Hyalinobatrachium tatayoi, Castroviejo-Fisher, Santiago, Ayarzagüena, José & Vilà, Carles, 2007

Castroviejo-Fisher, Santiago, Ayarzagüena, José & Vilà, Carles, 2007, A new species of Hyalinobatrachium (Centrolenidae: Anura) from Serranía de Perijá, Venezuela, Zootaxa 1441, pp. 51-62 : 52-59

Hyalinobatrachium tatayoi , sp. nov.

Holotype. MHNLS 17174, adult male ( Fig. 1a ,b) from a stream near Tokuko (09° 50’ 30.6’’ N, 72° 49’ 13.6’’ W; 301 m. a.s.l.), Estado de Zulia, Venezuela, collected on July 12, 2005 by the Santiago Castroviejo-Fisher, José Ayarzagüena, and Carles Vilà.

Paratypes. Same locality and date as holotype, MHNLS 17172–73, 17176, 17179–81, 17183– 84 adult males; MHNLS 17177 ( Fig. 2a ) and 17182 ( Fig.2 b), adult females. All collected by Santiago Castroviejo- Fisher, José Ayarzagüena, and Carles Vilà.

Diagnosis. The new species is placed in the genus Hyalinobatrachium because it has a bulbous liver (dissection of MHNLS 17173) and lacks a humeral spine in males ( Ruíz-Carranza & Lynch 1991; Duellman & Señaris 2003). The following combination of characters distinguish Hyalinobatrachium tatayoi from other species of the genus: 1) vomerine teeth absent; 2) white bones in life; 3) parietal peritoneum transparent; pericardial, hepatic and visceral peritonea white ( Figs. 1 b and 2b); 4) in life, the dorsal surface is dark apple green with small pale yellow spots; small melanophores reaching the last phalange of the fifth toe; yellow iris with black flecks more concentrated towards the pupil creating a horizontal band that connects the pupil with the lateral edges of the eye ( Fig. 1a ); colour in preservative cream with purple melanophores following pattern described above; 5) webbing on hand III 2 – 1 1/ 2 IV ( Fig. 3 a), absent between Fingers I and II and basal between Fingers II and III; 6) webbing on foot I 1 – 1 3/ 4 II 1 – 1 1/ 4 III 1+ – 2 IV 2 – 1 V ( Fig. 3 b); 7) snout semi-round in dorsal view and round in profile in holotype ( Fig. 4 a, but see Variation); 8) dorsal skin shagreen in life, in preservative slightly shagreen; 9) enamelled ulnar and tarsal folds, post cloacal enamelled warts and folds; 10) humeral spine absent; 11) tympanum covered by skin (not visible through skin); 12) adults of medium size (males between 21.5–22.4 mm and females 22–22.6 mm); 13) nuptial excrescence formed by a group of glands on Finger I; these glands are also visible on the lateral fringes of the other fingers and the membrane between Fingers III and IV; the glands also evident in the webbing between toes ( Figs. 3 a and b); 14) enamelled small glands on the lower part of the upper lip and over the skin covering the jaw ( Fig. 4 b); 15) when adpressed, Finger I almost as long as II; 16) bulbous liver; 17) males calling on the upper- and undersides of leaves; 18) single note advertisement call of 0.113–0.158 sec. duration, dominant frequency of 4561.7–4728.6 Hz and structured in two parts, first a group of modulated pulses and second a modulated sound (Fig. 5); 19) monolayer clutches located on the underside of leaves consisting on 35– 40 eggs, males guard clutches during the night.

We assign Hyalinobatrachium tatayoi sp. nov. to the Hyalinobatrachium fleischmanni group ( Ruíz-Carranza and Lynch 1991) because of the presence of white bones in life, white pericardial, visceral and hepatic peritonea, lack of vomerine teeth, and a clutch composed by one layer of eggs deposited on the underside of leaves.

This species can be distinguished from all the species in the Hyalinobatrachium chirripoi subgroup by having white pericardium versus transparent in the former.

In general, this species can be distinguished from all the species in the Hyalinobatrachium fleischmanni group by the presence of enamelled glands on the skin covering the jaw. This character, present in males and females of H. tatayoi , and easy to check in life and preserved individuals, readily differentiates H. tatayoi from other congenerics. Character states of species of the H. fleischmanni group, are summarized in Table 1.

