Mannophryne molinai, Rojas-Runjaic & Matta-Pereira & Marca, 2018

Rojas-Runjaic, Fernando J. M., Matta-Pereira, Miguel E. & Marca, Enrique La, 2018, Unveiling species diversity in collared frogs through morphological and bioacoustic evidence: a new Mannophryne (Amphibia, Aromobatidae) from Sierra de Aroa, northwestern Venezuela, and an amended definition and call description of M. herminae (Boettger, 1893), Zootaxa 4461 (4), pp. 451-476 : 454-467

Mannophryne molinai sp. nov.

( Figs. 1–2 , 4–5 )

Suggested common name in English: Sierra de Aroa Collared Frog

Suggested common name in Spanish: sapito acollarado de la Sierra de Aroa

Holotype. Adult male, MHNLS 21355 (field number FR 588; Figs. 1–2 ), from Quebrada La Rondona, Sierra de Aroa, Sucre municipality, Yaracuy state, Venezuela (10o19’20.8”N, 68o52’24.0”W; 1180 m asl; Fig. 3 ), collected on April 0 5, 2014, by F.J.M. Rojas-Runjaic, E. Camargo, and J.L. Vieira.

Paratypes. Nine specimens (six adult males and three adult females) all collected at the type locality: three males ( MHNLS 21536–21537, 21540; field numbers MEM 4, 7, 2, respectively) and two females ( MHNLS 21535; field number MEM 6, and ULABG 7821 [field number MEM 11]), collected on December 19, 2012, by M. Matta- Pereira and J. Piñero; three males ( MCP 13924 [ex-MHNLS 21336; Fig. 4c–d ], MHNLS 21338–21339; field numbers FR 569, 571–572) and one female ( MHNLS 21337; field number FR 570; Fig. 4a–b ), collected on April 04–05, 2014, by F.J.M. Rojas-Runjaic, E. Camargo, and J.L. Vieira.

Referred specimens. Four juveniles, and two lots of tadpoles, all collected at the type locality: one juvenile ( MHNLS 21356; field number FR 589) collected on April 0 5, 2014, by F.J.M. Rojas-Runjaic, E. Camargo and J.L. Vieira; two juveniles ( MHNLS 21543–21544; field numbers MEM 3 and 5, respectively) collected on December 12, 2012, and one juvenile ( MHNLS 21542; field number MEM 8) collected on February 27, 2014, by M. Matta- Pereira and J. Piñero; two lots of tadpoles ( MHNLS 21546–21547; field numbers MEM 10 and 12; collected from the backs of the males MHNLS 21536 and 21537 respectively) collected on December 19, 2012, by M. Matta- Pereira and J. Piñero.

Definition. The new species is defined by the unique combination of the following characters: (1) Small body size, with adult males smaller than females (SVL = 20.5–23.4 mm in males vs. 25.2–25.5 mm in females); (2) dorsal skin of body and hind limbs shagreen, moderately granular on flanks; small tubercles present on posterior third of dorsum, body flanks, and dorsal surfaces of thighs and shanks; ventral skin smooth; (3) snout rounded in dorsal view, protruding in profile; (4) nares visible ventrally; (5) tympanum small (~1/2 of ED), defined, about 1/3 concealed posterodorsally by a low supratympanic fold; tympanic annulus present below skin; tympanic membrane not differentiated; (6) short teeth present on maxillary arch; (7) median lingual process absent; (8) vocal sac in males single, subgular; (9) carpal pad absent; (10) metacarpal ridge low; (11) thenar tubercle conspicuous; (12) nuptial excrescences on thumb absent; (13) FIII not swollen; (14) tip of FIV surpassing distal subarticular tubercle of FIII; (15) FI and FII equal in size; (16) thin lateral fringes present on preaxial side of FII– FIII; (17) low and poorly defined lateral keels on pre- and postaxial sides of FI and FIV, and postaxial side of FII– FIII; (18) tarsal keel well-defined in all its extension, nearly straight, extending from the base of TI, where is continuous with the preaxial fringe, to the mid-tarsus, not merged with the inner metatarsal tubercle nor reduced at the level of this tubercle; (19) tarsal fringe absent; (20) middle metatarsal tubercle present, larger than inner one, non-protuberant, weakly defined; (21) metatarsal fold present, strongly developed distally; (22) wide lateral (pre- and postaxial) fringes in all toes; (23) toes basally webbed, webbing formula: I (1½–2–)–(2½–2¾) II (1¾–2–)–(3+–3⅓) III (2½–3+)– (4– –4+) IV (4– –4+)–(2½–3–) V; (24) discs weakly to moderately expanded on FI–FIV; moderately expanded on TI– TIV, and weakly to moderately expanded on TV; (25) paired dorsal digital scutes present on fingers and toes; (26) cloacal sheath short and slender; (27) supracloacal dermal flap present, conspicuous; (28) cloacal tubercles present; (29) iridescent golden to cream spot at dorsal forelimb and hind limb insertions present, diffuse; (30) pale paracloacal mark present, diffuse; (31) diffuse yellowish spots on hidden parts of hind limbs absent; (32) thigh dorsally pale brown with four to five transverse dark brown bands; (33) pale dorsolateral stripe diffuse, straight, reaching the level of the arm insertion or slightly surpassing midbody; (34) lateral dark band solid or formed by anastomosed spots, wider at the groin level; (35) oblique lateral stripe partial (not reaching the posterior border of the eye), solid, white or subtly tinged with yellow at the groin; (36) ventrolateral stripe white, cream or yellowish, poorly defined, formed by a wavy series of solid white spots; (37) dark dermal collar narrow, diffuse to solid, and complete in males; narrow (7.5–9.1% of SVL), reticulated, and complete in females; (38) dark lower labial stripe present, diffuse; (39) throat color in life: extensively colored with yellow in females, gray in males; (40) abdomen color white or spotted with yellow, and free or almost free of melanophores in females, dirty white in males; (41) iris golden, finely reticulated with black, with a dark copper horizontal band, pupil ring golden, complete; (42) tongue mustard yellow; (43) large intestine unpigmented; (44) adult testis unpigmented; (45) mature oocytes with the animal pole pigmented with dark brown; (46) skin blackening in males during call activity; (47) mercaptan-like odor present; (48) diurnal activity; (49) tadpole transport by males; (50) riparian habitat; (51) advertisement call composed of long trills of single tonal notes; (52) peak frequency of calls: 3.60–4.26 (3.96 ± 0.19) kHz; (53) fundamental frequency: 1.74–1.91 (1.87 ± 0.04) kHz; (54) rate of note emission: 2.08–3.36 notes/s (2.76 ± 0.52); (55) note duration: 0.04–0.13 (0.08 ± 0.03) s; (56) duration of silent intervals between notes: 0.14–0.57 (0.31 ± 0.10) s.

