Megophrys (Xenophrys) zunhebotoensis ( Mathew & Sen, 2007 )

Mahony, Stephen, Kamei, Rachunliu G., Teeling, Emma C. & Biju, S. D., 2020, Taxonomic review of the Asian Horned Frogs (Amphibia: Megophrys Kuhl & Van Hasselt) of Northeast India and Bangladesh previously misidentified as M. parva (Boulenger), with descriptions of three new species, Journal of Natural History 54 (1 - 4), pp. 119-194 : 175-182

Megophrys (Xenophrys) zunhebotoensis ( Mathew & Sen, 2007)

Xenophrys zunhebotoensis Mathew and Sen, 2007, p. 20 , In: Description of two new species of Xenophrys ( Amphibia : Anura : Megophryidae ) from north-east India. Cobra , 1(2), 18 – 28.

Holotype. Adult female ( V /A/ERS/ ZSI /774 — not examined directly [ Figure 15 ]) from ‘ INDIA: Nagaland, Zunheboto district, Nguti (Sukhalu), (collected from a mountain stream with rocks and boulders) (N. 25°58 ′ 45.1 ″, E. 94°30 ′ 24 ″), Alt. 1715 msl. ’, collector Rosamma Mathew (‘ and party ’ according to Mathew and Sen 2009) on 10 August 2005 ( Mathew and Sen 2007).

Paratype. Adult male ( V /A/ERS/ ZSI/775 — not examined), collection details as per holotype .

Referred specimens. Seven adult males ( CES 19909 [field tag RGK 0041 ; Figure 16 (a – c)], CES 19905 [field tag RGK 0042 ], CES 19900 [field tag RGK 0043 ], CES 19911 [field tag RGK 0044 ], CES 19903 [field tag RGK 0045 ], CES 19904 [field tag RGK 0046 ], CES 19908 [field tag RGK 0047 ]: topotypes) from Nguti stream (25.966944, 94.498333, 1820 m asl.), Sukhalu village, Zunheboto district , Nagaland state, NEI, collected by RGK and SKK on 12 May 2013; four adult males ( CES 19906 [field tag RGK 0062 ], CES 19910 [field tag RGK 0064 ], CES 19907 [field tag RGK 0065 ], CES 19902 [field tag RGK 0066 ]) and an adult female ( CES 19901 [field tag RGK 0063 ; Figure 16 (d)]) from Puliebadze forest (25.630555, 94.102222, 1540 m asl.), Jotsoma village , Kohima district , Nagaland state, NEI, collected by RGK on 20 May 2013; adult female ( SDBDU 2007.139 ) ~ 4 km road distance from Kohima Science College , near Puliebadze forest (25.639722, 94.058611, 1585 m asl.), Jotsoma village , Kohima district , Nagaland state, NEI, collected by RGK on 27 June 2007; adult female ( SDBDU 2009.342 [ Figure 16 (e)]) and adult male ( SDBDU 2009.374 ) from Lorü stream (25.639600, 94.055867, 1530 m asl.), Puliebadze forest , Jotsoma village , Kohima district , Nagaland state, NEI, collected by RGK on 4 – 8 June 2009; three adult males ( SDBDU 2007.047 – 049 ) from Vibalieza (25.709722, 94.053611, 810 m asl.), Sechu village , Sechu- Zubza circle, Kohima district , Nagaland state, NEI, collected by RGK and VK on 12 June 2007; two adult males ( SDBDU 2007.056 & SDBDU 2007.057 ) from Sechüma village (25.688889, 94.029444, 1470 m asl.), Sechu-Zubza circle, Kohima district , Nagaland state, NEI, collected by RGK and VK on 14 June 2007; five adult males ( SDBDU 2009.108 – - 110 [ Figure 16 (f)], SDBDU 2009.112 & SDBDU 2009.122 ) from Ganparui Taeuhthuak (24.628800, 93.713000, 1380 m asl.), Raenghzaeng village , Churachandpur district , Manipur state, NEI, collected by RGK on 16 May 2009; adult male ( SDBDU 2009.125 ) from below Rasuan (24.626017, 93.702000, 1585 m asl.), Akhuna thuak, Chalungkhou , Churachandpur district , Manipur state, NEI, collected by RGK on 18 May 2009 .