Description of Holotype. Adult male of medium size, SVL 21.5 mm; head slightly wider than body, HW 39.3% of SVL; ratio HW/HL of 1.39; snout semi-round in dorsal view and round in profile; ES/EL 0.85 and ES/IOD 1.22; loreal region concave; nostrils not prominent, round; internarinal region depressed; canthus rostralis not defined; eyes slightly bigger than congenerics, directed antero-laterally; EL 51.7% of HL; EW/IOD 1.1; tympanum covered by skin, indistinct, lack of supratympanic fold; dentigerous processes of vomer absent; choanae small, circular, widely separated; tongue elongate, ovoid, not attached to mouth posteriorly preservative (P). Present (+), absent (-). Hand webbing formula. Folds: enamelled ulnar and tarsal folds. AD: Anal decoration (enamelled warts and folds). Mand. glands:

enamelled glands on the skin covering the jaw. Glands in hand/feet: presence of warts on the webbing of hands and feet.

Taxa Snout(dorsal; Webbing Folds AD Mand. Glands Dorsal coloration (P) Iris (L) Source lateral) formula (P) (P) glands in hand/

(L, P) feet (P)

. crurifasciatum Truncate ; III 2 – 2 -/+ + - - Cream dotted with medium and big Yellow with dark This work

truncate IV melanophores, big cream spots flecks

duranti Truncate ; III 2 + – 2- - - - +; + Cream dotted with medium and big Yellow with a This work

truncate IV melanophores, medium size cream reddish ocular spots ring

. eccentricum Truncate ; III 2 – 2 - + - - Cream dotted with medium and big Yellow with a This work

truncate IV melanophores, big cream spots brown

circumpupillary zone concealing pupil, pupillary ring absent

. esmeralda Round; round III 2 + – 2+ - - - - Cream with small purple Golden with Ruíz-Carranza IV melanophores, small cream spots brown dots and Lynch (1998)

. fleischmanni Round ; truncate II 2 – 3 - - - - Cream with small purple Yellow with This work, 1/ 2 III 2 1/2 melanophores, small cream spots black flecks Savage (2002) – 2 IV

. ibama Round ; truncate III 2 + – 2- - - - - Cream dotted with medium and big Golden with Ruíz-Carranza IV melanophores, big cream spots brown dots and Lynch (1998) for about one sixth of its length; vocal slits extending from the sides of the base of tongue to the level of the mandibular joints; forearms slim; diameter of forearms about three times diameter of upper arms; enamelled ulnar fold extending from elbow to disc on Finger IV; lack of humeral spine; relative length of fingers: II <I <IV <III; finger discs wide, truncated and larger than those on toes; FIII 26% of EL; webbing absent between Fingers I–II and basal between II–III but a small fleck remains in the external side of Finger II, webbing formula on hand III 2 – 1 1/ 2 IV; subarticular tubercles round and small, hardly appreciable on Finger IV; supernumerary tubercles small and hardly appreciable; palmar tubercle round and small, thenar tubercle small and elongated; nuptial excrescences comprise a group of glands on the dorso-medial base of thumb, glands present on membranes and fingers, some of them (Finger IV) enamelled; hind limbs slender; TL 57.1% of SVL; enamelled tarsal fold present, extending to tip of Toe V; discs of toes round, truncate in profile; inner metatarsal tubercle small and ovoid, hardly appreciable; outer metatarsal tubercle absent; supernumerary tubercles very small, low and hardly visible; small gland cells on toes and on the webs between, some of them enamelled; webbing formula of feet I 1 – 1 3/ 4 II 1 – 1 1/ 4 III 1+ – 2 IV 2 – 1 V; in preservative, dorsal skin covered by white guanophores that make it shagreen, area around tympanum almost granular; skin on belly granular, other ventral surfaces smooth; cloacal opening directed posteriorly at upper level of thighs, concealed by a dermal fold and flanked by irregular enamelled warts.

Color in life: Dorsum apple green with small yellow spots on dorsum, femur, tibia and forearms, dusted with small dark melanophores on forearms, femur, tibia and tarsus reaching the distal phalange of the fifth toe. Fingers and toes dark yellow. Iris yellow reticulated by black flecks, presence of a black/dark grey horizontal “mask” that connects the pupil with the lateral edges of the eye. Parietal peritoneum transparent; pericardium and visceral peritonea white. Enamelled folds on ventro-lateral edges of Finger IV, forearms, elbows, Toe V and cloaca.

