Megophrys cf. pachyproctus, Huang, 1981

Shi, Shengchao, Zhang, Meihua, Xie, Feng, Jiang, Jianping, Liu, Wulin, Li Ding,, Luan, Li & Wang, Bin, 2020, Multiple data revealed two new species of the Asian horned toad Megophrys Kuhl & Van Hasselt, 1822 (Anura, Megophryidae) from the eastern corner of the Himalayas, ZooKeys 977, pp. 101-161 : 101

Megophrys cf. pachyproctus Figs 3C, H, M, R, W , 4B, E, H, K , 5C, H , 6C, G, K, O , 7 , 10C, D, H, I , Suppl. material 2: Figs S2, S5B, S5F; Tables 1 , 3, 4, Suppl. material 1: Tables S1, S2, S3, S5

Megophrys cf. pachyproctus Huang, 1981***

Specimens examined.

Four adult males, CIB022017061805 (Figs 3C, H, M, R, W , 5C, H , 7 ), CIB201706MT04, CIB022016061806, CIB022017061807, collected from Bari village, Medog County, Tibet Autonomous Region, China (29.32947°N, 95.36016°E, 1780 m) by SC Shi and L Ding, on 18 June 2017. One adult male (CIBMT171056), four adult females in gravidity (CIBMT171052, CIBMT171057, CIBMT171058, CIBMT171054), and one male toadlet (CIBMT171059) were collected from vicinity of Renqingbeng Temple (29.304832°N, 95.361682°E, 2003 m) by SC Shi on 26 October 2017.

Description of the representative (referred) specimen.

Adult male, CIB022017061805 (Figs 3C, H, M, R, W , 5C, H , 7 ). Measurements in mm. Body stout, relatively small size (SVL 34.8); protuberance beyond cloaca small, barely visible from ventral view, not swollen.

Head moderately large, wider than long (HW 12.3, HL 11.0, IFE 6.5, IBE 10.4); snout rounded in dorsal view, slightly projecting in profile, protruding beyond lower jaw; rostral appendage absent (SL 4.6); canthus rostralis blunt; loreal region concave, dorsal surface of snout slightly concave; nostril oval, nearly in the middle of distance from snout to eye (SN 2.2, EN 2.3), distance between nostrils almost equal to distance between upper eyelids (IN 3.9, IUE 3.8); tympanum smaller than half of eyes (EL 4.5, TYD 1.8); eye-tympanum distance subequal to tympanum diameter (TYE 1.7); tympanum irregular rounded, upper 1/3 conceal with supratympanic ridge; interorbital space flat, larger than upper eyelid (UEW 3.2); pineal ocellus not visible; vomerine ridges distinct, orientation of two ridges acutely angled, enlarged at ends where bearing several vomerine teeth; maxillary teeth present; tongue notched posteriorly, medial lingual process absent.

Forearm moderately long and wide, similar size of upper arms, shorter than hand (FAL 7.5, HAL 9.6); fingers long and thin, with rudimentary webbing; narrow lateral fringes present on finger III, indistinct on other fingers; subarticular tubercles absent; inner and outer metacarpal tubercles mostly fused, large, with the size of base of finger I; finger length formula I <II <IV <III; base of finger I strong, larger than base of finger II; tips of fingers slightly swollen, without pads (FIIIW 1.1).

Hindlimbs thin and long; tibio-tarsal articulation reaches middle eye; thighs shorter than shanks but longer than feet (TL 16.5, SHL 17.2, FOL 15.2, TFOL 24.0); toes long and thin, relative lengths I <II <V <III <IV, rudimentary webbed, with narrow lateral fringes, tips rounded, dermal ridges continuously present on ventral surface; subarticular tubercles absent; outer metatarsal tubercle tiny and rounded; inner metatarsal tubercle distinct (IMT 1.6), nearly oval, partially fused with toe I.