Description of topotypic referred specimen CES 19909 (measurements in mm). Mature male (SVL 33.2) ( Figure 16 (a – c)). Head small (HW 11.3, HL 11.2, IFE 5.5, IBE 9.4),

as wide as long; snout rounded in dorsal view, obtusely protruding in lateral view, slightly upturned towards tip, rostral appendage absent ( Figure 16 (c)); loreal region vertical, concave; canthus rostralis sharp; dorsal region of snout slightly concave; eye less than twice as long as maximum tympanum diameter, and longer than snout (EL 4.3, TYD 2.8, SL 4.1); eye – tympanum distance (TYE 1.6) approximately half maximum tympanum diameter; tympanum circular, not concealed by supratympanic ridge ( Figure 16 (c)); pupil in life elliptical, vertically orientated when contracted; nostril oval, orientated laterally, situated closer to eye than snout (EN 1.5, SN 2.3); internarial distance longer than eyelid width, and narrowest point between upper eyelids (IN 3.9, UEW 3.5, IUE 3.3); pineal ocellus not visible externally; vomerine ridges acute, narrow anteriorly, extending from level of anterior choanae border, widens suddenly posteriorly to become hemispherical at level posterior to choanae, equidistant from each other and choanae; vomerine teeth absent; maxillary teeth present; tongue large, posterior edge with weak median notch.

Forelimbs moderately short, thin, forearms slightly enlarged relative to upper forelimbs ( Figure 16 (a – c)), forearm shorter than hand length (FAL 7.5, HAL 8.9); fingers moderately long, not dorsoventrally flattened, lateral fringes absent, finger length formula I = II <IV <III (FIL 3.4, FIIL 3.4, FIIIL 6.7, FIVL 4.3); interdigital webbing, subarticular and supernumerary tubercles absent; thenar tubercles weakly developed; outer metacarpal tubercles absent; fingertips not expanded, with circular pads. Hindlimbs moderately long, thin ( Figure 16 (a – c)), shanks meet when thighs are held at right angle to body, thigh equal to shank length, and slightly shorter than foot (TL 14.8, SHL 15.0, FOL 15.0); toes long, rounded, lateral fringes absent; relative toe lengths I <II <V <III <IV; toe tips not dilated, but with distinct longitudinally oval pads; terminal groves absent; webbing at base of toes absent; outer metatarsal tubercle, subarticular and supernumerary tubercles absent; inner metatarsal tubercle present but barely distinguishable; ridge of callous tissue present on ventral surface of all digits.

Skin of dorsal surfaces of head, body and limbs rugose, covered with weakly developed tubercles; flanks and dorsum with small to medium-sized, scattered tubercles ( Figure 16 (c)); tympanum smooth, flat, surrounding area posterior to eye weakly granular ( Figure 16 (c)); small tubercular ridge present on outer edge of upper eyelids; supratympanic ridge narrow anteriorly, moderately wide posteriorly, extending from orbit in straight line to upper tympanum border, broadly curving obliquely downward along posterior border of tympanum terminating above shoulder on each side ( Figure 16 (c)); thin dorsolateral ridge extends from posterior to supratympanic ridge to approximately 60% distance to groin on each side; a comparatively weaker, ‘ V ’ -shaped parietoscapular ridge present, its apex extending beyond level of axilla; second inverted partial ‘ V ’ -shaped ridge present on middorsum, joining laterally with dorsolateral ridges ( Figure 16 (a,c)); pectoral and femoral glands moderately well developed, weakly raised. Dermal asperities present, white and black, sparse around margin of lower jaw and on tympanic region (except tympanum), sparse on mid-dorsum increasing in density posteriorly to above cloaca, sparse surrounding cloaca extending onto ventral proximal thighs, sparse on ridges on dorsal shanks and along ventrolateral tarsus; absent from all other surfaces.

Colour: In preservation: Dorsal and lateral surfaces of head, body, hindlimbs and forearms dark greyish-brown, slightly lighter on flanks and dorsal surfaces of upper arms; solid dark brown triangular marking on dorsal surface of head; wide vertical dark brown bar below eyes; tympanum dark brown; posterior half of supratympanic ridges yellowish-cream, anterior half mottled yellowish-cream and brown; dorsal surface of outer three fingers with dark brown blotches; lateral surfaces of thighs and shanks with dark brown spots and blotches. Throat primarily plain mid-greyish-brown, fading posteriorly on abdomen to primarily creamish-white; lower jaw with light grey and dark brown blotches circummarginally; ventral surfaces of forelimbs, and hindlimbs mottled pale brown and yellowish-cream; area surrounding vent and posterior surfaces of thighs dark brown; ventral surfaces of tarsus and feet dark brownish-grey with contrasting light grey callous ridges on toes; light grey oval patch on region where inner metatarsal tubercle would be on other species; hands ventrally light grey; pectoral and femoral glands yellowish-cream. In life ( Figure 16 (a – c)): Markings same as in preservation, colouration generally richer; groin without contrasting colouration; dorsal and lateral surfaces of head, body and limbs dark olive green with ridges, granules and tubercles bright orange, dense orange speckling on dorsal surfaces of limbs and digits and on lower flanks; throat dark grey, grading to olive green on chest and mottled white on abdomen, with dense orange speckling on chest and anterior abdomen; ventral forearms and shanks mottled and blotched dark brown and white, ventral thighs brown speckled with white granules; pectoral glands white, femoral glands orange with white tips; ventral hands, feet and shanks dark grey; pupil with faint light circummarginal ring, otherwise iris primarily brown and gold speckled.