Color in preservative: Dorsum clear lavender as a result of the presence of numerous dark purple melanophores. Presence of small cream spots correspond to the absence of melanophores. Melanophores more concentrated on the upper eyelids producing a darker pattern. Upper arms, hands and Toes I–IV cream and free of melanophores. Venter creamy white.

Measurements (in mm): SVL = 21.6; HL = 6.1; HW = 8.5; IOD = 2.2; EL = 3.2; EW = 2.4; ES = 2.7; FIII = 0.8; FL = 13; TL = 12.3; FL = 9. Measurements of the type series are shown in Table 2 .

Va ri a ti on. Females have a transparent bluish-green dorsum similar to the color of green gooseberries (see Figure 2a ) with a grey “mask” in the iris. This difference in coloration compared to males is more evident during daytime. Females also present gland cells in the webbing of fingers and toes. Shape of the head in dorsal and lateral views varies as follows: MHNLS 17172 semiround, truncate; MHNLS 17173 semiround, roundtruncate; MHNLS 17176 semiround, round-truncate; MHNLS 17177 semiround, truncate; MHNLS 17179 semiround, round; MHNLS 17180 round, sloping; MHNLS 17181 round, round; MHNLS 17182 semiround, round-truncate; MHNLS 17183 semiround, round-truncate; MHNLS 17184 semiround, round-truncate. The area between eyes and nostrils is very sloping in MHNLS 17172 and MHNLS 17177 creating a depression between the tip of the snout and the eyes. Webbing formula in feet varies as follows: I (1-1 1/2) – (1 3/4-2) II (1- 1+) – (1 3/4-2) III (1+-1 1/2) – 2 IV 2 – (1 1/4-1) V.

FIGURE 5. Oscillogram (top) and spectrogram (bottom) of 200 ms section of the call of the holotype of Hyalinobatrachium tatayoi sp. nov. Air and water temperature at the time of recording were 26.9 and 24.9° C.

Natural history. Specimens were found on leaves (1–3 m above water) along a stream. All males, except MHNLS 17181, were calling. Males started to call 30 minutes before dark from the upper side of leaves, and gradually moved to the underside where they emitted the advertisement call. The holotype was found on the underside of a leave guarding a monolayer clutch composed of 40 eggs (preserved in ethanol 70%, MHNLS 17178). Two individuals (MHNLS 17176–77) were found in amplexus in the underside of a leave, the female was gravid. Close to the amplectant pair we found a clutch (MHNLS 17178) composed of 35 eggs. Eggs were collected live and tadpoles were reared to different developmental stages and preserved in 70 % ethanol. Tadpoles will be described elsewhere. MHNLS 17183 was found calling on the underside of leave together with MHNLS 17182, a non gravid female. At a distance of one meter from this couple, MHNLS 17184 was calling from the upper side of a leave. We could not establish if parental care also occurs during daylight.

Calls. The calls described below correspond to MHNLS 17174, 17183 and specimens not captured. Two types of calls were identified. The advertisement call of H. tatayoi sp. nov. (Fig. 5) was emitted by individuals located on the underside of leaves and consisted of a single high-pitched, half pulsed, half modulated note lasting 0.113–0.158 seconds (average ± SD = 0.135 ± 0.0161; n = 20) with a call repetition rate of 8.8 calls/ minute, a dominant frequency of 4561.7–4728.6 Hz (4655.8 ± 61.7) and that it was clearly audible at long distances. All the calls analyzed (n= 20) were composed of two parts. The first third of the call consisted of 4–12 modulated pulses (7.5 ± 2.5). The group of pulses started at a frequency between 3293.4–36972.2 Hz (3336.4 ± 713.8) with the subsequent pulses increasing their frequency (= 4.5 KHz) and energy. The second part of the call consisted of a modulated sound that started with a slight increase in frequency, compared to the previous pulse, and reaching a maximum frequency 4684.1–5222.5 Hz (4991.8 ± 157.3). A very weak secondary frequency (harmonic) was detected in three calls (out of 20) at a frequency of about 13500 Hz, but it was too weak to be analyzed. Señaris and Ayarzagüena (2005) provided a description of the advertisement calls of all the Venezuelan species of Hyalinobatrachium , except H. fragile , and none of them resembles the call of H. tatayoi (see Table 3 for comparison). The advertisement call of H. fleischmanni ( Starret & Savage 1973; Ibáñez et al. 1999; Savage 2002) resembles the one of H. tatayoi in duration, dominant frequency and that it starts with a fast increase of its frequency. However, it lacks a well define group of pulses at the beginning of the call and the call is maintained over 5000 Hz.