Diagnosis. Based on the geographic distribution, we only compare Mannophryne molinai with the species of the M. collaris species Group (sensu Manzanilla et al. 2007; Grant et al. 2017): M. caquetio Mijares-Urrutia & Arends, 1999 , M. collaris (Boulenger, 1912) , M. cordilleriana La Marca, 1994 , M. herminae ( Boettger, 1893) , M. lamarcai Mijares-Urrutia & Arends, 1999 , M. larandina ( Yústiz, 1991) , M. orellana Barrio-Amorós, Santos & Molina, 2010 , M. urticans Barrio-Amorós, Santos & Molina, 2010 , and M. yustizi ( La Marca, 1989) . We also include in the diagnosis M. trujillensis Vargas & La Marca, 2007, and M. speeri La Marca, 2009 (not assigned to any species group) due to their geographic distribution (both from the Venezuelan Andes) and phenotypic affinities with this species group. Character states of M. molinai are presented in parentheses throughout the diagnosis.

Mannophryne caquetio is only known from Sierra de Churuguara in the Sistema Coriano (or Falcón-Lara mountain system; Vivas 2012), northwesternmost portion of the Cordillera de la Costa. Its tympanum diameter is ~1/3 of ED (~1/2 of ED); the disc on FIII is moderately expanded, being 2.5–2.8 times wider than adjacent phalanx (1.9–2.4 times wider); a slightly less extensive toe webbing is present between preaxial side of TIV and preaxial side of TV: (4–4½) IV (4+–4½)– 3– V (basally webbed, [4– –4+] IV [4– –4+]– [2½–3–] V); its metatarsal fold is strong and almost reaching the outer metatarsal tubercle (also strong, but only extending on the distal third or distal half of the metatarsus); lacks dark lower labial stripe (present, diffuse); and the pupil ring lacks peripheral lobes (with a ventral peripheral lobe).

Mannophryne collaris is restricted to the valley of the Chama river in the western versant of the Cordillera de Mérida in the Venezuelan Andes. Its adult size is larger and ranges between 24–26 mm SVL in males and 27–33 mm SVL in females (males: 20.5–23.4 mm; females: 25.2–25.5 mm SVL); it has more extensive toe webbing between postaxial side of TII and postaxial side of TIV: II (1–1½)–(2½–3) III 2 –(3–3½) IV (3–4) (basally webbed, II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]); it lacks dark lower labial stripe (present, diffuse); abdomen is light gray in adult males, profusely stippled with melanophores when seen under magnification (ivory white, less stippled); only the posterior two-thirds of throat on adult females are yellow in life, and pale free or almost free of melanophores in preservative (throat extensively yellow colored in life and free or almost free of melanophores in preservative); pupil ring lacks peripheral lobes (with a ventral peripheral lobe); the rate of note emission of calls is higher and ranges from 8–9 notes/s (2–3 notes/s); the duration of silent interval between notes is 0.06– 0.08 s (0.14– 0.57 s); and the peak frequency of calls is 3.55 kHz (3.60–4.26 kHz).

Mannophryne cordilleriana is restricted to the basins of the Santo Domingo and Calderas rivers in the eastern versant of the Cordillera de Mérida in the Venezuelan Andes. Body size in females is larger and ranges between 30–35 mm SVL (25.2–25.5 mm SVL); it has weakly expanded discs on TI–TII, being TI: 1.7–2.0, and TII: 1.8–2.4 times wider than adjacent phalanx (moderately expanded; TI: 2.0–2.3, TII: 2.5–2.7 times wider); more extensive toe webbing between postaxial side of TII and postaxial side of TIV: II (1–1½)–(2½–3) III(2–2½)– (3–3½) IV (3½– 4) (basally webbed, II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]); only the posterior two-thirds of throat in adult females are yellow in life, and pale, free or almost free of melanophores in preservative (all throat yellow in life, and free or almost free of melanophores in preservative); abdomen may be evenly or irregularly stippled with melanophores in adult males, and irregularly stippled in adult females (evenly stippled in males, and free or almost free of melanophores in adult females); pupil ring without peripheral lobes (with a ventral peripheral lobe).

Mannophryne herminae is known from the central portion of the northern slope of Cordillera de la Costa. It is very similar to M. molinai in body size, general color pattern and toe webbing, but can be easily distinguished by its markedly different advertisement call, which is composed by notes arranged in duplets emitted in long trills (trills of single notes, not arranged in duplets); its rate of note emission is higher, with 10–11 notes/s (2–3 notes/s), and up to 546 notes per trill (up to 89 notes per trill); the notes are shorter, ranging between 0.02– 0.04 s (note duration: 0.04– 0.13 s), and are less spaced, being 0.02– 0.04 s the range of duration of the silent intervals between notes of each duplet, and 0.09– 0.14 s between duplets (silent intervals between notes: 0.14–0.57); spectrally, its call differs only in the fundamental frequency, which ranges between 1.98–2.15 kHz (1.74–1.92 kHz). Additionally, its metatarsal fold is strong and almost reaching the outer metatarsal tubercle (also strong, but only extending from the base of TV to the distal third or distal half of the metatarsus); dark dermal collar is solid or with some small white spots in females (reticulated); the width of the collar in females ranges between 10.9–15.9% of SVL (7.5–9.1% of SVL); pupil ring lacks peripheral lobes (with a ventral peripheral lobe).

