Microhyla berdmorei (Blyth, 1856)

Trofimets, Alexei V., Dufresnes, Christophe, Pawangkhanant, Parinya, Bragin, Andrey M., Gorin, Vladislav A., Hasan, Mahmudul, Lalremsanga, Hmar Tlawmte, Muin, Mohd Abdul, Le, Dac Xuan, Nguyen, Tan Van, Suwannapoom, Chatmongkon & Poyarkov, Nikolay A., 2024, Four in one: An integrative taxonomic revision of the Microhyla berdmorei complex (Amphibia: Anura: Microhylidae) illustrates the tremendous amphibian diversity of Southeast Asia, Vertebrate Zoology 74, pp. 595-641 : 595-641

Microhyla berdmorei (Blyth, 1856)

Figures 6 A, B , 7 A , 8 , 9 , 10 A; Tables 3, 6, S 2

Common name.

Berdmore’s narrow-mouthed frog.

Synonymy and chresonymy.

Engystoma berdmorei Blyth, 1856 “ 1855 ”: 720. Type (s): not stated. Type locality: “ Schwe Gyen ” (now Shwegyin) on the Sitang River, “ Pegu ” (now Bago Region), Myanmar; Sclater (1892: 23).

Callula natatrix Cope, 1867: 192 . Syntypes: MCZ 630 (= MCZ 1587), and MCZ A-153454 -57 (apparently renumbered), according to Barbour and Loveridge (1929) and Harvard University, USA data (http://mczbase.mcz.harvard.edu). Type locality: “ Near Rangoon, Burmah ” (now Yangon Region, Myanmar); Li et al. (2019: 568).

Diplopelma (Engystoma) berdmorei — Günther (1868: 146).

Diplopelma pulchrum Theobald (1868: 83 , in part) (non Engystoma pulchrum Hallowell, 1861 , now Microhyla pulchra ; misidentification).

Diplopelma berdmorei — Theobald (1873: 112).

Microhyla berdmorii — Boulenger (1882: 166). Incorrect subsequent spelling.

Microhyla (Engystoma) berdmorei — Mason (1882: 292).

Microhyla (Engystoma) berdmorei — Boulenger in Mason (1882: 500).

Microhyla berdmorei — Bourret (1942: 509, in part); Frank and Ramus (1995: 90, in part); Dutta (1997: 58–59, in part); Das and Dutta (1998: 64); Chanda (2002: 36-39, in part); Choudhury (2002: 277, in part); Devi and Shamungou (2006: 317–324); Sarkar and Ray (2006: 291, in part); Das and Dutta (2007: 154–181); Wogan et al. (2008: 88, in part); Dinesh et al. (2009: 302: in part); Mahony et al. (2009: 80–94); Mathew and Sen (2010: 65–66); Sengupta et al. (2010: 30); Bjiu et al. (2019: 103); Garg et al. (2019: 15, in part); Li et al. (2019: 566, in part); Nguyen et al. (2019: 549-580, in part); Ahmad and Mim (2020: 36–71); Gorin et al. (2020: 1–47, in part); Hakim et al. (2020: 1239-1268) ; Poyarkov et al. (2020 c: 1525 –1558, in part); Gorin et al. (2021: 97, in part); Kundu et al. (2021: 1586–1591, in part); Zug (2022: 30, in part); Raj et al. (2023: 57–61); Dinesh et al. (2023: 7, in part); Frost (2024, page “ Microhyla berdmorei ” in part).

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

Microhyla butleri (non Microhyla butleri Boulenger, 1900 ) — Lalremsanga et al. (2007: 348; misidentification).

Microhyla sp. — Hasan et al. (2012: 162–172).

Types.

Not stated in the original publication; ZSIC 9718–20 (not examined by us) were listed as syntypes by Sclater (1892), although Blyth (1856) provided measurements for a single specimen. Garg et al. (2019) discussed the confusing status of the type specimens; see discussion below.

Revised diagnosis.

