Hyalinobatrachium adespinosai, Guayasamin & Vieira & Glor & Hutter, 2019

Guayasamin, Juan M., Vieira, José, Glor, Richard E. & Hutter, Carl R., 2019, A new glassfrog (Centrolenidae: Hyalinobatrachium) from the Topo River Basin, Amazonian slopes of the Andes of Ecuador, Amphibian & Reptile Conservation (e 194) 13 (2), pp. 133-144 : 135-139

Hyalinobatrachium adespinosai new species

urn:lsid:zoobank.org:act:46C6CBB4-ECE3-470E-A15C-4BB36A3301DE

Suggested English name: Adela’s Glassfrog

Suggested Spanish name: Rana de Cristal de Adela

Holotype. ZSFQ 1648 (JMG 583, Fig. 2 ), adult male from riverine vegetation along the San Jacinto River (1.3447°S, 78.1814°W; 1,795 m asl), Tungurahua Province, Ecuador, collected by CRH, REG, and KC on 4 August 2017.

Paratypes. ZSFQ 1650–52 , 1647 , adult males with same data as holotype .

Generic placement. The new species is placed in the genus Hyalinobatrachium ( Ruiz-Carranza and Lynch, 1991, as modified by Guayasamin et al. 2009) on the basis of morphological and molecular data. The main diagnostic phenotypic traits of Hyalinobatrachium are: (1) ventral parietal peritoneum completely transparent; (2) digestive tract and bulbous liver covered by iridophores; (3) humeral spines absent; (4) white bones in life; (5) males call from the underside of leaves; (6) females place the eggs on the underside of leaves; and (7) males provide extended parental care. All the aforementioned characteristics are shared by the new species. Additionally, analyses of the mitochondrial 16S gene place the new species as a close relative of other Hyalinobatrachium species ( Fig. 1 ); thus, generic placement in Hyalinobatrachium is unambiguous.

Diagnosis. Within the genus Hyalinobatrachium , the new species is diagnosable mainly by having a transparent pericardium. However, the new species is morphologically cryptic with three closely related taxa ( H. anachoretus , H. pellucidum , H. esmeralda ). Based on comparisons with specimens examined (see Appendix 1), all these species display a similar size and color pattern (pale green dorsum with yellow dots and a transparent venter and pericardium; red heart visible ventrally). However, calls between species diverge noticeably; the major difference is the structure of the call, with two species ( H. adespinosai sp. nov. and H. anachoretus ) having pulsed calls and the others having tonal vocalizations ( Fig. 3 ; Table 1). The call of H. adespinosai sp. nov. is further differentiated from that of H. anachoretus by being longer, having more pulses per note, and being produced at a higher rate (Table 1). Toe webbing (Toe IV) is less extensive in the new species (21/3 IV 2 +) than in H. anachoretus (1 + IV 1 +; Twomey et al. 2014). Additionally, the new species and H. anachoretus are separated by considerable distance (airline distance = 473 km), including one of the most important biogeographic barriers in South America, the Marañon valley (see Duellman 1999; Winger and Bater 2015 and references therein). Uncorrected p genetic distances for the mitochondrial gene 16S between H. adespinosai sp. nov. and its closest relatives are summarized in Table 2 .

Characterization. The following combination of characters is found in Hyalinobatrachium adespinosai sp. nov.: (1) dentigerous process of the vomer lacking teeth; (2) snout truncate in dorsal and lateral views; (3) tympanum barely visible, hidden under skin, with coloration similar to that of surrounding skin; (4) dorsal skin shagreen; (5) ventral skin areolate; cloacal ornamentation absent, paired round tubercles below vent absent; (6) parietal peritoneum transparent; pericardium with thin layer of iridophores (in life, a red heart is mostly visible ventrally); liver, viscera, and testes covered by iridophores; (7) liver bulbous; (8) humeral spines absent; (9) hand webbing formula: I (2–3) — (2–2 +) II (1–1 +) — 31/3 III (2–2 +) — (2 –– 2) IV; (10) foot webbing moderate; webbing formula: I 1— (12/3 –2 –) II (1–1 –) — (2 ––21/3) III (1–1 +) —(2 + – 21/3) IV 2 + — (1 + – 11/3) V; (11) fingers and toes with thin lateral fringes; ulnar and tarsal folds present, but low and difficult to distinguish, with thin layer of iridophores that extends to ventrolateral edges of Finger IV and Toe V; (12) nuptial excrescence present as a small pad on Finger I (Type V), prepollex not enlarged; prepollical spine not projecting (spine not exposed); (13) when appressed, Finger I longer than II; (14) diameter of eye about two times wider than disc on Finger III; (15) coloration in life: dorsal surfaces pale yellowish green with small pale yellow spots and minute gray to black melanophores; bones white; (16) coloration in preservative: dorsal surfaces pale cream with minute melanophores; (17) iris coloration in life: white with pale yellow hue and numerous minute lavender spots; (18) melanophores absent from most fingers and toes, but present on Finger IV and Toes IV and V; (19) males call from underside of leaves; advertisement call consisting of single note, distinctly pulsed (9–13 pulses per call), with duration of 0.382 –0.430 s, and dominant frequency at 4,645 –5,001 Hz; (20) males attend egg clutches located on the underside of leaves overhanging streams; clutch size of 22 embryos (n = 1); (21) SVL in adult males 20.5–22.2 mm (n = 3), females unknown; and (22) enameled tubercles absent from sides of head.

