Hyalinobatrachium tricolor, Castroviejo-Fisher, Santiago, Vilà, Carles, Ayarzagüena, José, Blanc, Michel & Ernst, Raffael, 2011

Castroviejo-Fisher, Santiago, Vilà, Carles, Ayarzagüena, José, Blanc, Michel & Ernst, Raffael, 2011, Species diversity of Hyalinobatrachium glassfrogs (Amphibia: Centrolenidae) from the Guiana Shield, with the description of two new species, Zootaxa 3132, pp. 1-55 : 33-36

Hyalinobatrachium tricolor sp. nov.

( Fig. 11 )

Hyalinobatrachium nouraguense Lescure and Marty, 2000: 74 .

Hyalinobatrachium aff. iaspidiense Guayasamin et al., 2008a: 580 .

Holotype. MNCN 44827 (field code MB 250), adult male from Crique Wapou (04°26' N, 52°9' W; 2 m), Kaw, French Guiana, collected by M. Blanc on April 11, 2005.

Paratopotypes. MNHN 2011.0116 (field code MB 247), MTD 48141 (field code MB 249), adult males collected by M. Blanc on April 4 and 11, 2005, respectively.

Paratype. MNCN 44828 (field code MB 326), adult male from Kaw Mountain (04°32' N, 52°13' W; 10 m), French Guiana, collected by M. Blanc on January 18, 2008.

Diagnosis. (1) Dentigerous processes on vomer and vomerine teeth absent; (2) snout truncated in dorsal and lateral view; (3) tympanum covered by skin, not visible through skin; (4) dorsal skin shagreened in life and preservative, (5) presence of small cloacal enameled warts; (6) parietal peritoneum transparent, pericardium transparent, visceral and hepatic peritonea white, all other peritonea transparent; (7) liver bulbous; (8) humeral spine absent; (9) webbing formula of fingers III 2 – (2 – 2+) IV; (10) webbing formula of toes I 1 – 2 II 1 – 2 III 1 – 2 IV 2 – 1 V; (11) enameled ulnar and tarsal folds; (12) nuptial pad Type-V, composed by a group of packed glands and situated in the medial, dorso-lateral internal side of Finger I, glands not present in other fingers, prepollex not evident from external view; (13) Finger I longer than Finger II; (14) eye diameter larger than width of disc on Finger III; (15) coloration in life: dorsum light green with big irregular darker green patches, brown warts, and minute melanophores, bones white; (16) coloration in preservative: cream with big irregular white patches and black dots; (17) iris yellow with dark grey flecks; (18) minute melanophores not extending throughout fingers and toes except base of Finger IV and Toe V; in life, tip of fingers and toes white; (19) advertisement call composed by four tonal notes but with a fast increase of energy at the beginning of each note lasting 0.19– 0.20 s, dominant frequency of 4628.11–4903.07 Hz, males call from the underside of leaves; (20) fighting behavior unknown; (21) egg clutches deposited on the underside of leaves, number of eggs per clutch 22 (N = 2), no parental care observed; (22) tadpole unknown; (23) medium size adult males, SVL = 20.3–21.0 mm (N = 4), females unknown.

Comparisons. Following Guayasamin et al. (2009), we placed the new species in the genus Hyalinobatrachium because of the following characters: humeral spine absent in adult males; digestive tract and bulbous liver covered by white peritonea; completely transparent ventral parietal peritoneum; white bones in life; dorsal coloration cream in preservative; males lack conspicuous dorsal spinules during breeding season; nuptial pad small and restricted to the inner edge of Finger I in males (Type V); dentigerous process of the vomer and vomerine teeth absent; males vocalize from the undersides of leaves, and females deposit one layer of eggs on the undersides of leaves.

The following unique combination of phenotypic characters differentiates Hyalinobatrachium tricolor sp. nov. from all other species in the genus: bones white in life, coloration in life lime green patches over a light green dorsum and brown warts, and advertisement call composed by four tonal notes lasting 0.19– 0.20 s and a dominant frequency of 4628.11–4903.07 Hz. Additional morphological, acoustic and genetic evidence supporting the status of this species could be found in Tables 1, 3, 5, and Figs 2 , 3, 11. Nonetheless, in preservative is, to the best of our knowledge, indistinguishable from H. iaspidiense and H. mesai .

