Hyalinobatrachium taylori

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 : 31-33

Hyalinobatrachium taylori

( Fig. 10 )

Centrolenella taylori Goin, 1968: 115 .

Hyalinobatrachium taylori Ruiz-Carranza and Lynch, 1991: 25 .

Type locality. Along New River, 228.6 m, Guyana.

Diagnosis. (1) Dentigerous processes of vomer and vomerine teeth absent; (2) snout round in dorsal view, sloping in lateral view; (3) tympanum small, appreciable in the lower portion; (4) dorsal skin from smooth to slightly shagreened in life and preservative; (5) ventral skin granular, presence of small cloacal enameled warts; (6) parietal peritoneum transparent, pericardium white with small transparent areas, visceral and hepatic peritonea white, all other peritonea transparent; (7) liver bulbous; (8) humeral spine absent; (9) webbing formula of fingers:III (1 1/2 – 2-) – (1+ – 1 1/2) IV; (10) webbing on foot: I (1 – 1+) – (2 – 2+) II (1 – 1+) – (2- – 2) III (1 – 1+) – (2 1/3 – 2 1/2) IV (2 – 2 1/4) – (1 – 1 1/3) V; (11) enameled ulnar and tarsal folds; (12) nuptial excrescences of Type-V composed of a cluster of glands and situated in the medial, dorsolateral internal side of Finger I and extended externally reaching the base of the disc, glands are also present in webs and fringes of fingers II, III and IV, 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 dark green with pale green spots usually bearing a white fleck (iridiophores) in the center of each spot, bones green; (16) coloration in preservative: dorsum cream with very small purple melanophores making a “pale lavender coat” and white flecks (iridiophores); (17) iris grey with a black reticulate net; (18) minute melanophores not extending throughout fingers and toes, except base of Finger IV and complete Toes V and IV; in life, tip of fingers and toes orange; (19) advertisement call composed of 5–9 tonal notes lasting 0.652– 1.052 s, and a dominant frequency between 4010.00–4350.00 Hz, males call on the upper side of leaves; (20) fighting behavior unknown; (21) egg clutches deposited on the underside of leaves, parental care not observed in males; (22) tadpole with sinistral spiracle, on the last third of the body and directed posteriorly; very short and medial vent tube; (23) adult size between 18.1–19.4 (19.0 ± 0.5, N = 5) mm in males and 20.6 mm in one female.

Comparisons. The following unique combination of phenotypic characters differentiates Hyalinobatrachium taylori from all other species in the genus: snout rounded and sloping in dorsal and lateral views respectivelly, tympanic membrane and annulus appreciable in life, pericardium white with transparent spots, hand webbing formula III (1 1/2-2-) – (1+-1 1/2) IV, dorsal coloration in life dark green with small white dots, dorsal coloration in preservative cream with minute purple melanophores making a “lavender coat” and cream dots, iris coloration in life grey with a black reticulated net, coloration of bones in life green, coloration of hands and feet in life orange, and a tonal 5–9 notes advertisement call without frequency modulation, lasting 0.65– 1.05 s and with dominant frequency of 4010.0–4350.0 Hz.

Morphological, bioacoustic and genetic evidences allowing the differentiation between Hyalinobatrachium taylori and all other species of Hyalinobatrachium from the GS are summarized in Figures 2 , 3, 10 and Tables 1, 3.

Remarks. The morphological study of the complete type series of H. taylori (N = 5) indicated the presence of three differentiated phenotypes. The holotype ( Fig. 10 A) is unique among the type specimens and is characterized by its slender appearance, snout round in dorsal view and sloping in profile, pericardium partially white (dissected), dorsal coloration pale lavender with small unpigmented areas, webbing formula between external Fingers III 2 – 1 – IV, and presence of glands in fringes between fingers. This combination of characters is unique among all the known species of Hyalinobatrachium and is only found in those specimens identified by Ayarzagüena (1992), Señaris and Ayarzagüena (2005), Kok and Castroviejo-Fisher (2008), and Kok and Kalamandeen (2008) as H. taylori ( Fig. 10 B–D). Furthermore, we have identified three specimens from French Guiana ( Fig. 10 C–D, Appendix I) that show a phenotype concordant with that of H. taylori . All of these specimens for whom the character could be observed, show green bones in life. The coloration patterns observed in life specimens from Guyana, French Guiana, and Venezuela clearly allows distinction from any other species observed in the area. It shows green bones in life, dark green dorsal surfaces with small clear green areas and white flecks due to concentration of iridiophores, partially transparent pericardium, and metallic lavender iris with dark brown reticulations and a few bronze punctuations ( Fig. 10 B–D). Also, males call exclusively from the upper side of leaves while in all other species but H. kawense sp. nov. males call predominantly from the underside of leaves.