Description of the holotype. ZSFQ 1648, adult male with SVL 22.2 mm. Head wider than long (head width 38% of SVL; head length 77% of head width). Snout truncate in dorsal and lateral views. Loreal region flat and nearly vertical, nostrils slightly protuberant, elliptical; internarial region concave anterodorsally; canthus rostralis well defined. Eyes small, directed anterolaterally, eyes about 45° relative to midline (where anterior-facing eyes would be 90° relative to midline). Tympanum annulus barely visible through the skin; tympanic membrane differentiated and pigmented as surrounding skin. Dentigerous processes on vomers absent; choanae large, oval, separated widely (distance about the same as between nostrils); tongue round, white in preservative, anterior 4/5 attached to mouth; vocal slits present, extending along floor of mouth lateral to tongue; enameled glands absent from lower part of upper jaw. Ulnar fold present, with a thin layer of iridophores, and continuing along the external edge of Finger IV; humeral spine absent. Relative lengths of fingers: I < II < IV < III; finger discs rounded, about the same size as discs on toes, disc on Finger III 54% of eye width; finger webbing reduced between Fingers I– III, moderate between Fingers III and IV, with formula I 3—2 + II 1 + — 31/3 III 2 — 2 IV. Prepollex concealed; subarticular tubercles round, faint; few small supernumerary tubercles present, palmar tubercle round and small, thenar tubercle ovoid; nuptial excrescences present as a small pad on external edge of Finger I (Type V). Hind limbs slender, tibia length 58% of SVL; tarsal fold present, with thin layer of iridophores; discs of toes round, inner metatarsal tubercle small; outer metatarsal tubercle round, but very difficult to distinguish. Webbing formula of feet: I 1— 2 – II 1— 21/3 III 1 + — 21/3 IV —2 + — 1 V. In preservative, dorsal skin peppered with small dark lavender melanophores; dorsal skin shagreen; skin on venter areolate; cloacal opening at level of upper thighs, cloacal ornamentation present as a lightly enameled cloacal fold and small tubercles. Parietal peritoneum transparent; pericardium with a very thin layer of iridophores that, in life, exposes a red heart; urinary bladder lacking iridophores; liver, viscera, and testes fully covered by iridophores. Kidneys rounded, approximately bean-shaped; liver bulbous.

Coloration in life. Dorsal surfaces apple green to yellowish green with diffuse yellow spots and minute gray to black melanophores. Melanophores absent from fingers and toes, except Finger IV and Toes IV and V. Ventrally, parietal peritoneum and pericardium transparent, with a red heart always visible, even when a very thin layer of iridophores is present on the pericardium of some individuals. Visceral peritoneum of gall bladder and urinary bladder transparent; hepatic and visceral peritonea white; ventral vein red. Iris pale yellowish white, with numerous minute lavender spots. Bones white.

Coloration in preservative. Dorsal surfaces cream, dotted with minute dark lavender melanophores; venter uniform cream; visceral peritoneum lacking iridophores; pericardium with a very thin layer of iridophores. Iris silvery white with minute lavender melanophores.

Measurements. Measurements of the type series are shown in Table 3 .

Variation. Variation in hand webbing is as follows: I (2–3) — (2–2 +) II (1–1 +) — 31/3 III (2–2 +) — (2 –– 2) IV. Foot webbing variation is as follows: I 1— (12/3 –2 –) II (1–1 –) —(2 ––21/3) III (1–1 +) —(2 + – 21/3) IV 2 + — (1 + – 11/3) V.

