Bioacoustics of Hyloscirtus japreria

Etymology. The specific epithet japreria is a nominative used as a noun in apposition. Japreria is an indigenous ethnic group of Carib linguistic affiliation, self-designates as Yankshit. Originally, they lived in the Colombian side of the Sierra de Perijá, and later moved to the Venezuelan side along the Colombian border ( Halbmayer 2013 ). The Japreria had been traditionally considered as a subgroup of the Yukpa ethnic group ( De Villamañán & De Santelos 1957 ), but currently are recognized as an independent group ( Oquendo 2004 ). Its population was ca. 200 individuals according to the 2002 census and its idiom is currently considered as threatened ( Lewis et al . 2016 ). We nominate this new taxon honoring the Japreria people and warning on its cultural loss. Call description of Hyloscirtus callipeza . Advertisement calls of Hyloscirtus callipeza are composed of short tonal notes arranged in long trills ( Fig. 11 ). All notes have multiple amplitude modulation, with three peaks of amplitude per note ( Fig. 11c ). The average duration of note trills is 10.40 ± 6.43 (4.99–17.50) seconds. The average rate of note emission is 5.72 ± 0.18 (5.51–5.83) notes/s, and each note trill contained in average 59.7 ± 37.9 (29– 102) notes. Average note duration is 0.018 ± 0.001 (0.016–0.019) seconds, and the average duration of silent intervals between notes is 0.157 ± 0.010 (0.146–0.181) seconds; notes do not have frequency modulation. Average peak frequency is 3.27 ± 0.03 (3.20–3.33) kHz. Average low frequency is 2.98 ± 0.03 (2.92–3.06) kHz, and average high frequency is 3.61 ± 0.05 (3.47–3.66) kHz. The fundamental frequency is 1.62 ± 0.02 (1.59–1.65) kHz. No additional harmonics were detected in the spectrograms ( Figs. 11b, d ).

Hyloscirtus japreria sp. nov. is a nocturnal and riparian frog. Its presence in the creeks can be readily detected by its conspicuous vocalization, but calling males are visually difficult to detect because they generally call while hidden. All males collected in the two localities at Cerro Las Antenas were found calling actively at the end of the dry season (March) and during the rainy season (July). Also several males were actively calling in May 2009 at the creek of Guacharaca Camp, and in July 2012 at El Manantialito creek. In all localities calling males were found in a variety of sites, generally hidden in bromeliads ( Fig. 10b ), leaf-sheath of Heliconeaceae plants, within rock crevices, and behind waterfalls ( Fig. 10a ), but occasionally they were calling while exposed on ferns leaves, palms, and bush branches near small waterfalls ( Figs. 5c , 10c ). All females were found on leaves and branches near calling males. Only one female was found at Cerro Las Antenas in March 2008 , another three at Guacharaca Camp in May 2009 , and one at El Manantialito in July 2012 . All these five females contain well-developed eggs in their oviducts (noted through skin of the flanks). Metamorphs and post-metamorphs ( Fig. 5f ) were seen in March 2008 at the creeks of Cerro Las Antenas, and in July 2012 at El Manantialito creek. All the specimens collected released a strong odor like moist leaf litter when they were handled.