Variation. See Table 2 for morphometric characters of 22 adult males and three adult females. Other referred specimens agree with that described above in general morphology, with the following exceptions: on several specimens, toe III is equal in length to toe V; relative finger length formula varies, I = II <IV < III, I = II = IV < III, I <II <IV < III and VI <I = II < III; swollen portion of vomerine ridges may be almost circular or oblong, and can appear to be positioned closer to each other, closer to choanae, or equally distant from either; enlarged portion of vomerine ridges may be weak, moderately well developed, or occasionally absent (e.g. SDBDU 2009.110 ; CES 19907); vomerine teeth small when present; posterior medial edge of tongue typically weakly bifurcate, though this bifurcation is not obvious on some specimens presumably due to preservation condition, medial lingual process always absent; presence and extent of dorsolateral ridges vary considerably between individuals, from up to ~80% trunk length to completely absent; supratympanic ridge conceals upper border of tympanum on some specimens; outer upper eyelid can have a short transverse dermal ridge, a small tubercle, or neither a ridge nor tubercle; pectoral and femoral glands may be small to relatively large in diameter, and can appear flat or weakly raised on specimens in preservation; parietoscapular and sacral ridges vary considerably between individuals, with the following configurations observed: anterior only ‘ V ’ -shaped, ‘ \ / ’ -shaped, or ‘) (’ -shaped, or ‘ X ’ -shaped parietoscapular ridge configurations; on mid-dorsum a complete or incomplete inverted ‘ V ’ or ‘ U ’ -shaped sacral ridge configuration; both a ‘ V ’ -shaped parietoscapular ridge and an inverted ‘ U ’ -shaped sacral ridge, which may or may not connect with parietoscapular ridge; white and/or black dermal asperities cover on males varies by individual, and may also be present or absent on the following surfaces: along upper lips and anterior lateral surface of snout, sparse patch surrounding cloaca can extend onto ventral proximal thighs, few may also be scattered elsewhere on ventral thighs and shanks, and posterior upper eyelids; on females, dermal asperities sparse on mid-dorsum, increasing posteriorly to above cloaca, but absent from all other surfaces; thenar tubercles can be moderately well developed; outer metacarpal tubercles distinct on some specimens; digit tips appear slightly expanded on many specimens, particularly those from Kohima area ; extent of dorsal and lateral tubercles and short ridges on body and limbs varies extensively between individuals ( Figures 15 and 16 ) . Colouration and markings vary considerably between individuals ( Figures 15 and 16 ); groin region and rear of thighs of some males and females with contrasting colouration from pale orange to a deep orangish-red (e.g. Figure 16 (d)).

Secondary sexual characters. Males: typically have slightly raised nuptial pads covered with black micro-asperities, oval on finger I, positioned on mid-dorsal surface of digit base, extending approximately half of length of proximal phalange; nuptial pad small and oval or circular shaped on finger II, on mid-dorsal surface of base of digit; external vocal sac distinct on some specimens as loose skin, forming a large single subgular sac that extends onto anterior chest when fully inflated; internal vocal slit present on floor of mouth, near rear of lower mandible on both sides; forearms slightly to moderately enlarged relative to upper forelimbs; fleshy projection above cloaca absent. Females: nuptial pads, external vocal sac, internal vocal slits, and enlarged forearms, all absent; dermal asperities restricted to posterior dorsum; ova unpigmented.

