Cryptic diversity within the Megophrys major species group (Amphibia: Megophryidae) of the Asian Horned Frogs: Phylogenetic perspectives and a taxonomic revision of South Asian taxa, with descriptions of four new species Author Mahony, Stephen Author Kamei, Rachunliu G. Author Teeling, Emma C. text Zootaxa 2018 2018-11-19 4523 1 1 96 journal article 27943 10.11646/zootaxa.4523.1.1 23903efe-ba7a-438c-a04f-d4b08680b640 1175-5326 2610202 96B7B9E3-9F49-4983-A46C-D29CD6B2EE49 Megophrys ( Xenophrys ) glandulosa Fei, Ye and Huang, 1990 ( Figure 24 ; Table 1 ) Megophrys glandulosa Fei, Ye and Huang 1990 :99 , 273. In : Key to Chinese Amphibians. Publishing House for Scientific and Technological Literature, Chongqing , China : 364 pp. + 2 + [iv]. Holotype . Adult male ( CIB 873112 : Figure 24 ), from “Wuliang shan, Jingdong, Yunnan Province , altitude 1900m ” (= Wuliang Mountain [~ 24°49'27"N , 100°26'31"E ], Jingdong Yi Autonomous County , Pu’er Prefecture , Yunnan Province , China ), collected by Liang Fei on 29 March 1987 ( Fei et al. 1992 ). Paratypes . Adult female (“ allotype ” CIB 873201), from the “same locality as that of the holotype , altitude 2100m ”, collector not mentioned, 0 2 May 1975 ; 25 males and two females (specimen numbers not mentioned in Fei et al. [1992] ), from “Wuliang shan, Jingdong, Yunnan Province , altitude 1900–2100m ”, collectors Liang Fei, Younzhao Huang and Jiarui Luo, between 29 and 30 March 1987 ( Fei et al. 1992 ). Examined specimens. Adult male (CIB 873112––photos only), holotype . Provisionally referred examined specimens. Two adult males (CAS 221395, CAS 221484), from two localities on the road between Ahtonga and Babaw ( 27°15'27.2"N , 97°50'32.4"E and 27°17'24.3"N , 97°51'52.4"E ), Machanbaw township, Putao district, Kachin state, Myanmar , collected by H. Win and R. Shaung on 0 5 September 2001 , and J.B. Slowinski, D.-O. Rao, G.O.U. Wogan, H. Win, A.K. Shein and H. Tun on 0 7 September 2001 ; one adult male ( CAS 221442 ), from Aureinga Camp ( 27°17'36.4"N , 97°51'50"E ), Naung Mon township , Putao district , Kachin state, Myanmar , collected by J.B. Slowinski , G.O.U. Wogan, H . Win and A.K. Shein on 0 7 September 2001 . Description of type series. Refer to Fei et al. (1992) for the description in Chinese language text, and Huang et al. (1998) for the English translation of Fei et al. (1992) . See Figure 24 for colouration in preservative of the holotype . Description of referred specimen CAS 22 1442 (measurements in mm). Mature male (SVL 81.0). Head large (HW 31.3, HL 30.2, IFE 13.6, IBE 21.2), wider than long, snout broadly pointed in dorsal view, obtusely protruding beyond mandible in lateral view, without rostral appendage; loreal region acute, concave, with well developed canthus rostralis; dorsal surface of snout concave; eye diameter larger than maximum tympanum diameter, and shorter than snout (EL 7.9, TYD 5.1, SL 10.1); eye–tympanum distance (TYE 6.7) longer than tympanum diameter; tympanum distinctly oval, obliquely orientated, upper ~10% concealed by supratympanic ridge; pupil vertically elliptical; nostril positioned laterally, oval, obliquely oriented with raised posterior rim, closer to eye than to snout (EN 4.6, SN 6.2); upper eyelid width subequal to narrowest point between upper eyelids, and less than internarial distance (UEW 7.5, IUE 7.6, IN 9.3); pineal ocellus absent; vomerine ridges well developed, ovoid, positioned between choanae, extending posterior to choanae, slightly closer to choanae than to each other; vomerine teeth present, moderately long; maxillary teeth present; tongue moderately large, distinctly notched posteriorly, medial lingual process absent. Forelimbs moderately long, thick; forearms enlarged relative to upper forelimbs, and shorter than hand length (FAL 17.3, HAL 21.3); fingers moderately long, narrow, finger length formula IV<I=II<III (FIL 10.6, FIIL 10.6, FIIIL 13.1, FIVL 8.4); interdigital webbing, lateral fringes, subarticular and supernumerary tubercles absent; thenar tubercle distinct; metacarpal tubercles absent; digit tips slightly dilated, flattened, with subcircular pads, terminal grooves