Mannophryne lamarcai is restricted to the Serranía de Ziruma, between the northern limit of the Venezuelan Andes and the western limit of Cordillera de La Costa. Its snout is nearly truncate in dorsal view (rounded); it has more extensive toe webbing on preaxial side of TII, ranging between 2–2½ (toe webbing formula on preaxial side of TII is 2½–2¾), and also between postaxial side of TIII and preaxial side of TIV: III (2–2½)–(3½–4–) IV (webbing less extensive between TIII–TIV: III [2½–3+]–[4– –4+] IV); its metatarsal fold is strong and almost reaching the outer metatarsal tubercle (also strong, but only extending on the distal third or distal half of the metatarsus); dorsolateral stripe is solid or diffuse (always diffuse) and extensive, reaching midbody or up to the level of the groin (reaching the level of the arm insertion or the midbody); only the posterior half to posterior two-thirds of throat in adult females are yellow colored in life, and pale free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative); the dark dermal collar is solid in adult females (reticulated); pupil ring lacks peripheral lobes (with a ventral peripheral lobe).

Mannophryne larandina is known from Sierra de Barbacoas, northeastern limit of the Cordillera de Mérida in the Venezuelan Andes. Adult females of this species are larger, reaching up to 31.0 mm of SVL (up to 25.5 mm of SVL); the nares are laterodorsally oriented and barely visible in dorsal view (lateroventrally oriented and only visible in ventral view); the basal subarticular tubercles of toes are elongated (rounded to slightly elliptical); it has more extensive toe webbing: I (0+–1–)–(2– –2+) II (1– –1+)–(2¾–3–) III (2– –2+)–(3⅓–3½) IV (3¾–4–)–(2– –2+) V (basally webbed; I [1½–2–]–[2½–2¾] II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]–[2½–3–] V); the posterior half of throat in adult females is yellow in life, and pale, free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative); dark dermal collar in adult males is diffuse and speckled with white (diffuse or solid but without white spots); abdomen in adult males is pale gray with discrete white spots (dirty ivory); pupil ring without peripheral lobes (with a ventral peripheral lobe).

Mannophryne orellana is restricted to the southern part of the eastern versant of the Cordillera de Mérida in the Venezuelan Andes. This is a larger species with adult males and females ranging between 25.4–27.3 mm, and 29.5– 32.9 mm of SVL, respectively (males: 20.5–23.4 mm SVL; females: 25.2–25.5 mm SVL); basal subarticular tubercles of toes are elongated (rounded to slightly elliptical); has a much more extensive toe webbing: I (0+–1–)– (2–2+) II (1+–1⅓)–(2¾–3–) III (1¾–2)–(2¾–3+) IV (3+–3¾)–(2– –2+) V (basally webbed; I [1½–2–]–[2½–2¾] II [1¾– 2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]–[2½–3–] V); lacks pale dorsolateral and ventrolateral stripes (both present); the dark dermal collar in females is narrow (wide), solid and without white spots (reticulated); posterior half of throat in adult females is yellow in life, and pale free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative). The calls of Mannophryne orellana are trills of pulsed notes (trills of tonal notes), emitted at a rate of 10–13 notes/s (2–3 notes/s); the note duration ranges between 0.03– 0.04 s (0.04– 0.13 s), and the silent interval between notes is 0.04– 0.05 s (0.14– 0.57 s); its peak frequency is about 3.42 kHz (3.60–4.26 kHz).

Mannophryne speeri is known from Sierra de Portuguesa, at the northern part of the eastern versant of the Cordillera de Mérida, in the Venezuelan Andes. Adult females of this species are smaller, ranging between 23.0– 24.1 mm of SVL (females: 25.2–25.5 mm SVL); the discs on FI–FII are weakly expanded, being respectively 1.6– 1.9, and 1.7–1.9 times wider than their adjacent phalanges (1.8–2.1, and 1.8–2.3 times wider); it has slightly more extensive toe webbing: I (1+–1½)–(2+–2⅓) II (1½–1¾)–(3– –3+) III (2½–3–)–(3¾–4–) IV (4– –4+)–(2⅓–2½) V (basally webbed; I [1½–2–]–[2½–2¾] II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]–[2½–3–] V); nares are laterodorsally oriented and barely visible in dorsal view (lateroventrally oriented and only visible in ventral view); only the posterior half of throat in adult females is yellow in life, and pale free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative); pupil ring lacks peripheral lobes (with a ventral peripheral lobe).

Mannophryne trujillensis is endemic from the valley of the Castán river, in the eastern versant of the Cordillera de Mérida in the Venezuelan Andes. The adult females of this species are larger, reaching up to 27.5 mm of SVL (up to 25.5 mm of SVL); it has more extensive toe webbing: I (1+–1½)–(2–2⅓) II (1+–1½)–(2¾–3+) III (2+–2½)–(3½ –3¾) IV (4– –4+)–(2+–2¾) V (basally webbed; I [1½–2–]–[2½–2¾] II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]– [2½–3–] V); its metatarsal fold is strong and almost reaching the outer metatarsal tubercle (also strong, but only extending on the distal third or distal half of the metatarsus); only the posterior two-thirds of throat in adult females are yellow in life, and pale free or almost free of melanophores in preservative (all throat yellow in life and free or almost free of melanophores in preservative); dark dermal collar is finely speckled with small white spots in adult females (reticulated); the abdomen typically is evenly stippled with melanophores in adult females (free or almost free of melanophores in adult females); pupil ring lacks peripheral lobes (with a ventral peripheral lobe).