Morphological comparisons. Megophrys zunhebotoensis (adult males N = 22, adult females N = 3) differs from the following species that have not yet been assigned to a subgenus or species group through molecular analyses: from M. damrei and M. shuichengensis by smaller adult size, male SVL 28.4 – 33.9 mm, female SVL 37.0 – 39.5 mm (vs. M. damrei : adult male SVL 47.7 – 57.1 mm, N = 7, adult female SVL 69.1 mm, N = 1 [Mahony 2011; Neang et al. 2013]; M. shuichengensis : adult male SVL 102.0 – 118.3 mm, N = 8, adult female SVL 99.8 – 115.6 mm, N = 7 [ Tian et al. 2000]); from M. feii by larger adult size, male SVL 28.4 – 33.9 mm, female SVL 37.0 – 39.5 mm (vs. adult male SVL 24.3 – 25.1 mm, N = 4, adult female SVL 28.2 – 28.9 mm, N = 2), lateral dermal fringes on toes absent (vs. present), and nuptial pads on fingers of males present (vs. absent) ( Yang et al. 2018).

Megophrys zunhebotoensis differs from M. parva s.s. by typically smaller adult size, male SVL 28.4 – 33.9 mm, female SVL 37.0 – 39.5 mm (vs. male SVL 33.9 – 36.0 mm, N = 2, female SVL 41.1 – 41.4 mm, N = 2), and typically larger eye length relative to snout length, EL/SL (mean±SD) 103.2 ± 5.8%, range 87.2 – 112.8%, N = 26 (vs. EL/SL 93.5 ± 1.7%, range 90.7 – 95.2%, N = 4).

Megophrys zunhebotoensis differs from all species molecularly assigned to the M. (X.) megacephala SG based on the following characters: from M. ancrae by smaller adult male size, SVL 28.4 – 33.9 mm (vs. SVL 39.1 – 45.0 mm, N = 8), upper eyelids with a short ridge or blunt tubercle, when present (vs. sharp horn-like tubercle), tympanum circular (vs. oval); from M. megacephala by smaller adult size, male SVL 28.4 – 33.9 mm, female SVL 37.0 – 39.5 mm (vs. male SVL 45.9 – 53.4 mm, N = 7, female SVL 49.3 – 64.0 mm, N = 3), and narrower head HW/SVL 32.3 – 37.5%, N = 25 (vs. HW/SVL 40.2 – 45.1%, N = 12); from the typically larger sized species M. oropedion and M. serchhipii , by adult male SVL 28.4 – 33.9 mm, female SVL 37.0 – 39.5 mm (vs. M. oropedion male SVL 32.8 – 39.2 mm, N = 9, female SVL 44.1 – 48.7 mm, N = 2; M. serchhipii male SVL 36.1 – 46.7 mm, N = 25, female SVL 46.1 – 53.0 mm, N = 4).

Refer to the ‘ Morphological comparison ’ sections of Megophrys dzukou sp. nov., Megophrys awuh sp. nov., and Megophrys numhbumaeng sp. nov. for further diagnoses. Etymology. The specific epithet ‘zunhebotoensis’ is a toponym after the locality where the type specimens were collected.

Suggested common name. ‘ Zunheboto Horned Frog ’ has been suggested by Dinesh et al. (2009).

Distribution. Prior to this study, Megophrys zunhebotoensis was known only from the type locality. This study considerably extends the geographical distribution and elevational range (~ 810 – 1820 m asl.). In Nagaland, it was found in Zunheboto district in the north, and numerous localities in Kohima district in the south of the state ( Figure 2 ). In western Manipur state, it has been found from a couple of localities in Churachandpur district ( Figure 2 ). Reports of this species from elsewhere in NEI are erroneous (see Remarks section below).

Habitat and natural history. At Vibalieza and Sechüma village, calling males were all found among wet leaf litter, bushes and grass (perched up to 1.3 m above ground level) next to seasonal small (~ 1 m wide with ~ 0.3 m water level) rocky hill streams between 18:00 and 20:15 h during late May to mid-June. The males were all located by their calls, while females were located during opportunistic searching of the same habitat. These streams flowed through moderately dense secondary forest. Heavily gravid females were found on roadside vegetation below 0.5 m from ground level during early and late June; SDBDU 2007.139 was found on a dirt road after heavy rains. At the type locality, calling males were collected from stems and leaves of ferns and bushes ( Eupatorium sp. Linnaeus) on the banks of the Nguti stream, perched between 0.5 and 1 m above ground level. Nguti stream is a very small narrow hill stream; when RGK visited the site in May 2013, the water level was quite low (~ 30 cm in depth), the borders of the stream quite dry and anthropogenically disturbed — there were at least a dozen water pipes, as are nearly always the case in NEI where there is no piped water supply and local people harvest water directly from hill streams. The species was observed to be quite common around the village of Sukhalu, and in and around Zunheboto town where its calls were heard from numerous roadside streams within the town. The Manipur populations were collected between 18:30 and 20:00 h from bushes alongside hill streams in relatively intact secondary forest. The calling males were collected from ground level under leaf litter or from leaves and stems at about 0.5 m above ground level.

