Hyalinobatrachium yaku, Guayasamin, Juan M., Cisneros-Heredia, Diego F., Maynard, Ross J., Lynch, Ryan L., Culebras, Jaime & Hamilton, Paul S., 2017
Guayasamin, Juan M., Cisneros-Heredia, Diego F., Maynard, Ross J., Lynch, Ryan L., Culebras, Jaime & Hamilton, Paul S., 2017, A marvelous new glassfrog (Centrolenidae, Hyalinobatrachium) from Amazonian Ecuador, ZooKeys 673, pp. 1-20: 3-7
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Hyalinobatrachium yaku sp. n.
MZUTI 5001 (Fig. 1), adult male collected from a stream affluent of the Kallana river (1.4696°S, 77.2784°W, 325 m), nearby the Kichwa community of Kallana, province of Pastaza, Ecuador, collected by JC and Carlos Morochz on 15 April 2016.
MZUTI 5002, adult male, same locality and collection data as holotype.
QCAZ 55628 (Fig. 1), adult male, QCAZ 53352, immature male, and QCAZ 53354, 56664, juveniles, all from Timburi-Cocha Research Station (0.4800°S, 77.2829°W, 300 m) near San José de Payamino, province of Orellana, Ecuador, collected by RJM, PSH, and RLL on June 2012. ZSFQ 02322, adult female from Ahuano (1.0632°S, 77.5265°W, 360 m), province of Napo, Ecuador, collected by DFCH and Jean-Marc Touzet on 5 April 1998.
The new species is placed in the genus Hyalinobatrachium (Ruiz-Carranza & 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; and (5) males call from the undersides of leaves. All the aforementioned characteristics are shared by the new species. Additionally, analyses of three mitochondrial genes place the new species as a close relative of other Hyalinobatrachium species (Fig. 2); thus, generic placement in Hyalinobatrachium is unambiguous.
The following combination of characters can distinguish Hyalinobatrachium yaku from other glassfrogs: (1) dentigerous process of the vomer lacking teeth; (2) snout truncate in dorsal and lateral views; (3) lower half of tympanic annulus visible; tympanic membrane clearly differentiated and with coloration similar to that of surrounding skin; (4) dorsal skin shagreen; (5) ventral skin areolate; cloacal area glandular, with one tubercular slightly enameled patch on each side of the cloaca, paired round tubercles below vent absent; (6) parietal peritoneum, pericardium, kidneys and urinary bladder transparent (lacking iridophores); hepatic, gastrointestinal, and testicular peritonea covered by iridophores; (7) liver bulbous; (8) humeral spines absent; (9) basal webbing between Fingers I and II, moderate webbing between external fingers; hand webbing formula: I 2 - 2 II 0+ - 3+ III 2- - (1-2-) IV; (10) foot webbing moderate; webbing formula: I (1-1+) - (2-2-) II (0+-1) - (2+-21/3) III 1 - 21/3 IV 21/3 - (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 edge 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 2.1 times wider than disc on Finger III; (15) coloration in life: dorsal surfaces apple green to yellowish green with small yellow spots and minute gray to black melanophores; posterior head and anterior half of the body with few small, well-defined dark green spots placed middorsally; bones white; (16) coloration in preservative: dorsal surfaces pale cream with minute lavender to black melanophores; (17) iris coloration in life: silver to yellow, with minute dark spots that are concentrated around pupil, giving impression of a diffuse ring; (18) melanophores present on Finger IV and Toes IV–V, absent on other fingers and toes; in life, hands and feet are cream with a light green hue, with tips of fingers and toes being yellowish green; (19) males call from the undersides of leaves; advertisement call consisting of a single tonal note; call duration note 0.27-0.4 s, dominant frequency 5219-5330 Hz, with no frequency modulation; (20) males attend egg clutches located on the underside of leaves overhanging streams, clutch size unknown; (21) SVL in adult males 20.8-22.3 mm (n = 3), in adult female 21.1 mm (n = 1); (22) enameled glands absent from sides of head.
Comparisons with similar species.