Mannophryne urticans is restricted to the western piedmont of Cordillera de Mérida in the Venezuelan Andes. This is a larger species with adult males and females ranging between 23.8–27.5 mm, and 25.9–30.8 mm of SVL, respectively (males: 20.5–23.4 mm SVL; females: 25.2–25.5 mm SVL); has a slightly more extensive toe webbing: I (1+–1–)–(2–2¼) II (1+–1⅓)–(2¾–3–) III (2– –2¼)–(3⅓–3½) IV (3¾–4+)–(2– –2+) V (basally webbed; I [1½–2–]–[2½– 2¾] II [1¾–2–]–[3+–3⅓] III [2½–3+]–[4– –4+] IV [4– –4+]–[2½–3–] V); lacks pale dorsolateral and ventrolateral stripes (both present); dark dermal collar in females is narrower, ranging between 4.7–6.6% of SVL (wider, 7.5–9.1% of SVL), solid (reticulated) and medially broken or almost broken (always complete); only the posterior two-thirds of throat of adult females are yellow in life, and pale free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative). The calls of Mannophryne urticans are trills of pulsed notes (trills of tonal notes), emitted at a rate of 5–6 notes/s (2–3 notes/s); the notes have a duration of 0.02 s (0.04– 0.13 s), and the silent interval between notes is 0.07– 0.08 s (0.14– 0.57 s); its peak frequency is about 3.56 kHz (3.60–4.26 kHz).

Finally, Mannophryne yustizi is known only from Sierra de Portuguesa, in the northernmost portion of the eastern versant of the Cordillera de Mérida in the Venezuelan Andes. Adult females of this species are larger, reaching 26.8–30.6 mm of SVL (25.2–25.5 mm of SVL); the basal subarticular tubercles of toes are elongated (rounded to slightly elliptical); has a slightly more extensive toe webbing between preaxial sides of TI and TIII: I (1+–1½)–(2+–2⅓) II (1⅓–1¾)–(3– –3+) III (basally webbed; I [1½–2–]–[2½–2¾] II [1¾–2–]–[3+–3⅓] III); the dorsolateral stripe is solid to diffuse (always diffuse) and more extensive, reaching the midbody or up to the level of the groin (reaching the level of the arm insertion or up to the midbody); only the posterior half of throat in adult females is yellow in life, and pale free or almost free of melanophores in preservative (all the throat yellow in life and free or almost free of melanophores in preservative); dark dermal collar in females is wider, ranging between 9.0–13.5% SVL (narrower, 7.5–9.1% SVL); in males the dark dermal collar is diffuse, speckled with small white spots to reticulated, and complete or medially broken (diffuse to solid, without white spots, and complete); the abdomen in males is pale gray, densely stippled with melanophores evenly distributed or clumped (dirty ivory, less stippled, non-clumped melanophores), and occasionally speckled with small white dots (without small white dots).

Description of the holotype. An adult male ( Figs. 1–2 ) of 21.2 mm SVL. Body robust, short and slightly wider than head ( Fig. 1a ). Head as long as wide (HeL: 37.3% of SVL; HW: 37.7% of SVL; HeL/HW: 1.0). Snout short, rounded in dorsal view ( Fig. 2a ), protruding in profile ( Fig. 2c ). Eye-naris distance shorter than eye diameter (EN/ED: 0.6). Nares small, elliptical, lateroventrally oriented, situated laterally to the tip of the snout, visible from the front and barely visible ventrally, not visible dorsally; nares with a thin dermal flap on the posterior half which is posterodorsally lobulated. Canthus rostralis distinct, almost straight in dorsal view, slightly rounded in cross section; loreal region flat, vertical. Interorbital region wider than upper eyelid; interorbital distance slightly shorter than internarial distance (IoD/InD: 0.8). Eye prominent (ED: 13.2% of SVL). Tympanum small (DT/ED: 0.5), defined; tympanic annulus present concealed below skin but forming a weak relief in it; tympanic membrane not differentiated; about 1/3 of the tympanum concealed posterodorsally by a low supratympanic fold formed by superficial slip of musculus depressor mandibulae; tympanum posteroventral to the eye, almost touching the angle of jaws ( Fig. 2c ). Short teeth present on maxillary arch, concealed by inner surface of upper lip. Choanae small, rounded, anterolaterally positioned on the roof of the mouth, anterior to eye bulge. Tongue cordiform, 1/3 free posteriorly, without median lingual process.

Forelimb ( Fig. 2d ) slender, with three small ulnar tubercles longitudinally aligned on the ventroexternal surface of the forearm. Hand length 29.7% of SVL. Carpal pad absent. Palmar tubercle large, swollen, welldefined, rounded. Thenar tubercle elliptical (about two times longer than wide), small (larger diameter about 2/3 of palmar tubercle diameter), swelling, and evident in both palmar view and profile. One slightly elliptical subarticular tubercle each on FI and FII, similar in size to thenar tubercle, and two small, circular tubercles each on FIII and FIV; all subarticular tubercles conspicuous and swollen. Palmar supernumerary tubercles absent. Metacarpal ridge present, low. Nuptial excrescences on thumb absent. FIII not swollen. Relative length of adpressed fingers: III>IV>II>I; tip of FIV surpassing distal subarticular tubercle of FIII when fingers are juxtaposed. FI and FII equal in size. Thin lateral fringes present on preaxial side of FII–FIII, weak and poorly defined lateral keels on pre- and postaxial sides of FI and FIV, and on postaxial side of FII–FIII. Finger discs present, moderately expanded; width of discs corresponding (from FI to FIV, on both hands) to 2.0–2.1, 2.2–2.3, 2.2–2.4 and 2.0–2.2 times the width of their respective adjacent phalanges. Disc width of FIII 1/2 of tympanum diameter (F3D/TD: 0.5). Tip of discs slightly rounded to nearly truncated; disc pad transversely elliptical. Paired dorsal digital scutes conspicuous and protuberant in all fingers.