Microhyla berdmorei sensu stricto is characterized by a combination of the following morphological features: (1) large body size ( SVL 33.0 mm in a male, 36.3-38.1 mm in females), with moderately slender and triangular body habitus; (2) head wider than long; (3) dorsal skin shagreened with occasional small tubercles; (4) snout rounded in dorsal and ventral views, obtusely pointed in lateral view; (5) first finger shorter than half of the second finger length; (6) finger tips with weak disks bearing wide and shallow dorsomedial grooves; (7) toes with distinct disks, each bearing a narrow and deep dorsomedial groove; (8) tibiotarsal articulation of the adpressed limb extending far beyond snout; (9) toe webbing reaching disks on all toes except toe IV; webbing formula: i 1-1 ii 1 - 2 iii 1 - 2 iv 2 - 1 v; (10) throat and chin dusty gray to almost black in breeding males; belly yellowish-white; (11) dorsal surfaces of forelimbs and hindlimbs with narrow prominent crossbars, up to 5–6 crossbars on thighs; (12) dark-brown patch above cloacal opening inverted-U-shaped or crescent-shaped; dark blotches on both sides of cloaca; (13) dorsum generally with distinct olive-brown “ teddy-bear ” - pattern edged with light brown; dark dorsal markings may be indistinct or completely absent; (14) body flanks with black irregular spots and blotches; (15) broad olive-gray lateral band extending from armpit to middle of trunk; (16) light postocular stripe yellowish-beige with no dark 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 five specimens of M. berdmorei sensu stricto from India (see Table S 2 for details).

Description of the voucher specimen MZMU A-8003 (Fig. 9 ).

An adult female in a good state of preservation. Body size large ( SVL 36.4 mm; other measurements are presented in Table S 2). Body habitus slender, triangular, and dorsoventrally flattened (Fig. 9 ). Head triangular in dorsal view; wider than long ( HW / HL ratio 1.19). Snout comparatively short and protruding (SL / HL ratio 0.46), rounded in dorsal view (Fig. 9 A ), obtusely pointed in profile, noticeably extending beyond the edge of the lower jaw (Fig. 9 E ). Eyes large, protruding in dorsal and lateral views, significantly shorter than the snout ( EL / SL ratio 0.71), slightly longer than interorbital distance ( IOD / EL ratio 0.90). Canthus rostralis distinct, rounded; loreal area slightly concave. Nostrils oval-shaped, with lateral orientation, situated below the canthus rostralis, slightly closer to tip of snout than to eye. Interorbital distance greater than internarial distance ( IND / IOD ratio 0.86). Upper eyelid length less than the interorbital distance ( UEW / IOD ratio 0.79). Tympanum concealed, supratympanic fold indistinct, marked by a series of low tubercles (Fig. 9 E ). Tongue slender, rounded, free for the posterior four-fifths of its length; vomerine teeth absent. Eggs seen through the incision on the left lateral side of belly; eggs small, rounded, ca. 1.3–1.5 mm in diameter, pigmented (Fig. 9 B ).

Forelimbs short and slender (Fig. 9 A, B ); lower arm elongated and thin ( LAL / FLL ratio 0.85), hand less than half of forelimb length ( HAL / FLL ratio 0.48). Fingers slender and elongated; finger webbing or skin fringes absent. First finger well-developed, notably less than half of the second finger length (Fig. 9 D ); the relative finger length formula: I <II ≤ IV <III. Fingertips rounded, slightly expanded into disks notably narrower than the basal phalanges of the respective fingers. Finger tips lacking peripheral grooves bearing a wide and shallow median notch on the dorsal surface of each finger (Fig. 6 B ). Finger tips almost equal in width, with the first finger tip slightly narrower. Subarticular tubercles on fingers distinct, large, rounded, and protruding; the distal subarticular tubercle on the fourth finger less distinct. The subarticular tubercle formula: 1, 1, 2, 2 (Fig. 9 D ). Two metacarpal tubercles: inner metacarpal tubercle distinct, protruding, rounded in shape; outer metacarpal tubercle rounded and flattened, its diameter subequal to the diameter of inner metacarpal tubercle ( OPTL / IPTL ratio 0.89).

Hindlimbs long, slender, almost four times longer than the forelimbs ( HLL / FLL ratio 3.85). Thighs muscular, massive (Fig. 9 B ), shanks elongated and slender, comprising approximately one-third of the hindlimb length (TL / HLL ratio 0.35). When the limbs are positioned 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 the tibia ( FL / HLL ratio 0.31, TL / FL ratio 1.16). The relative toe lengths: I <II <V ≤ III <IV. Shanks smooth, inner tarsal fold absent. Tips of all toes distinctly widened into round disks, notably wider than the finger tips (4 FDD / 3 FDD ratio 1.75). Toe webbing fully developed, reaching the disks on all toes except the toe IV; webbing formula: i 1-1 ii 1 - 2 iii 1 - 2 iv 2 - 1 v (Fig. 6 A ). Subarticular tubercles on toes distinct, rounded, slightly protruding, subarticular tubercle formula: 1, 1, 2, 3, 2 (Fig. 9 D ). Internal metatarsal tubercle of moderate size, slightly elongated, with indistinct margins, comprising less than half the length of the first toe ( IMTL / 1 TOEL ratio 0.36, Fig. 9 C ). Outer metatarsal tubercle small but distinct, rounded, prominent with well-defined margins, subequal to the length of inner metatarsal tubercle ( OMTL / IMTL ratio 0.94, Fig. 9 C ).