Skin. Dorsal surface of head and body rough, densely scattered with small granules; temporal region and upper corner of mandible with rough granules; tympanum ring slightly raised; several small granules on edges of upper eyelids; supratympanic ridges extend from posterior upper eyelids to above forearm insertions, curving above tympanum, rear part thicker than the front; skin on flanks smoother than skin on dorsum, with several large warts and lesser granules; dorsolateral ridges distinct, irregularly stretch from above shoulder to near groin; a transverse skin ridge between upper eyelids; a near “V” -shaped skin ridge between shoulders, connected with the right dorsolateral ridge by a short skin ridge, a tubercle present near the end of “V” -shaped skin ridge; two oblique skin ridges connected with dorsolateral ridges at posterior; dorsal surface of upper arm covered with small granules in three rows from shoulder to elbow; small granules on dorsum of lower arm, hand, and hindlimbs, four transverse rows of granules on thighs and shanks; ventral surface of body and limbs smooth; pectoral glands small and rounded, with the size of first fingertip, close to axilla on chest; femoral glands small, closer to outer edge of knee than to cloaca.

Coloration in preservative.

(Fig. 3C, H, M, R, W ). Dorsal surface of head gray; dorsal surface of body pale gray; a darker gray triangle bet between eyes, little lighter in center, anterior corners reach to near out edge of upper eyelids; area around dorsal skin ridges darker, no clear “X” -shaped markings on dorsum; tubercles on flanks white and edged with dark patches on one side; lateral surface of head mottled with pale gray and grayish white; a dark stripe extend from behind upper eyelid to behind corners of the mouth, thicker in the middle, and covers tympanum entirely; no long white stripe present on upper lip; two dark strips from eyes to upper lips, two short dark bands on upper lips before eyes; iris dark covered with silver pigments radiated from pupil; dorsal and lateral surface of limbs pale gray with darker transverse bands, one or two broad dark brown transverse bands on forearms, and four indistinct transverse bands on dorsal thighs and shanks, dorsal tarsal pale gray with three indistinct transverse bands, dorsal surface of fingers and toes also covered with several darker transverse bands; gular and chest dusty white; edge of lower mandible white with five brown patches, the pair corresponding to places between nasals and eyes are largest; a short longitudinal light brown stripe present in middle of throat, two pairs of faint brown patches beside the short longitudinal light brown stripe; a brown stripes extending from posterior end of jaws to base of forearms on both sides; skin around pectoral glands faint brown, three medium size faint brown patches present on dusty white upper abdomen, lower abdomen cream-white reticulated with dusty brown pigments, no large longitudinal dark patches present on ventral lateral abdomen; ventral surface of forelimbs and hindlimbs dusty brown, mottled with several irregular brown patches; pectoral and femoral glands cream-white; nuptial pad grayish black.

Coloration in life.

(Fig. 7 ). Markings as described in preservative; flanks, lateral sides of head, dorsal surface of head, body, and limbs light brown in general with orange-red granules; tympanum and stripes under eyes brown; several cream-white dots present on flanks; two dark brown transverse bands present on forearms; four dark brown transverse bands present on thighs, shanks, and tarsi; ventral surface of head, and abdomen grayish white basically, two large longitudinal brown present on lateral sides of abdomen; chest, ventral surface of hand, thigh, and feet flesh colored; skins around cloaca, on groin, and anterior, posterior and ventral thigh without orange patches; iris dark brown reticulated with dense golden pigments, pupil edged with diamond-shaped golden ring; nuptial pad gray.

Skull.

(Fig. 5C, H ). Skull weakly ossified, width 1.15 × of length; maxillary overlapping with the quadratojugal; premaxillary and maxillary teeth weakly developed, most tooth separated from others by a distinct gap, 10/10 teeth present on left/right premaxillary, teeth absent on mandible; vomerine ridge moderate, few vomerine teeth weak, present on enlarged posterior end of vomerine ridge; nasal process of premaxilla protruding beyond skull; nasal bones separated from each other, half connected with sphenethmoid; sphenethmoid rough with curves and pits on dorsal and ventral surface, middle one third of front edge free from nasal bones, and protruding forward, separated from premaxilla; frontoparietal divided by a distinctly open sagittal suture, slightly wider posteriorly; anterior fontanelle small, slightly wider sagittal suture; front and rear part of frontoparietal almost equally wide; posterior edge of exoccipitals posterior to the line connecting conjunctions of quadratojugal and mandible; pterygoid moderate; anterior process of squamosal slender and sharp, tip closer to the junction of pterygoid and quadratojugal than its base, posterior process present; front part of prootic smooth, rear part rough, separated from exoccipitals; anterior process of parasphenoid in shape of fusiform, anterior part not raised above sphenethmoid, conjunction of parasphenoid anterior process meet with sphenethmoid narrow, width ca. half the constriction near its base; columella auris short.