(number of calls = 16). Time is given in seconds and frequency in Hertz, range is followed by mean and standard deviation.

First note Note duration 0.015–0.025; 0.018 ± 0.003

Dominant frequency 4706.76–4859.01; 4761.327 ± 50.859 Lower frequency 3840–4232; 3981.125 ± 113.933

Upper frequency 5032–5290; 5116.875 ± 69.894

Time between notes 0.018–0.03; 0.025 ± 0.003

Second note Note duration 0.011–0.019; 0.015 ± 0.003

Dominant frequency 4635.73–4935.13; 4790.738 ± 86.326 Lower frequency 3248.000–4075.000; 3813.688 ± 211.981 Upper frequency 5183.000–5635.000; 5372.000 ± 139.295

Time between notes 0.049–0.550; 0.116 ± 0.170

Third note Note duration 0.008–0.016; 0.011 ± 0.002

Dominant frequency 4672.220–4903.070; 4804.573 ± 75.012 Lower frequency 3150.000–4094.000; 3800.438 ± 265.126 Upper frequency 5290.000–5936.000; 5597.375 ± 175.162

Time between notes 0.061–0.660; 0.105 ± 0.148

Fourth note Note duration 0.008–0.110; 0.028 ± 0.036

Dominant frequency 4732.140–4935.130; 4816.679 ± 69.292 Lower frequency 3023.000–4251.000; 3844.250 ± 316.712 Upper frequency 5290.000–5976.000; 5668.688 ± 185.800

Remarks. Lescure and Marty (2000) cited H. iaspidiense (= nouraguense ) for Kaw, although they did not refer to any museum material. We assume that those specimens belong to H. tricolor sp. nov.

Description of holotype. Adult male of small size, SVL 20.3 mm; head wider than body, HW 41 % of SVL; head wider than long (HW/HL = 1.3); snout truncate in dorsal view and profile; ES/EL = 0.8 and ES/IOD = 1.2; loreal region concave; nostrils prominent, round; internarial region depressed; canthus rostralis defined; eyes small, directed antero-laterally; EL 50 % of HL; tympanic annulus indistinct, tympanic membrane absent, supratympanic fold absent; dentigerous processes on vomers absent; choanae circular, separated; tongue elongate, ovoid, not attached to mouth posteriorly 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 one and a half times the diameter of upper arms; enameled ulnar fold evident; humeral spine absent; relative length of fingers: II <I <IV <III; finger discs wide, truncated and larger than those of toes; FIII 30 % of EL; webbing absent between Fingers I–II and basal between II–III, webbing formula on hand III 2 – – 2+ IV; subarticular tubercles round; supernumerary tubercles slightly appreciable; palmar tubercle round and small, thenar tubercle small and elongated; nuptial excrescences Type V, glands on the lateral fringes of fingers not observed; hind limbs slender; TL 50 % of SVL; enameled tarsal fold evident; discs of toes round, truncate in profile; inner metatarsal tubercle small and ovoid; outer metatarsal tubercle absent; supernumerary tubercles slightly appreciable; webbing formula of feet I 1 – 2 II 1 – 2 III 1 – 2 IV 2 – 1 – V. In preservative, dorsal skin scarcely covered with enameled granules, area around tympanum almost granular; skin on belly and thighs granular, other ventral surfaces smooth; cloacal opening directed posteriorly at upper level of thighs, concealed by a dermal fold and flanked by evident and enameled irregular folds and warts.

Color in life. Dorsal surfaces light green with irregular lime green patches and dusted with minute black melanophores extending to the base of Finger IV and Toes IV and V. Presence of single and blotches of brown (coffee like color) warts over dorsal surfaces of body and posterior limbs. Tip of fingers and toes white to light green with traces of yellow. Enameled tarsal and dorsal folds extending to the tip of Finger IV and Toe I. Cloacal ornamentation consisting of enameled warts and folds. Iris yellowish, clearing out towards eyelids, and with dark flecks. Parietal peritoneum and pericardium transparent, pericardium, hepatic, and visceral peritonea white, peritonea covering all other internal organs not mentioned before transparent.