Vocalizations ( Fig. 3 ). The description is based on recordings from nine individuals (Codes LBE-C: 048– 057). The call of Hyalinobatrachium adespinosai sp. nov. has a striking resemblance to the chirp of a cricket, and was often confused for one in the field. Each call is composed of a single and high-pitched pulsed note, and has a duration of 0.38– 0.44 s (x = 0.38 ± 0.017). Time between calls varied from 2.0– 11.0 s (x = 4.58 ± 2.3). The fundamental frequency, the same as the dominant frequency, is at 4,645 –5,203 Hz (x = 4,855 ± 152). There is no frequency modulation. The first harmonic is at 9,336 –9,754 Hz and the second harmonic is at 14,159 – 14,444 Hz.

Ecology. All individuals of the new species were found on the underside of leaves of riverine vegetation along the San Jacinto River. The section of river was fast-flowing and had visible rapids. Although the population is locally abundant (as heard from numerous advertisement calls), individuals are very difficult to observe because they are usually found at the canopy level (4–16 m above ground level). The type series consists of males exclusively; they were calling in the months of July and August. One male ( ZSFQ 1648) was apparently guarding an egg clutch containing 22 embryos; both the adult male and the egg clutch were on the same leaf most of the time, but the male also moved to nearby leaves ( Fig. 4 ).

Distribution. Hyalinobatrachium adespinosai sp. nov. is only known from the type locality: San Jacinto River (1.3447°S, 78.1814°W; 1,795 m asl), Tungurahua Province, Ecuador ( Fig. 5 ).

Evolutionary relationships. The phylogenetic analyses recover Hyalinobatrachium adespinosai sp. nov. haplotypes as sister to haplotypes sampled from H. anachoretus and nested within other members of a monophyletic clade comprised of all other sampled species of Hyalinobatrachium ( Fig. 1 ). The most closely related species to H. adespinosai sp. nov. share several morphological traits, including a red heart exposed ventrally ( H. adespinosai + H. anachoretus + H. pellucidum + H. yaku ).

Table 1. Comparison among calls of closely related species of Hyalinobatrachium . The calls of all species were recorded at the corresponding type locality, except for that of H. esmeralda.

Call data were obtained from the following sources: H. anachoretus from Twomey et al. (2014), H. esmeralda from Acosta-Galvis (2017), and H. yaku from Guayasamin et al. (2017).

Etymology. The specific epithet adespinosai honors Adela Espinosa, an Ecuadorian conservationist and board member of the Jocotoco Foundation (http:// www.jocotoco.org). Adela’s work has focused on the conservation of species and ecosystems. The new glassfrog described here is found only within the limits of a natural reserve owned by Adela and her husband, Antonio Páez. We are delighted to recognize Adela’s devotion to nature with this marvelous species.

Conservation status. Available information is insufficient to fully assess the conservation status of Hyalinobatrachium adespinosai sp. nov. Therefore, following IUCN criteria, this species is considered as Data Deficient. The herpetological museums that house specimens collected near the type locality (Topo basin) were consulted, but there were no additional specimens of the new species. Although this might suggest a conservation category other than Data Deficient, we actually prefer to maintain this status because the new species is very difficult to find (i.e., a canopy specialist). Therefore, in this case, absence in nearby localities where herpetological surveys have been carried out does not necessarily indicate a true absence of the species.

Figures

Fig. 2. Hyalinobatrachium adespinosai sp. nov. in life, holotype.

Fig. 1. Phylogenetic relationships of Hyalinobatrachium inferred from the 16S mitochondrial gene under ML criteria.All sequences were downloaded from GenBank, except for those of the new species. GenBank codes are listed next to each terminal.Associated locality data is available at GenBank, as well as in Guayasamin et al. (2008), Castroviejo-Fisher et al. (2014), and Twomey et al. (2014).

Fig. 3. Call of Hyalinobatrachium adespinosai sp. nov., holotype, recorded in field conditions at the type locality. Air temperature: 18 °C.

Fig. 4. Natural history and in-situ photographs of the new species. (A) Adult male of Hyalinobatrachium adespinosai near his egg clutch; other males were observed on the same leaf as the egg clutch. (B) Close-up of the egg clutch. (C) Spider predation on an unattended egg clutch.

Fig. 5. Distribution of Hyalinobatrachium adespinosai sp. nov. in Ecuador.