on pads absent. Hindlimbs relatively long, thin; thigh length slightly shorter than shanks, and longer than feet (TL 39.3, SHL 41.4, FOL 37.9); toes long, thin, relative toe lengths I<II<V<III<IV; digit tips not dilated but flattened, with subcircular pads, terminal grooves on pads absent; toes with thick basal webbing, rudimentary between digits I and II, remaining webbing formula as follows: II1.9– 3III 2.3–3.9IV3.8– 2V ; moderately wide lateral fringes present on all toes; outer metatarsal, subarticular and supernumerary tubercles all absent; inner metatarsal tubercle present but barely distinguishable; ridge of thickened skin absent on ventral surface of digits. Skin on dorsal surfaces of snout, head and back primarily smooth; throat, chest and limbs smooth; flanks with moderately large tubercles approximately forming two longitudinal rows, interspersed with densely scattered small granular tubercles; posterior thigh and cloacal region primarily smooth with small scattered weakly raised tubercles; tympanum mostly smooth, slightly concave; sides of head finely granular; palpebral horn absent, replaced by short fleshy bump; supratympanic ridge narrow anteriorly, extends from posterior orbital border, curves down along upper and posterior border of tympanum, considerably broadening posteriorly, terminating above shoulder; narrow, raised dorsolateral ridge extending posteriorly from behind supratympanic ridge to ~75% trunk length on both sides; weakly raised V-shaped parietoscapular ridge present, extending posteriorly from temporal region on each side, meeting medially at level of forelimb insertion; pectoral glands flat, level with axilla on chest; femoral glands slightly raised, on posterior surface of thighs, closer to knees than to cloaca; small black and white dermal asperities form a broad dense band circummarginally on gular region, moderately dense on tympanic regions between tympanum and eyes, and along upper lips, sparse on anterior dorsum of body restricted to dorsal ridges, increasing in density posteriorly across dorsum, absent from all remaining surfaces. FIGURE 24. Megophrys glandulosa holotype: adult male (CIB 873112: SVL 78.4 mm [Fei et al. 1992]) in preservation: A . dorsal view; B . ventral view; C . profile view of head; D . ventral view of hand; E . ventral view of foot. Colouration : In preservative : Dorsal and lateral surfaces of head and body primarily plain brown; light-edged, dark brown triangular marking between eyes; faint darker brown V-shaped marking on anterior dorsum surrounding parietoscapular ridge, narrow broken dark brown stripe follows lower edge of dorsolateral ridges; larger tubercles on flanks dark brown with light tip; front of snout and lateral surfaces below canthus rostralis dark brown; greyish-white stripe on upper lip extends from nostril to rear of upper jaw, interrupted by wide dark brown vertical bar between lower edge of orbits and edge of mouth; besides narrow brown oblique stripe extending from posterior edge of orbits posteriorly to join light upper lip stripe, remaining lateral surfaces of head below supratympanic ridges solid dark brown; outer edges of eyelids dark brown; lower half of supratympanic ridges dark brown, upper half brown anteriorly, light yellowish-cream posteriorly; dorsal surfaces of forelimbs and hindlimbs brown; two dark brown blotches on anterior lateral surface of forearms; dorsal surface of outer three fingers with dark brown blotches; dorsal surfaces of hindlimbs with distinct brown transverse crossbars; outer lateral surfaces of thighs and shanks with dark brown spots and blotches; throat with large light brown blotches, few small white spots along its edge, light-edged wide dark brown stripe extends from posterior edge of lower jaw to ventral surface of upper forelimb on each side; chest and abdomen with faint large brown blotches on an otherwise pale greyishwhite background; ventral surfaces of forelimbs pale greyish-white; ventral surfaces of thighs densely mottled light brown and greyish-white, posterior surfaces of thighs (including area surrounding cloaca) and ventral surfaces of shanks and