Hind limbs ( Fig. 2e ) robust; thigh, shank and foot similar in size (ThL: 48.1% SVL; SL: 49.5% SVL; FL: 49.1% SVL). Tarsal keel well-defined in all its extension, nearly straight, its proximal end reaching the mid-tarsus; distally extends along the preaxial side of inner metatarsal tubercle (without merging with it nor reduced to this level) to reach the base of TI, were it merges with the preaxial fringe of this toe. Tarsal fringe absent. Inner metatarsal tubercle large, slightly swollen, well-defined, elliptical, 1.7–2.0 times longer than wide. Outer metatarsal tubercle, rounded, swollen, smaller than inner metatarsal tubercle (about 1/2 of its size). A large middle metatarsal tubercle is present between the inner and outer ones; slightly greater than inner metatarsal tubercle, elliptical, flat, weakly defined, its distal border reaching the level of proximal borders of the other two metatarsal tubercles. Metatarsal fold present, strong at the base of TV but weak at its proximal portion; distally, this fold is continuous with the postaxial fringe of TV. Plantar supernumerary tubercles absent. Toes slender, all with wide lateral (pre- and postaxial) fringes and basally webbed; webbing formula: I 1 ½–2½ II 1 ¾–3+ III (2½–2¾)–4– IV 4 +– 2½ V. Subarticular tubercles small (about 1/2–1/3 size of the inner metatarsal tubercle), rounded to near elliptical (longitudinally) and swollen; one on TI–TII, two on TIII and TV, three on TIV. Relative lengths of adpressed toes: IV>III>V>II>I; tip of TIII reaching the mid-level between distal and median subarticular tubercles of TIV; tip of TV reaching the distal half of the median subarticular tubercle of TIV. Toe discs present, moderately expanded on TI–TIV, weakly expanded on TV; width of discs corresponding (from TI to TV, on both feet) to 2.0–2.3, 2.5–2.7, 2.2–2.5, 2.2–2.4 and 1.7 times the width of their respective adjacent phalanges. Disc width of TIV about 1/2 of tympanum diameter (T4D/TD: 0.6). Tip of discs slightly rounded to nearly truncated; disc pad transversely elliptical. Paired dorsal digital scutes conspicuous and slightly protuberant in all toes.

Dorsal skin of body and hind limbs shagreen; moderately granular on upper eyelids and body flanks, smooth on forelimbs; with scattered small tubercles on the posterior third of dorsum, body flanks, and dorsal surfaces of thighs and shanks; head flank with one to two large and horizontally enlongated postcommisural tubercles ( Fig. 2c ). Ventral skin smooth on throat, chest, belly, forelimbs, and thighs. Several large tubercles are present at the base of the retrolateral surface of thighs, flanking the cloaca. Dermal flap above cloaca present, conspicuous ( Figs. 1a, c ). Cloacal sheath short and slender; cloacal opening ventrally oriented, above midlevel of thighs.

Measurements of the holotype (in mm). SVL: 26.7; SL: 14.0; ThL: 14.2; FL: 13.0; HaL: 7.4; HeL: 9.5; HW: 9.4; IoD: 3.3.; InD: 3.6; EN: 2.3; ED: 3.7; TD: 1.7; ETS: 4.1; F3D: 0.7; T4D: 0.9; F1L: 5.0: F2L: 5.2.

Color in life of the holotype (based on field notes and photos). Dorsal background color grayish brown, with abundant small dark brown dots and some scattered irregular pale greenish gray spots; these pale spots are iridescent when seen under magnification. Pale dorsolateral stripe diffuse, ill-defined, straight, extending dorsolaterally from external edge of upper eyelid to the mid-level of dorsum.

Sides of body with a well-defined blackish brown lateral band, finely stippled with greenish gray dots; lateral band extending from tip of snout to upper level of groin, covering the naris, and the two superior thirds of the eye and tympanum; the upper border of this band is almost straight and in contact with the dorsolateral pale stripe; posterior to the tympanum its lower border becomes broader and irregular, reaching the upper insertion of the arm and continues to the groin delimited ventrally by the ventrolateral stripe. Oblique lateral stripe (OLS) solid white in almost all its extension, subtly tinged with yellow at the groin, anteriorly broken in small spots, reaching mid-way between groin and eye (about the level of the forearm). The trace of OLS is coincident with a series of small nonkeratinized tubercles. Ventrolateral stripe (VLS) formed by a wavy series of solid white spots; with those close to the groin subtly tinged of yellow; VLS extending from the postcommisural area to the mid-level of the groin. Upper lip variegated with small cream and blackish brown spots.

Background color of throat cream translucent, dense and evenly stippled with melanophores; dark lower labial stripe present; dark dermal collar narrow, diffuse, with small scattered whitish dots (inconspicuous to eye naked but visible under magnification); its posterior border reaches the anterior level of arm insertion. Background color of the remaining ventral surfaces translucent grayish, densely stippled with melanophores on chest and decreasing in density toward posterior part of abdomen, undersurface of hind limbs. Parietal peritoneum on belly nacreous white, visible through skin. Ventral periphery of groin faintly tinged with yellow.

Dorsal surface of upper and forearm and hand pale brown, with small scattered greenish gray dots; a faint iridescent pale spot present at dorsal insertion of upper arm. A blackish brown stripe on the mid-level of both, pre- and postaxial sides of upper arm, extending from arm insertion to the articulation with the forearm. Two transverse blackish brown bands on dorsal surface of forearm; the three small ulnar tubercles longitudinally aligned on the ventroexternal surface of the forearm, white-colored. Dorsal surface of hand with one or two transverse blackish brown stripes. Fingers dorsally blackish brown, with small white spots coincident with the knuckles, more conspicuous on the distal ones of each finger. Dorsal digital scute coloration varies from almost completely white to stippled with white and blackish brown in a salt-and-pepper pattern. Palm and ventral surface of digits blackish gray, tubercles (palmar, thenar, subarticulars) and disc pads, pale gray.