Many species of Hyalinobatrachium are difficult to diagnose using only morphological or chromatic characters ( Castroviejo-Fisher et al. 2009; 2011); however the new species is diagnosable in life due to the presence of two unusual coloration traits: (i) the presence of middorsal dark green spots on the anterior half of the body (Fig. 1), and (ii) a completely exposed heart (parietal peritoneum and pericardium transparent). Only two other glassfrog species share, to some degree, these traits, the Central American H. talamancae and H. vireovittatum . However, phylogenetically, the new species is not closely related to H. talamancae nor H. vireovittatum . Also, the new species is easily distinguished by having a row of dark green middorsal spots (continuous middorsal line in H. talamancae and H. vireovittatum ). Furthermore, they have a very disjunct distribution ( H. talamancae and H. vireovittatum are found in Central America, whereas H. yaku inhabits the Amazonian lowlands). No Amazonian glassfrog has a dorsal pattern similar to the new species. Hyalinobatrachium munozorum and H. ruedai are sympatric with H. yaku , but they are distinguished by having white or mostly white pericardium (transparent in H. yaku ), dorsal melanophores as punctuations of different sizes (uniform-sized in H. yaku ), snout rounded in lateral view (truncate in H. yaku ) and by lacking the row of dark green middorsal spots of H. yaku . Hyalinobatrachium anachoretus is morphologically similar to H. yaku but differs by lacking the midddorsal dark green spots, and by its call with a lower dominant frequency (4670-4800 Hz versus 5219.3-5329.6 in H. yaku ). The most closely related species to H. yaku is H. pellucidum (Fig. 3); the two species differ by their call (Table 1) and dorsal color pattern (middorsal dark green spots present in H. yaku and absent in H. pellucidum ; Figs 1, 3).
Description of the holotype.
Adult male (MZUTI 5001) with SVL 20.8 mm. Head just wider than body; head width 37% of SVL; head width 1.07 times head length; head relatively short (Head length = 34% of SVL). Snout truncate in dorsal and lateral views. Loreal region slightly concave, nostrils slightly protuberant, elliptical; internarial region concave anterodorsally; canthus rostralis not well defined. Eyes small (eye diameter 12% of SVL), directed anterolaterally, eyes about 45° relative to midline. Tympanum with conspicuous dorsal inclination. Posterior half of tympanic annulus visible; tympanic membrane differentiated, pigmented as surrounding skin. Dentigerous processes on vomers lacking teeth, choanae large, circular; tongue oval, white in preservative, anterior 3/4 attached to mouth; vocal slits present, extending along floor of mouth lateral to tongue; enameled glands absent on sides of head. Ulnar fold present, but low and with very thin layer of iridophores. Relative length of fingers: I < II < IV < III; finger discs rounded, wider than toe discs; disc on Finger III 48% of eye diameter; basal finger webbing between Fingers I and II, moderate webbing between external fingers; hand webbing formula I 2 - 2 II 0+ - 3+ III 2- - 2- IV. Prepollex concealed; subarticular tubercles round, low; supernumerary tubercles absent, palmar tubercle round and small, thenar tubercle ovoid; nuptial excrescences present as a small pad on proximomedial edge of Finger I (Type V). Hind limbs slender, tibia length 59% of SVL; tarsal fold present, but low and with very thin layer of iridophores enameled; discs of toes small, round, inner metatarsal tubercle oval, small; outer metatarsal round, but very difficult to distinguish. Foot webbing moderate; webbing formula: I 1+ - 2 II 1 - 2+ III 1 - 21/3 IV 21/3 - 11/3 V. In preservative, dorsal skin peppered with small dark melanophores; dorsal skin shagreen; skin on venter areolate; cloacal opening at level of upper thighs, cloacal ornamentation present as an enameled cloacal fold and small tubercles covered with thin layer of iridophores. Parietal peritoneum and pericardium transparent, urinary bladder lacking iridophores, liver and viscera covered by iridophores; liver bulbous.
Coloration in life.
In adults, dorsum apple green to yellowish green with small yellow spots and minute gray to black melanophores; posterior head and anterior half of the body with few small, well-defined dark green spots placed middorsally; the anterior-most spot generally being the largest. Hands and feet are cream with a light green hue, with tips of fingers and toes being yellowish green; melanophores absent from fingers and toes, except Finger IV and Toes IV and V. Ventrally, parietal peritoneum and pericardium transparent, with red heart fully visible; visceral peritoneum of gall bladder and urinary bladder transparent; hepatic and visceral peritonea white. Ventral vein red. Iris silver to yellow, with minute dark spots that encircle the pupil, giving the impression of diffuse rings. Bones white.
Coloration in preservative.
Dorsal surfaces cream dotted with minute dark lavender to black melanophores; venter uniform white; peritonea as in life. Iris white with lavender melanophores that become more numerous near the pupil. There are no traces of the characteristic middorsal dark green spots in preserved specimens.
Measurements of the type series are shown in Table 2.
The other male from the type locality (MZUTI 5002) has more foot webbing (I 1 - 2- II 0+ - 2+ III 1 - 21/3 IV 21/3 - 1 V) than the holotype. Juveniles have the same color pattern as adults, but the number and extent of the middorsal green dots varies, but they are usually smaller and less pronounced posteriorly (Fig. 4).