tarsi primarily mid to dark brown with pale greyish-white scattered spots; some large dark brown spots and blotches laterally along abdomen on both sides; ventral surfaces of hands and feet greyish-brown; pectoral and femoral glands creamish-white. In life : Not documented for this specimen. Variation. Refer to Table 1 for morphometric variation within the provisionally referred specimen series, consisting of three adult males. The two other referred specimens generally resemble the referred specimen described above for most morphological characters with the following exceptions: CAS 221484 has more extensive webbing between Toes II to V (i.e., webbing formula: II2 –3.1 III2.8 – 4 IV 4– 2.5 V); CAS 221484 has relative finger lengths II=I< IV < III , CAS 221395 has IV <II<I< III ; finger tips not dilated relative to finger width on CAS 221484 and CAS 221395 ; vomerine teeth absent on CAS 221484 ; dorsolateral ridges extend almost entire trunk length on CAS 221484 ; 5–10% of upper tympanum surfaces are concealed by supratympanic ridges; on CAS 221395 , dermal asperities moderately dense on lateral surfaces of snout, dorsal surface of eyelids and dorsally on head adjacent to supratympanic ridges, sparse on dorsal tibia, outer and ventral tarsal surfaces; on CAS 221484 , dermal asperities formed dense wide circummarginal band along lower jaw, sparse on tympanic regions (absent on tympanum) and on posterior lateral dorsum, absent on all remaining surfaces; V-shaped dorsal marking absent on CAS 221484 . Secondary sexual characters. Males : nuptial pads present, weakly raised, covered with black micro-granules, covering almost entire dorsal surface of Finger I narrowing distally where it extends to base of distal phalange on inner dorsal side; nuptial pad small to moderately large on Finger II, positioned on base of digit on inner dorsal side (extending on to base of distal phalange on some individuals); external vocal sac indistinct; internal vocal slit present on floor of mouth on each side near rear of mandible; forearms enlarged relative to upper forelimbs. Females : not examined in this study. Morphological comparison. Adult body size ranges provided for Megophrys glandulosa include the measurements given in Fei et al. (2009) and the referred specimens examined in this study (total adult males, N =13; adult females, N =3). The remaining characters were assessed based only on the referred specimens and images of the holotype (total: adult males, N =4). Megophrys glandulosa differs from M. medogensis , M. zhangi , M. monticola , Megophrys periosa sp. nov. and M. robusta by the presence of a distinct white upper lip stripe (vs. absent), presence of broad lateral fringes on toes (vs. absent on M. medogensis , M. zhangi , M. monticola , and M. robusta ; usually absent, though very narrow when present on Megophrys periosa sp. nov. ), and differs further from M. medogensis , M. zhangi , and M. monticola by its larger adult size, male SVL 76.3–81.0 mm, female SVL 76.5–99.5 mm (vs. male SVL 57.2–68.0 mm, N =16; male SVL 32.5–37.2 mm , N =3; male SVL 38.2–49.5 mm , N =17, female SVL 40.5–56.1 mm , N =6, respectively); differs from Megophrys himalayana sp. nov. and M. mangshanensis by its larger adult male size, SVL 76.3–81.0 mm (vs. male SVL 68.0– 73.5 mm , N =7; male SVL 62.5 mm , N =1, respectively), and by broad lateral fringes on toes present (vs. absent); differs from M. major s.s. and Megophrys oreocrypta sp. nov. by presence of broad lateral fringes on toes, and toe tips not expanded (vs. occasional presence of narrow lateral fringes on toes, and toe tips distinctly expanded relative to toe width), ventral surface of thighs densely spotted and speckled (vs. immaculate); differs from Megophrys flavipunctata sp. nov. by its larger adult size, male SVL 76.3–81.0 mm, female SVL 76.5– 99.5 mm (vs. male SVL 56.9–68.4 mm , N =4, female SVL 68.0– 74.6 mm , N =3), by toe tips not expanded relative to toe width (vs. toe tips slightly expanded), ventral thighs densely spotted and speckled (vs. immaculate). Systematic position. The systematic position of Megophrys glandulosa within the MMC