Dorsal surface of hind limbs pale brown in brackground, speckled with white dots (coincident with small tubercles), and cross-banded with four to five transverse dark brown bands on thighs, three on shanks and tarsi, and two to three on the feet. A faint iridescent pale yellow spot present at dorsal insertion of thigh. Pale paracloacal marks short, diffuse, each merging with the background color of dorsal surface of thigh. A blackish brown stripe on the mid-level of both, pre- and postaxial sides of thigh, formed by a series of anastomosed irregular blotches; the preaxial stripe well-defined, extending from groin to knee, and fused with the transverse bands; the postaxial one less defined and only partially in contact with the transverse bands. Toes dorsally blackish brown, with small white spots coincident with the knuckles, more conspicuous on the distal ones of each toe. Dorsal digital scutes from almost totally white to stippled with white and blackish brown in a salt-and-pepper pattern. Ventral surface of hind limbs translucent pale gray; undersurface of thighs evenly stippled with melanophores (when seen under magnification); soles and undersurface of toes blackish brown; tubercles (metatarsals, subarticulars) and disc pads pale gray.

Iris golden, with fine black reticulation, and a wide transversal dark copper band; pupil ring not broken and with a ventral lobe, golden on inferior and superior portions, copper on anterior and posterior portions. Tongue mustard yellow.

Color of the holotype in preservative (after three years, September 2017). Dorsal background color of body dark brown with irregular pale brown spots; dorsolateral stripe faded ( Fig. 1a ). Lateral blackish band slightly paler and barely contrasting with dorsal background ( Fig. 1c ); oblique lateral and ventrolateral stripes ivory white, the latter inconspicuous, poorly differentiated from ventral coloration ( Fig. 1c ). Yellowish tones on posterior part of the oblique lateral stripe, ventrolateral portion of groin, and faint iridescent pale yellow spots at dorsal insertion of thighs and arms vanished.

Ventral background color (including ventral surface of forelimbs and hind limbs) ivory white ( Fig. 1b ); dark lower labial stripe and dark dermal collar dark brown, diffuse, formed by a profusion of melanophores (noted under magnification; Fig. 2b ); Throat, chest and anterior portion of belly densely stippled with melanophores, less dense and evenly stippled on posterior portion of belly ( Figs. 1a , 2b ).

Dorsal background color of forelimbs pale brown; the longitudinal blackish brown stripes on pre- and postaxial sides of upper arm, and transverse blackish brown bands on dorsal surface of forearm turned dark brown; ulnar tubercles and knuckles of fingers, ivory white; dorsal digital scutes of fingers grayish white; undersurface of upper arms evenly stippled with melanophores, almost free of melanophores on ventrointernal side of forearms; palms and ventral surfaces of fingers dark brown; tubercles and disc pads pale gray.

Dorsal background color of hind limbs pale brown, cream towards insertion of thigh and feet; paracloacal marks ivory white, fused with background color of thigh; cross-bands on thighs, shanks, tarsi and feet, and longitudinal pre- and postaxial stripes on thigh, dark brown; knuckles of toes ivory white; dorsal digital scutes of toes grayish white; undersurface of thighs evenly stippled with melanophores, undersurface of shanks almost free of melanophores; webbing translucent; soles and ventral surfaces of toes dark brown; tubercles and disc pads pale gray. Iris blackish brown; pupil ring not visible. Tongue creamy yellow.

Morphometric and color variation in the type series. As in all other species of the genus, Mannophryne molinai exhibits striking sexual dichromatism on the ventral surface of the body (in life), with a vivid yellow throat and a marked dark dermal collar in adult females, and grayish throat with poorly defined dark collar in adult males. Vocal slits and vocal sac are secondary sexual characters only present in males.

Sexual dimorphism is also seen in adult size, with males being smaller than females (SVL: 20.5–23.4 mm [21.6 ± 1.0; n = 7] in males vs. 25.2–25.5 mm [25.4 ± 0.2; n = 2] in females). The relative size of the tympanum varies between sexes, being larger in females (7.5–7.5% of SVL [7.5 ± 0.1; n = 2]) than in males (6.3–7.0% of SVL [6.7 ± 0.2; n = 7]). The relative size of the hands is larger in males (26.3–30.7% of SVL [28.4 ± 1.7; n = 7]) than in females (25.8–26.3% of SVL [26.0 ± 0.3; n = 2]). Hind limbs are also larger in males than in females: ThL: 48.1– 54.7% of SVL (50.6 ± 2.7; n = 7) in males vs. 44.7–46.0% of SVL (45.4 ± 0.9; n = 2) in females; SL: 49.5–53.7% of SVL (51.3 ± 1.8; n = 7) in males vs. 47.1–47.6% of SVL (47.3 ± 0.4; n = 2) in females; FL: 47.4–52.8% of SVL (49.6 ± 1.9; n = 7) in males vs. 43.3–45.1% of SVL (44.2 ± 1.3; n = 2) in females. The discs on fingers are slightly wider in males than in females (from FI–FIV, males: 2.0–2.1, 2.1–2.3, 2.1–2.4, 2.0–2.2 vs. females: 1.8, 1.8–1.9, 1.9–2.3, 1.6–1.9 x width of the adjacent phalanges).

