M. berdmorei sensu stricto); snout shape in dorsal and ventral views (obtusely pointed vs. rounded); crossbars on thighs wide, 3–4 crossbars on each thigh (vs. crossbars narrow, up to 5–6 crossbars on each thigh); background color of dorsum grayish-brown (vs. olive-brown with a bronze tinge); head longer than wide (vs. head wider than long); finger tips with weak disks lacking dorsomedial grooves (vs. finger tips with weak disks bearing wide and shallow dorsomedial grooves); and toes with well-developed disks lacking or bearing rudimentary dorsomedial grooves (vs. toes with distinct disks, each bearing narrow and deep dorsomedial groove).

For comparisons of M. malcolmi with other members of the M. berdmorei species complex, see below.