Variation.

(Suppl. material 2: Fig. S2). The topotypes have the following differences: tympanum diameter/eye diameter ratio varies from 0.40 to 0.60 for adults, 0.36 for the juvenile CIBMT171059; skin ridges between dorsolateral ridges on dorsum vary in configuration, i.e., "> <" (CIB022016061806) and “>” (CIB022017061807); and specimen CIB022017061807 with orange-red patches on groin, and flanks stained with orange-red. The three skulls similar in morphology (e.g., premaxillary and maxillary teeth weak; the nasal bones half connected with sphenethmoid; the sphenethmoid rough and protruding forward; tip of anterior process of parasphenoid narrow), but possessing following variation: vomerine teeth only present on left vomerine ridge of CIBMT171056; sagittal suture of CIBMT171056 partially occlusive near the center.

Secondary sexual characters.

Adult female with larger body size, average 1.17 × of males. Male with gray nuptial pad on inner first finger, spines on nuptial pad dense and small; single subgular vocal sac; vocal sac opening small, slit like; lineae musculinae absent.

Bioacoustics.

(Fig. 4B, E, H, K ; Tables 4 ; Suppl. material 1: Table S3). A total of 15 call groups and 82 calls were analyzed. Average dominant frequency of calls moderate, 3.2 kHz (3.2-3.3 kHz); call repetition rate moderate, average 0.9 calls per seconds; call interval long, average 493-720 ms; call groups with average 10.8 calls; call duration long (average 746 ms), and with lots of notes (average 42.1). To human ears, sound like pebbles hitting ground continuously.

Tadpole.

(Fig. 6C, G, K, O ; Suppl. material 1: Table S2). Description based on measurements and observation of tadpole specimen CIBMT20170611 at stage 25. Measurements in mm. Body 6.1, elongated; head slightly narrower than trunk; oral disk large, funnel like, positioned anterior-dorsal, width 1.6 × of body width; 4 rows of oval submarginal papillae on middle lower lip, 3 rows of oval submarginal papillae on both sides of upper lips; all these papillae range towards oral cavity; keratodonts absent; nares much closer to eyes than tip of snout (RN/NE 3.8); eyes round, positioned dorsolaterally; internarial distance (IND1.4) 85% of the interpupil distance (PP 1.63); spiracle mostly in left side of body, in right-handed helix from ventral view, the spiracular tube not protruding beyond body wall, positioned 63% of the distance between tip of the snout and trunk-tail junction, and below the horizontal mid trunk line; tail accounts 68% of total length; dorsal fin arise above trunk-tail junction, 38% of maximum body height; ventral fin connected to the trunk, with lesser height than dorsal fin, 31% of maximum body height; anal siphon opens medially; maximum tail muscle height 72% of maximum body height, maximum tail muscle width 53% of maximum body width; eleven small curves present on both lateral side of tail muscle.

When alive, dorsal body and tail basically with yellow-brown pigmentation; two golden spots in size of eyes present on dorsolateral mid body. In preservation, dorsal body, and most part of lateral tail with brown pigmentation; ventral body and tail fin semitransparent; lateral body and tail with pigmentation, but lower fin and ventral body barely pigmented.

Comparison.