Skin on dorsum shagreened, with rare small tubercles getting denser laterally (Fig. 7 A ). Dorsal surfaces of forelimbs almost smooth, with the exception of tiny tubercles present on forearms. Dorsal surface of hindlimbs with small tubercles sparsely scattered on thighs and shanks (Fig. 9 A ). Upper eyelid smooth. Body flanks smooth, numerous small warts around the tympanal region. Ventral sides of body and limbs completely smooth (Fig. 9 B ). Cloacal opening unmodified, with posterior orientation.

Coloration in life.

Dorsum in life olive-brown with a bronze tint laterally with a dark-brown “ teddy-bear ” pattern (see Rakotoarison et al. 2017) with irregular borders (Fig. 7 A ). Dark-brown triangular interorbital bar located between the posterior parts of upper eyelids continues posteriorly, sharply narrowing at the level of head base and broadening at the scapular area. A pair of dark-brown blotches edged with beige form a trapezoidal dark marking around the cloacal opening. A yellowish-beige light postocular stripe running from the posterior corner of the eye to the axilla (Fig. 7 A ).

Body and head flanks slightly darker than the lateral sides of the dorsum. Snout olive-brown lacking dark markings. Broad dark olive-gray band running posteriorly from the eye. Upper jaw dark-brown with a few irregular light-brown or cream spots below the eye. Narrow cream stripe running from the posterior corner of the eye to the axilla. Except for the upper arm, limbs dorsally with indistinct brownish crossbars and spots: two crossbars visible on lower arms, three crossbars on thighs and shanks. Fingers and toes with brown transverse dorsal bars.

Belly and chest yellowish-white, with a few irregular grayish spots in chest area (Fig. 7 A ). Throat and chin with dense dark-gray mottling, which gets darker along the edges of mandible and mouth corners. Ventral surfaces of limbs beige to bluish-gray lacking dark markings (Fig. 9 C, D ); feet ventrally with dark-brown marking extending from the tibiotarsal joint to the ventral surfaces of toes and toe webbing (Fig. 9 C ). Iris bronze with a distinct vertical dark stripe ventrally. Pupil round, black, outlined with a thin golden circle.

Coloration in preservative.

After two years in preservative, the pattern described above generally remains unchanged (Fig. 9 ). Dorsal background color faded to light-gray, and the dark dorsal markings became less discernible. The characteristic dark spot above the cloacal opening, the “ teddy-bear ” pattern, and other dark markings remain visible. Limbs fade to yellowish-gray, but the dark crossbars on the limbs remain visible. Ventral surfaces fade to light-beige; however, the dark markings on the chin still remain notable as brownish-gray mottling.

Variation.

The examined individuals are overall quite similar in appearance. Differences in size and body proportions are provided in Tables 4 and 5. In females, the body length ( SVL) ranges from 36.3 to 38.1 mm (n = 3); the single examined male had a smaller body size ( SVL 33.0 mm). Dorsal background coloration of the examined specimens varied from olive-brown to yellowish-brown. The male specimen had a notably darker chin than the examined females (Fig. 7 A ).

Etymology.

The species name “ berdmorei ” was given in honor of Captain Major Thomas Matthew Berdmore (1811–1859), a British officer and naturalist who was stationed in Myanmar during the mid- 19 th century. M. T. M. Berdmore was famous for the collection of numerous animal specimens, including this particular species of frog. Recommended common names: “ Berdmore’s narrow-mouthed frog ” (English); “ Nhái b ầu Béc-mơ ” (Vietnamese); “ uzkorot Berdmora ” (узкорот Бердмора, Russian); “ Changpîng ” (Mizo; literally meaning “ spindle frog ”); “ Eung mae nao Pama ” (อ ึ ่ งแม ่ หนาวพม ่ า, Thai).

Distribution.

Based on our definition of M. berdmorei sensu stricto, the actual range of this taxon (Fig. 1 ) is restricted to: India (northeastern part of the country: Meghalaya, Assam, Tripura, and Mizoram states), Bangladesh (central, northeastern, and southeastern parts of the country), and Myanmar (northwestern and central parts of the country). The earlier records of the occurrence of M. berdmorei in Indochina, Malaysia, and Indonesia refer to other species of the M. berdmorei complex described below.