Description of the holotype . An adult male ( Figs. 2a–b ) of 29.9 mm SVL. Body relatively slender (about 2.4 times longer than wide). Head slightly wider than long (HW: 35.6% of SVL; HeL: 32.9% of SVL; HeL/HW: 0.9). Snout rounded in dorsal view and profile ( Figs. 3a,c ). Eye-naris distance slightly shorter than eye diameter (EN/ ED: 0.9). Canthus rostralis distinct, slightly concave in dorsal view, rounded in cross section; loreal region concave and sloped; lips rounded, not flared; nostrils slightly protruded anterolaterally. Internarial region and top of head flat. Interorbital distance wider than upper eyelid. Eye prominent (ED: 10.2% of SVL). Tympanum distinct, small (TD/ED: 0.4; TD: 4% of SVL); membrane not differentiated but most of circumference of tympanic annulus visible through the skin; about 1/4 of the tympanum concealed dorsally by the supratympanic fold. Supratympanic fold developed, starting at posterior end of upper eyelid and reaching posterior margin of insertion of arm ( Fig. 3c ). Mental gland present, small (diameter about 11% of SVL), disc-shaped, covering the anterior third of throat ( Fig. 3b ). Dentigerous processes of vomers conspicuous, straight, narrowly separated from each other; each process bears 5/6 (right/left) teeth. Choanae large, elliptical, not concealed by palatal shelf of maxillary arch. Tongue oval, completely attached to the floor of mouth; vocal slits large, longitudinal, originating on sides of tongue and extending diagonally toward angle of mouth. Vocal sac moderately distensible, evident externally, bilobate, median and subgular. Forearm wider than upper arm; axillary membrane absent. Outer ulnar fold present ( Fig. 3c ). Fingers short and thick; discs on fingers round, slightly expanded laterally, with clearly defined circumferential groove; disc on FIII slightly wider than tympanum diameter. Relative lengths of fingers: I<II<IV<III. Fingers with fleshy dermal fringes; webbing present among fingers II–IV ( Fig. 3d ); webbing formula II 2 -–3+ III 2 ½–2+ IV . Subarticular tubercles swollen, round or oval; distal tubercle of FIV larger than all others and weakly bifid. Supernumerary tubercles present, small and rounded. Palmar tubercle small, flat, bifid, poorly defined. Prepollical tubercle elliptical, thick, not modified as a spine. Nuptial excrescences absent. Hind limbs robust; ThL: 46.0% SVL; SL: 50.3% SVL; FL: 40.6% SVL. Calcar tubercle absent. Outer and inner tarsal folds present ( Fig. 3e ), inner poorly defined. Toes short, with wide lateral fringes; toe discs small, rounded, barely expanded, slightly smaller than those on fingers. Relative length of toes: I<II<III<V<IV; extensive toe webbing, formula: I 2 -–2+ II 1 +–2½ III 1 ½–2½ IV 2 +–1+ V . Outer metatarsal tubercle small, rounded, slightly elevated; inner metatarsal tubercle elliptical, flat, about three times the size of the outer; subarticular tubercles round, moderately elevated; supernumerary tubercles present, small and rounded. Cloacal opening directed posteroventrally at mid-level of thighs; cloacal sheath short; margins of vent with numerous small folds; numerous warts around the cloaca; supracloacal fold present. Skin on dorsum, flanks, throat, chest, forearms, dorsal and inner surfaces of thighs, smooth; areolate on ventral surface of thighs and coarsely areolate on belly. White parietal peritoneum present, covering almost all ventral surface of abdominal cavity. Color in life of the holotype (based on photographs) . Dorsal background color pale yellow, densely and finely punctuated with dark brown, and with scattered small reddish brown spots. Flanks paler than dorsum and almost without dark brown punctuation. Ventral surfaces immaculate yellowish cream, except margins of the lower jaw that are punctuated with dark brown. Whitish stripes present on external border of upper eyelids and supratympanic folds, longitudinally on the mid-dorsum, on supracloacal fold, ulnar fold, inner and outer tarsal folds, and on dorsal internal surface of shanks. White warts around the cloaca. Axillae bright yellow; groins bright ocher. Fingers I–II, toes I–III, and interdigital membranes of fingers and toes immaculate bright