By having relative smaller body size (males 33.6-36.6, n = 5; females 40.6-42.8, n = 4; measurements in mm), Megophrys cf. pachyproctus differs from M. medogensis (males 57.2-68.7, n = 21), M. caudoprocta (males 70.8-81.3, n = 4); M. hoanglienensis (males 37.4-47.6, n = 11), M. jingdongensis (males 53.0-56.5, n = 3), M. liboensis (males 61.6-62.9, n = 4), M. omeimontis (males 56.0-59.5, n = 10), M. aceras (males 55.8-62.4, n = 6); M. ancrae (males 39.1-45.3, n = 8), M. damrei (male 57.1, n = 1), M. flavipunctata (males 56.9-68.4, n = 4), M. glandulosa (males 76.3-81.0, n = 10), M. himalayana (males 68.0-73.5, n = 6), M. lekaguli (males 55.6-66.6, n = 8), M. major (males 71.6-87.5, n = 12), M. mangshanensis (male 62.5, n = 1), M. maosonensis (male 77, n = 1), M. megacephala (males 45.9-53.4, n = 12), M. monticola (males 38.4-49.5, n = 17), M. periosa (males 71.3-93.8, n = 12), M. robusta (males 73.5-83.1, n = 6), M. longipes (male 47, n = 1; female 65, n = 1), M. oreocrypta (female 94.9, n = 1), M. serchhipii (male 37.1, n = 1), and M. takensis (males 47.3-53.0, n = 3).

By having relative larger body size (males 33.6-36.6, n = 5; females 40.6-42.8, n = 4; measurements in mm), Megophrys cf. pachyproctus differs from M. zunhebotoensis (male 30.0, n = 1; female 39.0, n = 1), M. rubrimera (males 26.7-30.5, n = 8), and M. angka (males 31.2-32.1, n = 2).

By tympanum present distinctly, Megophrys cf. pachyproctus differs from M. gigantica , M. nankiangensis , and M. shapingensis (vs. absent or concealed in the latter).

By vomerine ridge and teeth present, Megophrys cf. pachyproctus differs from M. wawuensis (vs. absent in the latter).

By maxillary teeth present, Megophrys cf. pachyproctus differs from M. elfina , M. gerti , M. hansi , M. koui , M. microstoma , and M. synoria (vs. absent in the latter).

By hind limbs long and head not wide and flat, Megophrys cf. pachyproctus differs from M. carinense , M. chuannanensis , M. feae , M. intermedia , and M. popei (vs. hind limbs short and head flat wide in the latter).

By lacking a single, wide and flat palpebral projection on the edge of the upper eyelid, Megophrys cf. pachyproctus differs from M. lancip , M. montana , M. parallela , M. baluensis , M. edwardinae , M. kobayashii , M. ligayae , M. nasuta , and M. kalimantanensis (vs. present in the latter).

By lacking rostral appendage, Megophrys cf. pachyproctus differs from M. stejnegeri (vs. having less rostral appendage in the latter).

By lacking a distinct horn-like tubercle at edge of upper eyelid, Megophrys cf. pachyproctus differs from M. dringi (vs. present in the latter).

By vomerine teeth present, Megophrys cf. pachyproctus differ from M. vegrandis , M. baolongensis , M. binchuanensis , M. binlingensis , M. boettgeri , M. brachykolos , M. cheni , M. kuatunensis , M. lini , M. lishuiensis , M. minor , M. obesa , M. palpebralespinosa , M. sangzhiensis , M. shuichengensis , M. spinata , M. tuberogranulata , M. wuliangshanensis , M. wushanensis , M. ombrophila , M. leishanensis , M. wugongensis , M. mufumontana , M. feii , M. auralensis , and M. huangshanensis , M. angka , M. shunhuangensis , M. jiangi , and M. xianjuensis (vs. absent in the latter).

By relatively finger lengths I <II <IV <III and nuptial pads present only on finger I, Megophrys cf. pachyproctus differs from M. nanlingensis (vs. relatively finger lengths II <I <IV <III, nuptial pads and nuptial spines invisible in males during breeding season in the latter).

By toes with rudimentary webbing, Megophrys cf. pachyproctus differs from M. serchhipii (vs. at least one fourth webbed in the latter).

By toes with narrow lateral fringes, Megophrys cf. pachyproctus differs from M. binchuanensis , M. cheni , M. jingdongensis , M. lini , M. rubrimera , M. shuichengensis , M. spinata , M. feii , M. vegrandis , and M. glandulosa (vs. wide in the latter).