Natural history notes.

Microhyla berdmorei sensu stricto inhabits various types of moist evergreen forests, including monsoon and perennial rainforest types. It is generally associated with hilly regions and is often found near streams; it also occurs in secondary forests. Specimens of this species are active day and night, often hiding in the leaf litter on the forest floor. When disturbed, they make extraordinary long and vigorous jumps to escape. In Assam State, India, breeding activity typically occurs in still pools between October and November ( Garg et al. 2019; IUCN 2022). The noisy rasping call of M. berdmorei sensu stricto can be heard at night from beside forest pools; we have observed specimens of this species displaying cephalic amplexus (Fig. 7 A ). In India, Garg et al. (2019) recorded specimens from thickly vegetated swampy areas near the water bodies, either inside secondary forests or adjacent to human settlements. In Lawachara N. P., Bangladesh, Hakim et al. (2020) found M. berdmorei on trails, roads, and leaf litter in mature forests, degraded forests, tea plantations, and village habitats. Microhyla berdmorei coexists with M. mymensinghensis Hasan et al., 2014 in the northeastern (Dinajpur, Parbatipur) region of Bangladesh ( Hasan et al. 2014). This species was found either in the grass below large trees, referred to as “ Lendi Korui ” by the locals, or in expansive fields with some vegetation and somewhat damp and loose soil. Indigenous to the region, this species is commonly referred to as “ Boro Laubichi Bang ”, and its diet mostly includes ants and other small insects ( Hasan et al. 2014). In Mizoram, India, the species prefers waterbodies with sandy to gravel bottoms for breeding ( Raj et al. 2023).

Tadpole.

Raj et al. (2023) presented a detailed description of the larval morphology of M. berdmorei from Aizawl, Mizoram, India. Tadpoles at Gosner stage 34 reach 20–21 mm in length; at Gosner stage 39 they reach 27–28 mm in length. At Gosner stage 37, body large, oval-shaped in dorsal view; body length comprises 37 % of total length; snout broad and truncate in dorsal view, acutely rounded in lateral view; eyes with lateral orientation; eye-nostril distance comprises 69 % of eye-snout distance; interorbital distance ca. three times greater than internarial distance; spiracle large, medial, located on ventral surface; spiracle-snout distance comprises 83 % of body length; vent tube opening medial, reaching ventral fin edge; ventral tail fin deeper than dorsal tail fin, reaching its maximal height at tail mid-length; caudal musculature comprises 40 % of tail height; tail tip sharply pointed, flagellated. Oral disc terminal, comprising a half of interorbital distance in width; lacking papillae or keratinized structures; a U-shaped medial notch protrudes from the mouth between the two semicircular labial flaps ( Lalremsanga and Muansanga 2022; Raj et al. 2023). In life, head, body, and caudal musculature translucent and white with numerous tiny melanophores; posterior parts of body darker due to pigmentation of inner integument; ventrally milky white and transparent with gut coils visible; few large melanophores present on both tail fins; smaller melanophores present on tail musculature. Tadpoles of M. berdmorei are lentic suspension feeders.

Advertisement call.

The male advertisement call of M. berdmorei represents a series of short rasping sounds resembling the sound of a ratchet. In an unpublished doctoral thesis, Lalremsanga (2011: 102) provided a description of the advertisement call for the M. berdmorei population from Mizoram, Northeast India. The call series consisted of one to seven calls emitted at a 3 s interval; a single call series lasted for 1.4– 1.6 s. Each call consisted of 7–12 pulses and lasted for 0.2 s at an interval of 0.06 s. The amplitude of the call increased slowly and reached a peak in the middle, which then decreased slowly until the end. The frequency spectra ranged between 1484 and 2046 Hz, with the dominant frequency being 1677 Hz.

Our recording of male advertisement call series of M. berdmorei from Aizawl, Mizoram State, India, consisted of several calls (2–5; average 3.6 ± 1.2) emitted at a 2.5 ± 0.2 s (1.47– 3.20 s) interval. A single call lasted for 0.20 ± 0.07 s (0.12–0.33) on average. Each call consisted of 11 ± 2.0 (9–13) pulses emitted at an interval of 0.06 s. The call’s amplitude increased slowly and reached a peak in the middle of the call, after which it gradually decreased; thus, each call’s relative amplitude profile has a symmetrical shape (Fig. 10 A ). The peak frequency of a call comprised 1892 ± 82 Hz (1781–1969 Hz), which is notably higher than the earlier estimates of Lalremsanga (2011).