Variation in general morphometric characters of the type series is shown in Table 1. The proportions of the head (slightly longer than wide to as wide as long) are very similar in the type series (HeL/HW: 1.0–1.1 [0.1 ± 0.0; n = 9]), and its relative size is slightly variable (HeL: 35.0–37.7% of SVL [36.3 ± 0.8; n = 9]; HW: 33.3–37.7% of SVL (35.7 ± 1.6; n = 9]). Interobital distance varies from slightly shorter to as longer as internarial distance (IoD/ InD: 0.8–1.0 [0.9 ± 0.1; n = 9]). The ratio of the tympanum diameter with respect to the eye diameter also varies slightly (TD/ED: 0.5–0.6 (0.5 ± 0.0; n = 9). The eye is prominent and its relative diameter shows similar variation in males and females (ED: 12.7–14.6% of SVL [13.8 ± 0.6; n = 9]). F3D/TD and T4D/TD ratios also show slight variation (F3D/TD: 0.4–0.5 [0.4 ± 0.0; n = 9]; T4D/TD: 0.5–0.6 [0.6 ± 0.1; n = 9]). The width of toe discs varies from weakly to moderately expanded but does not differ between sexes (from TI–TV: 2.0–2.3, 2.4–2.7, 2.2–2.8, 2.2–2.9, 1.7–2.2 x width of the adjacent phalanges). Foot webbing variation: I (1½–2–)–(2½–2¾) II (1¾–2–)–(3+– 3⅓) III (2½–3+)–(4– –4+) IV (4– –4+)–(2½–3–) V (n = 15); modal foot webbing formula: I 1 ½–2½ II 2 – –3⅓ III 2 ¾–4 IV 4 +–2¾ V (n = 15).

The dorsal color pattern of dark brown spots is very variable and differs among all specimens; in some preserved males dorsal color turns almost uniformly dark brown (MHNLS 21 339, 21536). Dorsolateral stripe varies in intensity in living specimens ( Figs. 4a, c ), but is always diffuse (almost imperceptible in most preserved specimens); also shows variation in extension, reaching the level of the arm insertion (e.g. MHNLS 21337; Fig. 4a ) or extending to midbody, well past the arm insertion (e.g. MCP 13924; Fig. 4c ). The lateral dark band varies from solid with small pale dots (e.g. MHNLS 21337; Fig. 4a ), to solid on top and formed by a profusion of irregular spots anastomosed below the oblique lateral stripe (e.g. MHNLS 21535). The dark dermal collar is well defined, complete, narrow and reticulated in females ( Fig. 5a–b ), whereas in males is less conspicuous, complete, and solid (MCP 13924 [ Fig. 4d ], MHNLS 21338–21339, 21538 [ Fig. 5d ]) or diffuse (21355, 21537–21540; Fig. 5c ). In life, the extension of the yellow coloration on the throat, chest and belly of adult females is also variable; the throat is yellow in all or almost all its extension, and some specimens have yellow coloration only on the posterior portion or the periphery of the belly, while others show most of belly and chest yellow (MHNLS 21337; Fig.4b ).

Call description. Advertisement calls of Mannophryne molinai are composed of short tonal notes arranged in trills ( Fig. 6a ). The duration of call trills among the three males recorded was 13.58 ± 12.09 (1.93–39.55) s. The rate of note emission was 2.76 ± 0.52 (2.08–3.36) notes/s ( Fig. 6c ), and each call contained 36.43 ± 26.48 (4–89) notes. Note duration was 0.08 ± 0.03 (0.04–0.13) s, and the duration of silent intervals between notes 0.31 ± 0.10 (0.14–0.57) s. Notes have a slight ascending frequency modulation ( Figs. 6b, d ). Peak frequency was 3.96 ± 0.19 (3.60–4.26) kHz; with its lower and upper frequencies of 3.71 ± 0.23 (3.26–4.05) kHz and 4.20 ± 0.14 (3.82–4.43) kHz, respectively, and a bandwidth of 0.49 ± 0.13 (0.30–0.79) kHz. The fundamental frequency was 1.87 ± 0.04 (1.74–1.92) kHz. Four additional harmonics (3rd–6th; Figs. 6b, d ) were observed above peak frequency, at 5.43– 5.99, 6.80–7.47, 8.96–9.73, and 10.51–11.65 kHz, respectively. Fundamental frequency and the other four additional harmonics were not detected due to background noise in the spectrograms of calls emitted by two of the three specimens recorded.

Habitat and natural history. Mannophryne molinai inhabits narrow rapid mountain creeks surrounded by forest ( Fig. 7 ) in Sierra de Aroa. The phytocoenoses of the type locality corresponds to Coastal cloud forest ( Huber & Alarcón 1988), which ranges in this mountain system from 1,000 to 1,940 m asl (highest elevation for the Sierra de Aroa). Other populations of Mannophryne have been reported from lower altitudinal belts of this range (Barrio- Amorós 1999) whereas none are known from higher elevations (F.J.M. Rojas-Runjaic, pers. obs.) by which, we presume that the type locality is in the higher limit of the altitudinal distribution of this species, and probably it is more common at lower belts occupied by Premontane humid and very humid forests ( Ewel et al. 1976).

The region has a seasonal climatic regime, with a dry period from October–March, and a rainy period from April–September, with a maximum rain peak in July. Annual precipitation ranges between 800–1,500 mm, and annual temperature varies from 10–26.55 °C ( Lentino & Bruni 1994).

Mannophryne molinai is a diurnal and riparian frog. Adult males, adult females and juveniles were all detected from the watercourse (above rocks) to about three meters from the edge of the water; no specimen was detected inside the forest beyond the limits of the creek. Adult males call actively during the day, either hidden in crevices near small waterfalls, under rocks and fallen trunks, or exposed above rocks or trunks, but always very close to the watercourse. Calling males found on April, 04–05, 2014 were recorded at different moments during the morning and evening (between 11:45–18:30 h) but call activity was detected almost uninterruptedly from around 9:00 h (when we arrived) until near nightfall (ca. 19:00 h). Peaks of call activity (i.e. more males calling, and individual males calling more actively) were apparently related to periods of higher solar intensity throughout the day. All males observed during call activity were uniformly black colored, but several minutes after collection they became brighter and a more complex color pattern emerged, consisting of a grayish brown background with blackish brown spots, bands, and pale stripes. During nocturnal surveys several specimens were found, apparently active on rocks and trunks, but there was no call activity.