Remarks. Similar technical issues discussed above regarding the original description of M. serchhipii also apply to the description of M. zunhebotoensis , except that the type specimens were adults ( Mathew and Sen 2007) in this case. Mathew and Sen (2009) provided low-resolution colour images of the holotype. Considering this species appears to be quite common around Kohima town, the capital of Nagaland state, and relatively widespread in the region, it is likely that specimens of this species might be misidentified in other collections.

Saikia and Sen (2012) provided a short description and photographs of a specimen ( V /A/ ERS/1009) from Mawmluh, near Sohra (spelled ‘ Cherrapunjee ’) in Meghalaya which they identified as M . zunhebotoensis. They noted that the specimen is considerably larger than the type specimens of M. zunhebotoensis, SVL 55 mm (vs. <40 mm). The photographs of the specimen ( Saikia and Sen 2012, Pl. 1) and SVL correspond morphologically with M . serchhipii which is now known to be present in the area based on historical collections (this study). Kharkongor et al. (2018) also reported the same specimen ( V /A/ NERC/1009 ) as M . ‘ zunhebotoensis’ but with the locality ‘ Mawbah area, near Cherrapunjee, East Khasi Hills , Meghalaya ’. Sangma and Saikia (2015) reported M. ‘ zunhebotoensis’ from Tura Peak ‘ (N 25° 30 ′ 56.5 ″ & E 90°30 ′ 19.2 ″) at an elevation of 845 m ’ based on a single specimen that was not collected, with SVL of either ‘ 8.5 cm ’ (p. 2410) or ‘ 95 mm ’ (p. 2408) . The figured animal ( Sangma and Saikia 2015, Pl. 7a) clearly represents a member of the M. (X.) major SG (see Mahony et al. 2018), and not M. zunhebotoensis (maximum SVL <40 mm). Saikia et al. (2017) provided notes, basic measurements and a photo of a specimen ( ZSI / V / APRC /A-111) from Papum Pare district , Arunachal Pradesh which they identified as M . zunhebotoensis. The large size ( SVL 66.3 mm) and photo of the specimen indicate that it may represent one of the M. (X.) major SG taxa, but certainly not M. zunhebotoensis . Saikia and Sinha (2018) subsequently referred the same specimen to M. robusta Boulenger, 1908 without justification. Considering that insufficient morphological information was provided in Saikia et al. (2017) and Saikia and Sinha (2018) to verify the specimen ’ s identification, we suggest that the identity of this specimen be considered unverified and should not be considered conspecific with M. zunhebotoensis .

See Figures 1, S1 , & S3 and the remarks section for Megophrys awuh sp. nov. for a note on the systematic position of this species in the M. (X.) megacephala SG.

Figures

Figure 1. ML phylogenetic tree of the subgenus Megophrys (Xenophrys) based on the concatenated mt +nuDNA alignment. Bootstrap values ≥95% are represented by a black spot; 80–95% represented by a grey spot; <80% not given. Numbers next to species names correspond with specimen numbers in Table 1.

Figure 2. Topographic distribution map of the Megophrys (X.) megacephala SG taxa: Left. All taxa from Northeast India and surrounding countries: diamonds represent type localities; circles represent referred localities based on examined specimens; circles with central dot represent identifications based on literature where sufficient evidence was available (see Remarks sections); Right. Inset rectangle enlarged to show the distributions of species from more densely sampled southern Nagaland and northern Manipur states, Northeast India. Blue lines represent major rivers; grey lines represent international borders.

Figure 15. Megophrys zunhebotoensis adult female holotype (ZSI/ERS V/A/774: SVL 39.0 mm: Mathew and Sen 2007) in preservation, from Zunheboto district, Nagaland state, India: (a). dorsal view; (b). ventral view; (c). profile view; (d). ventral view of hand; E. ventral view of foot.

Figure 16. Megophrys zunhebotoensis adult referred specimens, from India: (a–c). male topotype (CES 19909: SVL 33.2 mm) from Zunheboto district, Nagaland state: (a). dorsal view after euthanisation; (b). ventral view after euthanisation; (c). dorsolateral view in life; (d). female (CES 19901: SVL 39.5 mm) in life, from Puliebadze forest, Kohima district, Nagaland state; (e). female (SDBDU 2009.342: SVL 39.1 mm) in life, from Puliebadze forest, Kohima district, Nagaland state; (f). adult male (SDBDU 2009.110: SVL 29.5 mm) in life, from Churachandpur district, Manipur state.