By dorsal skin rough but without spines, Megophrys cf. pachyproctus differs from the following species: M. vegrandis (vs. smooth); M. medogensis (vs. smooth with small granules); M. daweimontis (vs. smooth); M. fansipanensis (vs. smooth with small granules); M. oropedion (vs. smooth with small granules); M. parva (vs. smooth); M. zhangi (vs. smooth); and M. jiulianensis (vs. dorsal skin rough with spines).

By snout rounded in dorsal view and nuptial pad only present only on finger I, Megophrys cf. pachyproctus differs from M. dongguanensis (vs. snout pointed, nuptial pads present on the first two fingers in the latter).

Megophrys cf. pachyproctus further differs from M. medogensis by the following characters: nuptial pads only present on finger I in males (vs. on the first two fingers in the latter); dorsal skin rough (vs. relatively smooth in the latter); vomerine ridge moderate, vomerine teeth weak (vs. both strong in the latter).

By having following characters of skull, Megophrys cf. pachyproctus differs from M. medogensis : skull weakly ossified, opening of anterior fontanelle present, sagittal suture distinctly open (vs. skull well ossified, opening of anterior fontanelle and sagittal suture occlusive in the latter); frontoparietal front equals rear (vs. distinctly wider in the latter); sphenethmoid rough with curves and pits, middle front edge protruding (vs. relatively smooth with few pits, truncate in the latter); exoccipitals posterior to the line connecting conjunctions of quadratojugal and mandible (vs. anterior in the latter); and columella auris short (vs. long in the latter).

By having following characters of bioacoustics, Megophrys cf. pachyproctus differs from M. medogensis (Tables 3 , Suppl. material 1: Table S5): call duration significantly much longer (491-889 ms vs. 121-241 ms; P <0.001); dominant frequency significantly higher (3.2-3.3kHz vs. 2.3-3.0 kHz; P <0.01); and call intervals significantly longer (493-720 ms vs. 153-254 ms; P <0.001).

Megophrys cf. pachyproctus very resemble M. pachyproctus on morphology, but differs from the latter in the following characters: protuberance beyond cloaca small, barely visible from ventral view, not swollen (vs. protuberance present on vent beyond cloaca large, swollen, arc-shaped, can be seen on both dorsal and lateral view in the latter); inner metatarsal tubercle distinct partially fused with toe I (vs. inner metatarsal tubercle separate from base of toe I at a distance nearly twice its diameter in the latter). Megophrys cf. pachyproctus further differs from M. pachyproctus by having the following characters on skull morphology: premaxillary and maxillary teeth weak, separated from others by gaps (vs. strong, closely positioned with others in the latter); inner edge of nasal bones half contact with sphenethmoid (vs. mostly in the latter); sphenethmoid rough with curves and pits, middle front edge protruding (vs. relatively smooth with few pits, truncate in the latter); and conjunction of parasphenoid anterior process meet with sphenethmoid narrow, width ca. half the constriction near its base (vs. moderate, ca. three quarters in the latter).

Distribution and natural history.

This group is currently known at elevation from 1560 m to 2003 m in Medog County, Tibet Autonomous Region, China. It inhabits mountain streams of subtropical forests. During June, males call on branches and leaves of bushes near mountain stream with a distance at least three meters from others, where covered with dense broad leaf forests (Figs 10C, D, H, I , Suppl. material 2: Fig. S5B, S5F). Females collected during October were gravid with well-developed eggs, and also found on leaves of floor vegetation like Elatostema species and ferns near small mountain streams. Distribution elevation overlap with M. medogensis at 1560 m, where a small stream pond was found to have tadpoles of three Megophrys species on 18 June, including M. medogensis (at stage 42), Megophrys cf. pachyproctus (at stages 26-27), and Megophrys yeae sp. nov. (at stages 28-35). Theloderma sp. and Amolops medogensis Li and Rao, 2005 were recorded at the same habitat.

Figures

Figure 3. Photos of specimens of Megophrys species in Medog. A-E dorsal views of adult male holotype NWIPB 770650 of M. pachyproctus, adult male topotype CIB 022017061406 of M. medogensis, adult male CIB 022017061805 of M. cf. pachyproctus, adult male holotype CIBMT 171053 of Megophrys zhoui sp. nov., and adult male holotype CIB 201706 MT 02 of Megophrys yeae sp. nov., respectively F-J ventral views of the specimens, respectively K-O lateral view of head of the specimens, respectively P-T ventral view of hand of the specimens, respectively U-Y ventral view of foot of the specimens, respectively. Scale bar for body view equal to 10 mm, and for partial view 5 mm.