could not be resolved in this study possibly due to incomplete sampling of nuclear markers (i.e., absence of CXCR4, TTN and SACS; Appendix I, Table 2). Analyses of the mtDNA datasets (16S and CO1 gene trees, and 16S+CO1 concatenated tree), the RHOD gene, and the concatenated mt+nuDNA dataset indicated that this species is a distinct lineage ( Figure 4 ; Appendix II, Figure 5 ), however, the RAG1 gene tree (not shown) and concatenated nuDNA analyses indicated that this species may have close affinity to the species referred to here as M. cf. maosonensis [1], though this relationship received very low support (Appendix II, Figure 6 ). Etymology. The specific epithet “ glandulosa ” is Latin, with glandul meaning “gland”, and the suffix - osa meaning “abundant”, presumably a reference to the tubercles on the flanks of this species, a character that is not useful for diagnosing this species from other species in the MMC. Suggested common name: Glandular White-lipped Horned Frog. Distribution. Besides the type locality, M. glandulosa has been reported from numerous localities in Yunnan Province between 1900 and 2500 m asl. (e.g., Jiang et al. 2003 ; Fu et al. 2006 ; Fei et al. 2009 ), and Kachin state, northern Myanmar by Wogan et al. (2008) ( Figure 8A ). Reports of this species from further west in Northeast India and Bhutan are not here considered reliable (see Remarks below). Remarks. Megophrys glandulosa was described (in Chinese text) as new twice based on the same type series ( Fei et al. 1990 , 1992). Fei et al. (1992) was subsequently translated into English by Huang et al. (1998) . It is highly unlikely that the Bhutan ( Wangyal 2013 ) and Indian ( Meghalaya , Nagaland and West Bengal states: Ao et al. 2003 ; Deuti & Ayyaswamy 2008 ; Mathew & Sen 2010 ; Sangma & Saikia 2015 ) populations are conspecific with Megophrys glandulosa s.s. Ao et al. (2003) reported a specimen of this species from Puliebadze ( 25°37'0"N , 94°5'0"E , 2225 m asl.), Kohima district, Nagaland state, Northeast India . Though we have not examined this specimen, we report two species of MMC from Kohima district in this study ( M. major s.s. 450– 1255 m asl. and Megophrys flavipunctata sp. nov. 1575–1810 m asl.). Based on the elevation that Ao et al .’s (2003) specimen was collected, we suspect that it might represent Megophrys flavipunctata sp. nov. Mathew and Sen (2010) provided an undiagnostic description of M. glandulosa for India with an accompanying photo of a specimen that appears to represent M. major s.s. A report of two specimens of Megophrys [as Xenophrys ] glandulosa from Tura Peak, West Garo Hills, in Meghalaya state provided by Sangma and Saikia (2015 : 2407, pl. 4a) appears to represent an adult Megophrys oreocrypta sp. nov. based on the figure provided for one of the specimens. An additional report of M. glandulosa by Deuti and Ayyaswamy (2008) was based on a collection from Latpanchar, Darjeeling district, West Bengal state, Northeast India . The figured individual displays typical characters seen on M. robusta , i.e., slightly enlarged posterior supratympanic ridge (vs. greatly enlarged, and beanshaped on M. glandulosa [ Figure 24C ]); the distinctive white upper lip stripe of M. glandulosa is not apparent on the figured animal, and the iris colour matches that of M. robusta perfectly. Although some of the characters that were described, such as ventral markings, could correspond with M. glandulosa , other characters such as swollen digit tips, and rudimentary webbing between toes do not (see description provided above). Pending re-examination of the specimens reported by Deuti and Ayyaswamy (2008) , we recommend that Darjeeling, and Northeast India in general, are not included in the distribution of M. glandulosa . Wangyal (2013) reported M. glandulosa and M. major from Bhutan , however, the two specimens photographed exhibit characters that allow a reasonable preliminary identification as M. robusta , i.e., both lack the light upper lip stripe seen on M. glandulosa and M. major , and have pale iris colouration that is characteristic of the M. robusta / M. medogensis clade in the MMSG.