Comparisons.

Microhyla berdmorei sensu stricto can be distinguished from all other known Microhyla species currently known from South and Southeast Asia by its complete foot webbing, extending well beyond the first subarticular tubercle on either sides of toe IV and reaching up to the disks on the remaining toes (vs. rudimentary to medium foot webbing in all other species); by terminal phalanges of toes Y-shaped (vs. simple, knobbed, or T-shaped in all other species; see Garg et al. 2019); and by toe tips enlarged into disks with dorso-terminal grooves (vs. almost absent). This species can be differentiated from its close genetic congener M. darevskii by finger I length less than half of finger II length (F 1 <½ F 2 vs. F 1> ½ F 2); by weak disks present on fingers (vs. finger disks totally absent); by ventral color lightly colored, yellowish-white with irregular grayish spots (vs. no yellow color on groin and belly); by pattern on flanks and shanks consisting of brown or black irregular spots and blotches (vs. absent); by iris coloration bronze with a distinct dark vertical stripe below the pupil (vs. golden with black reticulation); and by foot webbing reaching to disks except toe IV (vs. reaching to disks on all toes) (see Blyth 1856; Poyarkov et al. 2014; Garg et al. 2019; our data).

For comparisons of M. berdmorei sensu stricto with other closely related members of the M. berdmorei species complex, see below.

Figures

Figure 1. Distribution of the species lineages of the Microhyla berdmorei species complex as identified in the phylogenetic analyses. Star denotes type localities, with their corresponding taxon names in colored clouds; synonyms are shown in quotes; colors correspond to those used in Figures 2–5; symbol shapes denote mtDNA lineages shown in Figure 2. Base map created using simplemappr. net. For locality information see Table S 1. Photos by A. V. Trofimets, A. M. Bragin, P. Pawangkhanant and N. A. Poyarkov.

Figure 6. Dorsal aspects of fourth toes (A, C, E, G) and third fingers (B, D, F, H) of the Microhyla berdmorei species complex members. А, B M. berdmorei sensu stricto, MZMU A- 8005; C, D M. malcolmi, ZMMU A- 7973; E, F M. sundaica sp. nov., ZMMU A- 8011, holotype; G, H M. peninsularis sp. nov., ZMMU A- 8016, holotype. Scale bar equals to 1 mm. Drawings by A. M. Bragin.

Figure 7. Members of the Microhyla berdmorei species complex in life. А M. berdmorei sensu stricto, MZMU A- 8005 and MZMU A- 8003 (a couple showing cephalic amplexus) from Aizawl, Mizoram State, India; B M. malcolmi, ZMMU A- 7973 from Than To, Yala Province, Thailand; C M. sundaica sp. nov., ZMMU A- 8011 (holotype) from environs of Sungai Tua Recreational Forest, Selangor State, Malaysia; D M. peninsularis sp. nov., ZMMU A- 8016 (holotype) from Lam Plok Waterfall, Trang Province, Thailand. Photographs by: A. M. Bragin (A), N. A. Poyarkov (B), A. T. Aful (C), P. Pawangkhanant (D).

Figure 8. Microhyla berdmorei sensu stricto in preservative – specimen MCZ A- 1587 (syntype of Callula natatrix Cope, 1867) from “ Near Rangoon, Burmah ” (now environs of Yangon Region, Myanmar). A Dorsal aspect; B ventral aspect; C lateral view of head. Scale bar equals 3 mm. Photographs by Harvard University, USA (http://mczbase.mcz.harvard.edu/guid/MCZ:Herp:A-1587).

Figure 9. Microhyla berdmorei sensu stricto in preservative – specimen MZMU A- 8003 (adult female) from Aizawl, Mizoram State, India: A Dorsal aspect; B ventral aspect; C plantar view of the right foot; D volar view of the left hand; E lateral view of head. Scale bar equals 3 mm. Photographs by A. V. Trofimets.

Figure 10. Male advertisement call of the M. berdmorei species complex members, showing a 8 s waveform of relative amplitude (Rel. amp., above), the corresponding spectrogram of the same call (Spec., middle), and expanded 3.6 s waveform of relative amplitude of the same call (Exp. Rel. amp., below) for each species. A M. berdmorei from Aizawl, Mizoram State, India; B M. malcolmi from Song Hinh Forest Reserve, Phu Yen Province, Vietnam; C M. sundaica sp. nov. from Gunung Jerai Mt., Kedah State, Peninsular Malaysia.