The second call consisted on a variation of the first one and was emitted by specimens located on the upper side of leaves. It had the same structure as the advertisement call, but it could be differentiated by having a weaker group of modulated pulses, with less energy and a smaller increase in the frequency.

Distribution and ecology. Hyalinobatrachium tatayoi is only known for the Venezuelan Cordillera de Perijá, in the Northern border between Colombia and Venezuela ( Fig. 6 ). For political and security reasons the Serranía de Perijá has been poorly explored during the last 30 years and current knowledge of its biodiversity is limited. The type locality is part of the submontane rainforest ( La Marca & Soriano 2004). Specimens were located during sunset and night along a stream used to provide water to the Tocuco village. Rana palmipes Spix and juveniles of Bufo haematiticus Cope were found syntopically.

Etymology. This species is dedicated to Santiago Castroviejo Bolíbar “Tatayo” for his work on plant taxonomy and systematics in the Neotropic and the Paleartic and for his help, support and love to SCF.

Figures

FIGURE 3. Ventral view of hand (a) and foot (b) of Hyalinobatrachium tatayoi sp. nov., paratype MHNLS- 17173.

FIGURE 4. Lateral (a) and ventral (b) view of head of Hyalinobatrachium tatayoi sp. nov., holotype.

FIGURE 6. Distribution of Hyalinobatrachium tatayoi sp. nov. in Serranía de Perijá, Zulia, Venezuela. We only represent the distribution of H. fleischmanni in Cordillera Oriental, Colombia.

FIGURE 1. a) Male of Hyalinobatrachium tatayoi sp. nov., holotype; b) Ventral view.

FIGURE 2. a) Female of Hyalinobatrachium tatayoi sp. nov., paratype MHNLS 17177; b) Ventral view of Hyalinobatrachium tatayoi sp. nov., paratype MHNLS 17182. Arrow indicates small white enamelled glands delimiting the jaw.

Tables

TABLE 2. Measurements of the type specimens of Hyalinobatrachium tatayoi sp. nov. (M, male; F, female; for other abbreviations, see Material and Methods).

Collection number Sex	SVL	HL	HW	IOD	EL	EW	ES	FIII	FL	TL	FL
MHNLS 17174 M	21.6	6.1	8.5	2.2	3.2	2.4	2.7	0.8	13.0	12.3	9.0
MHNLS 17172 M	21.5	5.4	8.2	2.2	3.2	1.8	2.4	1.0	12.0	11.3	9.1
MHNLS 17173 M	21.9	6.1	7.9	2.3	2.7	1.8	2.8	1.0	13.1	12.5	9.3
MHNLS 17176 M	21.8	6.1	8.3	2	3	1.7	2.5	0.8	12.2	11.7	8.4
MHNLS 17179 M	22.3	6.1	7.9	2.2	2.9	1.4	2.6	1.0	12.9	12.2	8.7
MHNLS 17180 M	21.8	6.1	8.0	2.3	3.3	1.8	2.9	0.8	12.4	11.8	9.5
MHNLS 17181 M	23.2	7.4	9.0	2.8	3.1	1.6	2.8	1.0	12.0	12.5	9.1
MHNLS 17183 M	24.4	6.7	9.2	2.3	3.2	1.6	3.2	1.0	12.7	13.3	10.2
MHNLS 17184 M	22.7	6.3	8.2	2.6	3.1	1.4	2.8	0.8	12.7	12.5	9.5
MHNLS 17177 F	22.6	6.3	8.4	2.5	3.1	1.6	2.8	0.9	12.6	12.8	9.1
MHNLS 17182 F	22.1	6.1	8.6	2.3	3.2	1.5	2.9	1.0	11.0	12.5	8.8