Color in preservative. Background of dorsal surfaces cream and dotted by a coat of minute dark melanophores and black dots. Large and irregular white patches due to concentration iridiophores. Note that the brown warts of live specimens become black dots undistinguishable from those of Hyalinobatrachium iaspidiense and H. mesai . Enameled tarsal, ulnar and cloacal folds. Iris white. Peritonea as mentioned above.

Variation. Measurements and body proportions of the holotype and paratype MNCN 44828 are presented in Table 2. The number and aggregation of brown warts varies between specimens from just two aggregated warts in MTD 48141 to 21 single warts in MNHN 2011.0116.

Advertisement call. We recorded 16 calls of Hyalinobatrachium tricolor sp. nov. from its type locality from two not collected specimens. We assigned the recorded calls to the new species because they are identical to the ear to those emitted by specimens of the type series, which we observed calling. The call of Hyalinobatrachium tricolor sp. nov. is unique among all other species of the genus by having four notes per call ( Fig. 2 H, Tables 3, 5). All other described species of Hyalinobatrachium with known calls have a single note call except H. taylori (5–9 notes per call). Barrio-Amorós and Brewer-Carías (2008) mention that H. mesai had one and two notes calls; however, we think that this rather represent two calls within a short interval of time, which have been observed in topotypes of H. iaspidiense (J. Ayarzagüena, personal observation). Each note of the call of H. tricolor sp. nov. is tonal but with a high increase in frequency at the beginning from 3023.0–4251.0 Hz (3640.2 ± 555.5) to a maximum of 5183.0–5976.0 Hz (5551.7 ± 348.6). The call lasts for 0.19– 0.20 s (0.20 ± 0.003) with a dominant frequency of 4628.1–4903.1 Hz (4777.3 ± 85.8). Values for the measured parameters for each note are presented in Table 5.

Etymology. The specific epithet refers to its dorsal coloration, which is a combination of three colors: light green, dark green and brown in life, and cream, white and black in preservative.

Biology and tadpole. Males call from the underside of leaves during night and close to egg clutches. Together with MNCN 44828 we collected two clutches of 22 eggs each.

Ecology and distribution. Specimens were found in the Crique Wapou, Réserve Naturelle des Marais de Kaw-Roura, and in Kaw Mountain, French Guiana. These localities are at low elevation (2–10 m) and occupied by Amazon rainforest. Males were found on leaves on the vegetation over streams 0.5–1.5 m deep and at heights of 4– 5 m. This species is only known from these two localities in French Guiana and it is restricted to the Guiana Shield.

Figures

FIGURES 2. Comparative oscillograms and spectograms of advertisement calls of Hyalinobatrachium species from the Guiana Shield and H. fleischmanni: (A) H. fleischmanni from Panama, audio from Ibañez et al. (1999); (B) H. kawense sp. nov. from French Guiana, MNCN 44825; (C) H. cappellei Venezuela, MHNLS 17328; (D) H. cappellei French Guiana, audio from Marty and Gaucher (1999); (E) H. iaspidiense from Venezuela, MHNLS 13495; (F) H. iaspidiense from French Guiana, audio from Marty and Gaucher (1999); (G) H. mesai, holotype; (H) H. tricolor sp. nov. from type locality in French Guiana, uncollected specimen; (I) H. mondolfii from Venezuela, MHNLS 17120; (J) H. taylori from Venezuela, MHNLS 13496.

FIGURE 11. Hyalinobatrachium tricolor sp. nov. from Kaw, French Guiana. (A, B) holotype, MNCN 44827, SVL = 20.3 mm; (C) paratopotype MNHN 2011.0116, SVL = 21.0 mm; (D, E) paratype MNCN 44828, SVL = 20.7 mm; (F) egg clutch on the underside of a leafcollected with MNCN 44828. Photographs by SCF (A) and MB (B – F).