The description is based on a series of ten calls emitted by the holotype and recorded by JC. The advertisement call of Hyalinobatrachium yaku is a single and high pitched tonal note (Fig. 5). Neither frequency nor amplitude modulation was observed. The call lasts 0.27-0.4 s (0.3 ± 0.03) and has an average call rate of 9.0 calls /minute. Time between calls varied from 5.3-8.9 s (7.1 ± 1.1). The dominant frequency, which is included in the fundamental frequency, ranges from 5219.3-5329.6 Hz (5283.8 ± 35.0). The frequency band has a lower frequency of 5207.3-5314.8 Hz (5264.6 ± 34.6) and an upper frequency of 5236.5-5340.5 Hz (5299.1 ± 34.1).
At Kallana, the holotype and one paratype (MZUTI 5002) were found calling from the underside of leaves of riverine vegetation in pristine forest. The holotype was on the same leaf as two egg clutches, approximately 3 m above the stream. The paratype was also calling from the underside of a leaf nearly 6 m above water. The stream itself was slow-flowing, relatively narrow (approximately 3 m wide), and with depths no greater than 100 cm. Syntopic species at Kallana are: Nymphargus mariae , Teratohyla midas , Agalychnis hulli , Phyllomedusa tomopterna , Hypsiboas calcaratus , H. geographicus , Osteocephalus fuscifacies , Pristimantis enigmaticus , and P. peruvianus .
At Ahuano, the single individual was found on the underside of a leaf at 1 m above water in riverine vegetation along a small stream, tributary of the Arajuno River. The stream was slow-flowing, very narrow (approximately 1m wide), and shallow (approxi mately 40 cm deep). The area was covered by secondary forests. At Ahuano, Hyalinobatrachium yaku was found in syntopy with Teratohyla midas and H. ruedai ( Cisneros-Heredia and McDiarmid 2006b).
Unlike individuals found at Kallana and Ahuano, individuals from San José de Payamino were found perched on leaves of small shrubs, ferns, and grasses (30-150 cm above ground) in disturbed secondary forest. All but one individual were found within a relatively small area near the Timburi Cocha Research Station bordering the Payamino River, with the additional individual found in slightly more mature secondary growth 50 m east of a dirt road situated approximately 1.5 km west of the research station (see Maynard et al. 2016). Additionally, all individuals recorded at San José de Payamino were found >30 m from any stream. Due to this unusual circumstance, syntopic species associated with H. yaku at San José de Payamino is rather extensive, as amphibian diversity in secondary forest at this site is high ( Maynard et al. 2016). Syntopic glassfrog species include: Cochranella resplendens , Hyalinobatrachium munozorum , and Teratohyla midas . Other sympatric amphibian species include: Allobates femoralis (complex), Hyloxalus sauli , Rhaebo ecuadorensis , Rhinella margaritifera , R. marina , Dendropsophus marmoratus , Hypsiboas boans , H. cinerascens , H. geographicus , H. punctatus , Nyctimantis rugiceps , Osteocephalus buckleyi , O. mutabor , Osteocephalus sp., Phyllomedusa tarsius , P. vaillantii , Scinax garbei , S. ruber , Hypodactylus nigrovittatus , Pristimantis acuminatus , P. altamazonicus , P. conspicillatus , P. croceoinguinis , P. delius , P. diadematus , P. kichwarum , P. lanthanites , P. librarius , P. variabilis , P. aff. martiae , Adenomera andreae , Engystomops petersi , Leptodactylus wagneri , Lithodytes lineatus , Chiasmocleis bassleri , Bolitoglossa peruviana .
Hyalinobatrachium yaku is only known from three localities on the Amazonian lowlands of Ecuador at elevations between 300-360 m. The two most-distant sites, Kallana in province of Pastaza, and San José de Payamino in province of Orellana, are approximately 110 km from one another, while Ahuano, province of Napo, is midway between them (Fig. 6). Given the geographic distance between the localities where the new species has been found, it is likely that H. yaku has a broader distribution, including areas in nearby Peru.
All inferred phylogenetic trees show that Hyalinobatrachium yaku and H. pellucidum are sister species (Fig. 2). Trees obtained for each mitochondrial gene trees are congruent with the tree shown in Figure 2.
The specific epithet yaku is the Kichwa word for water. Water, in the form of streams, is fundamental for the reproductive biology of all glassfrogs. Water pollution, mainly through oil and mining activities, represents one of the biggest threats for Amazonian amphibians, as well as for numerous other water-dependent species.
Given that Hyalinobatrachium species are morphologically conserved and that many distinctive color traits are lost in preserved specimens (i.e., dorsal green spots), finding new records of H. yaku in herpetological collections is challenging. Also, many species of the genus are arboreal and difficult to find in nature, but this scarcity does not necessarily mean that the species have low abundances. Available information is insufficient to suggest an evaluation following IUCN criteria, thus we suggest that H. yaku is a Data Deficient species.
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