Two paratypes of Hyalinobatrachium taylori (RMNH 11473–4) show a more robust appearance, snout truncated in dorsal and lateral view, transparent pericardium (dissected in both), dorsal coloration cream, webbing formula between external Fingers III 2 – 2 IV, and absence of glands in fringes between fingers. This combination of characters corresponds to the one exhibited by the holotype of H. cappellei (see above and Fig. 4 A); accordingly we assign RMNH 11473–4 to this species. Also, specimens from French Guiana ( Fig. 4 C–F, H) and Suriname, identified by Lescure (1975), Hoogmoed and Avila-Pires (1990), and Lescure and Marty (2000) as Hyalinobatrachium taylori , and those from Guyana referred to as H. sp2 by Ernst et al. (2005) and as H. aff. ignioculus by Guayasamin et al. (2008a) (see specimens under H. cappellei in the Appendix I) share with the holotype of H. cappellei all of the morphological characters studied.

Finally, the two other paratypes (BM 1939.1.1.64, RMNH 11472) have a snout round dorsal and lateral view, white pericardium (dissected in both), dorsal coloration cream, and hand webbing formula III 2 – 1 IV. These specimens plus four from French Guiana and one from Suriname share all of the studied morphological characters with Hyalinobatrachium mondolfii ( Fig. 8 ); thus we assigned them to this species.

We have detected a genetic gap between the populations of Hyalinobatrachium taylori (sensu this work) of Gran Sabana in Venezuela and the ones from French Guiana (genetic distance = 3 %). If these two populations represent different species, most likely the ones from the lowlands ( Guyana and French Guiana) would correspond to H. taylori while the ones from the uplands and highlands of Venezuela would need a name. However, our sample size is small (N = 4) and we miss sequences from intermediate localities ( Guyana) so we cannot exclude that processes like isolation by distance could be causing the observed pattern.

Hyalinobatrachium taylori is unique among species belonging to the same genus because has bones green in life, an iris grey with black reticulation, dorsum dark green, and males only call from the upper side of leaves. These characters are shared with species like Vitreorana antisthenesi , Teratohyla pulverata , and T. amelie and led Señaris and Ayarzagüena (2005) to place H. taylori outside the Hyalinobatrachium fleischmanni Group ( Ruiz-Carranza & Lynch 1991, 1998). Guayasamin et al. (2008a, 2009) conducted phylogenetic analyses of six genetic markers and showed that H. taylori clusters within the diversity of Hyalinobatrachium species previously assigned to the fleischmanni Group.

Biology and tadpole. Señaris and Ayarzagüena (2005) described the position of calling males, number of eggs per clutch, advertisement call, and tadpole. Field observations by SCF, MB, and P. Kok ( Venezuela, French Guiana, and Guyana respectively) confirm these observations.

Ecology and distribution. Normally uses the high strata of vegetation surrounding streams for reproduction (2–30 m over the water). Endemic to the Guiana Shield, it has a wide distribution from the top of western tepuys to the eastern GS (200–2000 m). It has been found in French Guiana, Guyana, and Venezuela. Most likely occurs in Suriname (see Noonan & Bonett 2003 for a discussion about the type locality) and adjacent Brazil.

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.

FIGURES 4. Adult males of Hyalinobatrachium cappellei, resurrected in this work from synonymy with H. fleischmanni. Note the variability in pupil and pericardium coloration. Specimens from French Guiana and Suriname were previously identified as H. taylori. Specimens from Guyana and Venezuela were previously identified as H. crurifasciatum, H. eccentricum, or H. ignioculus. In this work we consider these three species junior synonyms of H. cappellei (see Appendix I for previous identifications). (A) Holotype, SVL = 21.6 mm; (B) RMNH 37850, SVL = 23.6 mm; (C) MNHN 2011.0109, SVL = 25.0 mm; (D) MNHN 2011.0108, SVL = 25.0 mm; (E, H) MTD 48146, SVL = 24.0 mm; (F) MTD 48140, SVL = 24.0 mm; (G, J) MHNLS 17327, SVL = 21.0 mm; (I) MHNLS 17135, SVL = 20.3 mm; (K) MHNLS 17328, SVL = 21.7 mm; (L) MHNLS 17335, SVL = 22.3 mm. Photographs by SCF (A – B, G, I – J) and MB (C – F, H).

FIGURES 8. Adult males of Hyalinobatrachium mondolfii. (A) Topotype, MHNLS 17122, SVL = 22.2 mm; (B) MNHN 2011.0126, SVL = 23.0 mm; (C) MTD 48148, SVL = 22.0 mm; (D, E) SMNS 12255, SVL = 20.7 mm; (F) egg clutch on the underside of a leaf. Photographs by SCF (A), MB (B – C, F) and RE (D – E).

FIGURE 10. Adult males of Hyalinobatrachium taylori. (A) Holotype, BMNH 1939.1. 1.65, SVL = 19.0 mm; (B) IRSNB 13987, SVL = 19.0 mm; (C, D) MNHN 2011.0112; SVL = 21.0 mm. Photographs by PK (A – B) and MB (C – D).