yellow. Iris gray with thin black reticulation. Color of the holotype in preservative (after eight years, May 2017 ). Dorsal and ventral background color pale cream ( Fig. 2a–b ). Head, lower jaw, and all dorsal surfaces (except fingers I–II and toes I–III), with dense and fine pale brown punctuation. Whitish stripes on border of upper eyelids, inner and outer tarsal fold, dorsal internal surface of shanks, and mid-dorsal, all barely visible; whitish and more defined stripes on the supratympanic, ulnar and supracloacal folds. Warts around the cloaca with faint whitish coloration. Measurements of the holotype (in mm). SVL: 29.9; SL: 15.0; ThL: 13.7; FL: 12.1; HaL: 9.4; HeL: 9.8; HW: 10.6; IO: 4.1; InD: 2.6; EN: 2.6; ED: 3.0; TD: 1.2; ETS: 4.5; F3D: 1.5; T4D: 1.4; F1L: 5.5: F2L: 7.0. See Table 2 for measurements of the type series. Morphological and color variation. Hyloscirtus japreria sp. nov. exhibits sexual dimorphism in size ( Fig. 2 ), with adult females larger than males (males: 28.8–32.7 mm [30.3 ± 1.1; n = 17] of SVL vs . females: 35.6–39.1 mm [37.1 ± 1.4; n = 5]). Mental gland, vocal slits and vocal sac are secondary sexual characters present in males and absent in females. Variation of general morphometric characters of the type series is shown in Table 2 . The proportions of the head (slightly wider than long to as wide as long) are very similar in the type series and do not differ between sexes (HeL/HW: 0.9–1.0; n = 22), but the relative size of the head is slightly larger in males (HeL: 29.4–33.5% of SVL [32.1 ± 1.0; n = 17]; HW: 31.8–37.0% of SVL [34.6 ± 1.3; n = 17]) than in females (HeL: 28.7–30.4% of SVL [29.7 ± 0.7; n = 5]; HW: 28.8–33.7% of SVL [32.0 ± 2.0; n = 5]). The tympanum is relatively small (3.4–5.0% of SVL [4.2 ± 0.4; n = 22]) and its ratio with respect to the eye has little variation between sexes (TD/ED: 0.3–0.4 [ n = 17] in males vs. 0.4–0.5 [ n = 5] in females). EN/ED ratio is also variable; however, in all but one specimen of the type series, eye-naris distance is smaller than eye diameter (0.6–1.0 [0.8 ± 0.1; n = 22]). The eye is prominent and relatively bigger in males than females (ED: 10.2–12.0% of SVL [10.8 ± 0.6; n = 17] in males vs. 9.2–10.4% of SVL [9.9 ± 0.5; n = 5] in females). ETS/ED ratio is also slightly variable but snout is always longer than eye diameter (1.1–1.5 [1.3 ± 0.1; n = 22]). Hand length ranges from 24.5–31.6% of SVL (29.0 ± 1.7; n = 22). Thigh length ranges from 43.5–48.9% of SVL (46.4 ± 1.6; n = 22); shank length ranges from 44.8–52.8% of SVL (49.2 ± 1.9; n = 22), and foot length ranges from 35.2–42.8% of SVL (38.8 ± 1.7; n = 22). Hand webbing variation: II (2-–2+)–(3+–3¼) III (2½–3-)–(2+–2½) IV ; modal hand webbing formula: II 2 -–3+ III 2 ½–2+ IV . Foot webbing variation: I 2 -–(2+–2½) II (1+–1½)–(2–3-) III (1+–1½)–(2+–3-) IV (2+–3-)–(1+–1¼) V ; modal foot webbing formula: I 2 -–2+ II 1 +–2½ III 1 ½–2½ IV 2 ½–1+ V . Morphometric Males ( n = 17) Females ( n = 5) Characters X ± SD Min-Max X ± SD Min-Max SVL 30.3 ± 1.1 28.8–32.7 37.1 ± 1.4 35.6–39.1 SL 14.8 ± 0.5 13.8–15.9 18.7 ± 0.5 18.0–19.2 Thl 14.1 ± 0.4 13.4–14.9 17.1 ± 0.5 16.5–17.8 FL 11.6 ± 0.4 10.9–12.6 14.8 ± 0.5 14.5–15.6 HaL 8.8 ± 0.4 8.3–9.9 10.5 ± 0.8 9.6–11.3 HeL 9.7 ± 0.2 9.4–10.2 11.0± 0.2 10.8–11.2 HW 10.5 ± 0.4 9.8–11.0 11.8 ± 0.6 11.2–12.4 IO 4.0 ± 0.2 3.5–4.3 4.6 ± 0.1 4.4–4.8 InD 2.4 ± 0.1 2.2–2.8 2.6 ± 0.1 2.5–2.7 EN 2.7 ± 0.2 2.3–3.1 3.2 ± 0.3 2.9–3.5 ED 3.3 ± 0.2 3.0–3.7 3.7 ± 0.1 3.5–3.8 TD 1.2 ± 0.1 1.0–1.5 1.7 ± 0.1 1.5–1.8 ETS 4.4 ± 0.2 4.0–4.6 4.9 ± 0.2 4.7–5.2 F3D 1.5 ± 0.1 1.2–1.7 1.7 ± 0.2 1.5–1.9 T4D 1.3 ± 0.1 1.1–1.5 1.5 ± 0.1 1.3–1.6 F1L 5.4 ± 0.2 4.8–5.8 6.5 ± 0.4 5.8–7.1 F2L 6.9 ± 0.3 6.3–7.4 8.2 ± 0.5 7.7–9.0 Skin texture, warts, folds, shape of the head and aspect of the tympanum do not exhibit relevant variation in the examined specimens. Mental gland very conspicuous and similar to the holotype in almost all males of the type series; roughly pentagonal in shape in MHNLS 18971, and less defined in MHNLS 18837, 19234 and 19237. Color pattern is variable in Hyloscirtus japreria sp. nov. ; metamorphs and juveniles are typically apple green with dorsal and interorbital blackish spots ( Fig. 5f ). Background color in live adults can be pale cream, pale yellow, greenish yellow, pale green, and yellowish brown ( Fig. 5 ); dorsal pale brown punctuation is very variable (in life and in preserved specimens), with some specimens showing dense and finely punctuated patterns, others scattered punctuated, or with scattered reddish brown spots alternated with densely (or scattered) punctuation ( Figs. 5–6 ). Blackish brown canthal stripes and blackish brown spots above the upper eyelids are present in some specimens (male MHNLS 22568, and females, MHNLS 18837, 18867–18868 18972, 18988, 19235). The intensity of the whitish stripes on the different folds is also variable, and the mid-dorsal whitish stripe can be present (males MHNLS 18838, 18971–18972, 19234, 22568, and females MHNLS 18868, 19235, 19166–19167) or absent (males MHNLS 18837, 18867–18868, 18888–18889, 18988, 19168, 19237). Ventrally, some specimens have scattered dots on the mandible (males MHNLS 18837–18838, 18867, 18869, 18888–18889, 18971–18972, 18988, 19168, 19234, and female MHNLS 19166). Call description. Advertisement calls of Hyloscirtus japreria sp. nov. are formed by very long trills of short tonal notes ( Fig. 7 ). Notes present amplitude modulation, with a single peak of amplitude ( Fig. 7c ). The average duration of note trills among the three specimens recorded is 114.93 ± 40.24 (79.72–159.62) seconds. The average rate of note emission is 6.36 ± 0.61 (5.30–6.71) notes/s, and each note trill contained in average 738 ± 284.18 (421– 1058) notes. Average note duration is 0.041 ± 0.005 (0.037–0.046) seconds, and the average duration of silent intervals between notes 0.102 ± 0.002 (0.101–0.105) seconds; notes do not have frequency modulation. Average peak frequency is 3.13 ± 0.04 (3.08–3.15) kHz. Lower frequency of notes is 2.99 ± 0.06 (2.92–3.03) kHz on average, and average upper frequency reaches 3.28 ± 0.01 (3.27–3.28) kHz. The fundamental frequency is 1.57 ± 0.02 (1.54–1.59) kHz. At least three other harmonics are detectable in the spectrograms, at 4.63–4.78 kHz, 11.52– 11.58 kHz, and 17.79–17.85 kHz ( Figs. 7b,d ).

Diagnosis. Hyloscirtus japreria sp. nov. is readily distinguishable from all other species in the H. armatus and H. larinopygion groups by the presence of mental gland in males (present in almost all species of H. bogotensis species group). Of the 16 species currently included in the H. bogotensis Group only five are known to occur on the northwestern portion of the Andes (northern Cordillera Oriental of Colombia, Sierra de Perijá and Cordillera de Mérida in Venezuela); these are: H. callipeza , H. estevesi , H. jahni , H. lascinius and H. platydactylus ( Fig. 4 ). Hyloscirtus japreria sp. nov. differs from H. callipeza (characters of the latter in parenthesis) by having ulnar, outer and inner tarsal folds (absent), snout rounded in profile (truncate), tympanic annulus distinct (barely visible), skin of belly coarsely areolate (granular), webbing bright yellow in life (pale orange), by having a whitish ulnar stripe (absent), a whitish stripe on dorsal internal surface of shank (absent), and iris gray with thin black reticulation (bronze with thin black reticulation); also adult females of H. japreria sp. nov. are larger than females of H. callipeza (maximum SVL: 39.1 mm in H. japreria sp. nov. vs. 36.7 mm in H. callipeza ). These two species also differ in temporal and spectral characteristics of advertisement calls: H. japreria sp. nov. emits much longer trills (79.72– 159.62 s vs. 4.99– 17.50 s ), and more notes by trill (421–1,058 vs . 29–102 notes) than H. callipeza ; the notes of H. japreria sp. nov. are also longer (0.037– 0.046 s vs . 0.016–0.019) and less spaced (time between notes: 0.101– 0.105 s vs . 0.146– 0.181 s ) than those of H. callipeza . The two species also differ in the number of amplitude peaks per note, with a single peak in H. japreria sp. nov. ( Fig. 7c ) and three peaks of amplitude per note in H. callipeza ( Fig. 11c ). Finally, both peak and fundamental frequencies are lower in H. japreria sp. nov. than in H. callipeza (peak frequency: 3.08–3.15 kHz vs . 3.20–3.33 kHz; fundamental frequency: 1.54–1.59 kHz vs . 1.59– 1.65).