Specimens located one to three meters away from the watercourse tended to escape when noticing our presence, executing a series of rapid jumps to take refuge under rocks, trunks or leaf litter, but when located near the edge of the creek they jumped into the water, either to stay static at the bottom (typically in pools), or to get carried away by the current and quickly reach the shore about one meter downstream.

As in other species of Mannophryne , tadpole transport is done by males. The specimens MHNLS 21536 and 21537, collected on December 19, 2012, were carrying 10 and 16 tadpoles on their backs (lots MHNLS 21546 and 21547, respectively). Tadpoles already released by the parents were found in small ponds of the creek. All the specimens collected released a mild mercaptan-like odor when handled.

Distribution. Mannophryne molinai is only known from its type locality (La Rondona), at the southeastern slope of Sierra de Aroa, in the western portion of the Cordillera de la Costa ( Fig. 3 ). Other populations known from the northeastern and western foothills of Sierra de Aroa should be evaluated in order to determine if they correspond to the new species.

Conservation status. The Sierra de Aroa has an extension of ca. 1,141 ha and is protected at its northern portion by the Yurubí national park. However, the original forests on the slopes (Premontane humid and very humid forests, and part of the cloud forest) of this mountain system were almost entirely replaced by crops, and only the highest areas still maintain intact their cloud forest (Hubber & Oliveira-Miranda 2010). Recently, the cloud forest of the Sierra de Aroa was classified as Vulnerable (Criterion A4) due that a reduction ḵ 30% of its extension is projected in the next 50 years ( Oliveira-Miranda et al. 2010). Mannophryne molinai is known only from the type locality, at a creek in the cloud forest, and is locally abundant. As commented above, it is likely that its distribution is more extensive into the Sierra de Aroa toward the lower belts occupied by relicts of premontane forest, but restricted to this mountain system. Therefore, based on its presumed restricted area of occupancy, with a plausible future threat that could drive the species to Critically Endangered or even Extinct in a short time, we propose to classify M. molinai as Vulnerable under the criterion VU D2 of the IUCN (2012).

Etymology. The specific epithet “ molinai ” is a patronymic honoring the late César Ramón Molina Rodríguez (1960–2015) ( Fig. 8 ), a prominent Venezuelan herpetologist, colleague, and friend. César made great contributions to the knowledge of the diversity and conservation of Venezuelan amphibians and reptiles, materialized in nearly a hundred scientific papers, and several conservation strategies, action plans and projects. His dedication to the training of numerous students through the teaching of herpetology in classrooms, field courses, and mentoring of theses, evidenced his passion for the amphibians and reptiles, and his commitment with the development of the study of the Venezuelan herpetofauna ( Hernández 2015). César also had particular interest by the collared frogs; his PhD thesis was about the ecology of a population of Mannophryne from the valley of Caracas in Venezuela, and he co-authored the description of M. orellana , M. urticans and M. vulcano ( Barrio-Amorós et al. 2010a) . We make a posthumous recognition to his admirable work and friendship, naming this new species in his memory. The name “ molinai ” is used as a masculine singular noun, in the genitive case.

Figures

FIGURE 1. Male holotype (MHNLS 21355) of Mannophryne molinai sp. nov. in dorsal (a), ventral (b), and lateral (c) views. Scale bar represents 10 mm. Photos: F.J.M. Rojas-Runjaic

FIGURE 2. Detailed photos of the head (a, b, c), left hand (d) and foot (e) of the holotype (MHNLS 21355) of Mannophryne molinai sp. nov. Scale bars represent 2 mm. Photos: A. Jaramillo.

FIGURE 3. Map of northern Venezuela, and Trinidad and Tobago, indicating the type localities of the 20 known species of Mannophryne: 1. M. molinai sp. nov.; 2. M. caquetio; 3. M. collaris; 4. M. cordilleriana; 5. M. herminae; 6. M. lamarcai; 7. M. larandina; 8. M. leonardoi; 9. M. neblina; 10. M. oblitterata; 11. M. olmonae; 12. M. orellana; 13. M. riveroi; 14. M. speeri; 15. M. trinitatis; 16. M. trujillensis; 17. M. urticans; 18. M. venezuelensis; 19. M. vulcano; 20. M. yustizi.

FIGURE 4. Female and male paratype specimens of Mannophryne molinai sp. nov. in life. (a) Dorsolateral and (b) ventral views of the paratype female MHNLS 21337; (c) dorsolateral and (d) ventral views of the paratype male MCP 13924 (ex- MHNLS 21336). Photos: F.J.M. Rojas-Runjaic

FIGURE 5. Ventral view of four preserved paratypes of Mannophryne molinai sp. nov. showing variation in the dark dermal collar. Paratype females MHNLS 21337 (a), and MHNLS 21535 (b); paratype males MHNLS 21537 (c), and MHNLS 21538 (d). Fotos: F.J.M. Rojas-Runjaic

FIGURE 6. Advertisement call of Mannophryne molinai sp. nov. Oscillogram (a) and spectrogram (b) of a 5 s fragment of the call. Detailed view of the oscillogram (c) and spectrogram (d) of a 1 s section of the same recording.

FIGURE 7. La Rondona creek, Sierra de Aroa, northwestern Venezuela, type locality of Mannophryne molinai sp. nov. (a) View of a small pool and (b) crevices below a waterfall were several specimens of the type series were found. Photos: F.J.M. Rojas-Runjaic.

FIGURE 8. César Ramón Molina Rodriguez (1960–2015) with an amplectant couple of the critically endangered Rancho Grande Harlequin Frog Atelopus cruciger in January 2010. We named Mannophryne molinai sp. nov. after him in a posthumous recognition of his friendship and contributions to the knowledge of the diversity and conservation of Venezuelan amphibians and reptiles. Photo: F.J.M. Rojas-Runjaic.