Figure 4. Visualization of advertisement calls of three Megophrys species from Medog. A-C visualizations of 60 seconds waveform of relative amplitude over time for M. medogensis (one unvouchered individual recorded in the vicinity of Medog urban area), M. cf. pachyproctus (CIB 022017061807), and Megophrys yeae sp. nov. (paratype CIB 022017061804), respectively D-F visualizations of 20 seconds waveform of relative amplitude over time G-I visualizations of two seconds waveform of relative amplitude for the species, respectively J-L visualizations of two seconds waveform of spectrogram for the species, respectively.

Figure 5. Skull of Megophrys species in Medog. A-E dorsal views of adult male holotype NWIPB 770650 of M. pachyproctus, adult male topotype CIB 022017061406 of M. medogensis, adult male CIB 022017061805 of M. cf. pachyproctus, adult male holotype CIBMT 171053 of Megophrys zhoui sp. nov., and adult male holotype CIB 201706 MT 02 of Megophrys yeae sp. nov., respectively F-J ventral views of the specimens, respectively. Key to skull: 1 premaxillary; 2 maxillary; 3 nasal; 4 sphenethmoid; 5 anterior fontanelle; 6 frontoparietal; 7 sagittal suture; 8 pterygoid; 9 squamosal; 10 quadratojugal; 11 prootic; 12 exoccipital; 13 vomerine ridge; 14 mandible; 15 anterior process of parasphenoid; 16 columella auris. Scale bar equal to 5 mm.

Figure 6. Tadpole specimens of four groups of three Megophrys species from Medog. A-D dorsal views of the low-middle-elevation tadpole CIBMT 20170621 of M. medogensis (Goser stage 35), the high-elevation tadpole CIBMT 171001 of M. medogensis (stage 27), tadpole CIBMT 20170611 of M. cf. pachyproctus (stage 25), tadpole CIBMT 170604 of Megophrys yeae sp. nov. (stage 35), respectively E-H lateral views of the tadpoles, respectively I - L ventral views of the tadpoles, respectively. M-P dorsal views of head of the tadpoles, respectively. Scale bar for body view equal to 10 mm, and for head view 2 mm.

Figure 7. The adult male CIB 022017061805 of M. cf. pachyproctus in life. A dorsolateral view of body B ventral view of body C dorsolateral view of head D ventral view of hand E ventral view of foot.

Figure 10. Microhabitats of Megophrys toads in the field in Medog. A stream at elevation 850 m in Didong village, harboring the low-middle-elevation M. medogensis and Megophrys yeae sp. nov. B a stream at 1530 m in Gelin village, hosting the low-middle-elevation M. medogensis and M. pachyproctus C a stream at 1780 m in Bari village, harboring low-middle-elevation M. medogensis, M. cf. pachyproctus and Megophrys yeae sp. nov. D a stream at 2003 m in the vicinity of Renqingbeng Temple, hosting M. cf. pachyproctus and Megophrys zhoui sp. nov. E a stream at 2142 m in Gedang village, hosting M. medogensis F one adult male of low-middle-elevation M. medogensis calling on a dead leaf on the tropical forest ground nearby a stream in Didong village G the adult male paratype CIB 022017061102 of Megophrys yeae sp. nov. calling on a leaf of dense bushes under tropical forest, ca. 0.5 m above a stream in Didong village H the adult male CIB 022017061806 of M. cf. pachyproctus calling on a branch of dead bush, ca. 0.5 m above ground under subtropical forest in Bari village I the gravid female CIBMT 171054 of M. cf. pachyproctus precariously climbing up onto a stem of herb, ca. 0.3 m above a tiny stream under subtropical forest in Renqingbeng J the adult male holotype CIBMT 171053 of Megophrys zhoui sp. nov. sitting on a split of a fern leaf in a small stream under subtropical forest in the vicinity of Renqingbeng Temple.