Hyalinobatrachium nouns, Guayasamin & Brunner & Valencia-Aguilar & Franco-Mena & Ringler & Medina Armijos & Morochz & Bustamante & Maynard & Culebras, 2022

Guayasamin, Juan M., Brunner, Rebecca M., Valencia-Aguilar, Anyelet, Franco-Mena, Daniela, Ringler, Eva, Medina Armijos, Anderson, Morochz, Carlos, Bustamante, Lucas, Maynard, Ross J. & Culebras, Jaime, 2022, Two new glassfrogs (Centrolenidae: Hyalinobatrachium) from Ecuador, with comments on the endangered biodiversity of the Andes, PeerJ 10, pp. 1-34 : 19-23

Hyalinobatrachium nouns new species

LSID: 1A908651-9A82-4DCA-9960-E8DC525F5ADF

Suggested English name: Nouns’ Glassfrog

Suggested Spanish name: Rana de Cristal de Nouns

Holotype. MZUTI 3299 , adult male from stream in Bosque Protector Los Cedros (0.310 N, 78.781 W; 1,420 m a.s.l.), Cordillera de Toisán , Imbabura Province, Ecuador, collected by Mariela Palacios, Jaime Culebras and Juan M. Guayasamin, on 12 March 2012.

Paratypes. CJ7703 , adult male from stream in Bosque Protector Los Cedros (0.30241 N, 78.78558 W; 1,229 m a.s.l.), Cordillera de Toisán, Imbabura Province, Ecuador, collected by Morley Read and Arturo Guasti on 8 November 2017. CJ7722 , adult male from stream in Bosque Protector Los Cedros (0.30191 N, 78.78513 W; 1,241 m a.s.l.), Cordillera de Toisán , Imbabura province, Ecuador, collected by Morley Read and Arturo Guasti on November 11 th 2017. CJ7723 , adult male from stream in Bosque Protector Los Cedros (0.30302 N, 78.78674 W; 1,313 m a.s.l.), Cordillera de Toisán , Imbabura province, Ecuador, collected by Morley Read and Arturo Guasti on November 11 th 2017. ZSFQ-0537 , adult male from stream in Río Manduriacu Reserve (0.31126 N, 78.8588 W; 1,254 m a.s.l.), Cordillera de Toisán , Imbabura province, Ecuador, collected by José Vieira, Scott Trageser, and Ross J. Maynard on 10 February 2018. ZSFQ-3906 , metamorph from stream in Río Manduriacu Reserve (0.3099 N, 78.8567 W; 1,202 m a.s.l.), Cordillera de Toisán , Imbabura province, Ecuador, collected by Ross J. Maynard and Jaime Culebras on 23 November 2019.

Generic placement. Based of morphological and molecular data, the new species is placed in the genus Hyalinobatrachium sensu Ruiz-Carranza & Lynch , as modified by Guayasamin et al. (2009). The molecular phylogeny ( Fig. 2 ) places the new species within the genus Hyalinobatrachium with high confidence. Phenotypically, Hyalinobatrachium nouns sp. nov. shares the following diagnostic traits of the genus Hyalinobatrachium : (1) completely transparent ventral parietal peritoneum; (2) digestive tract and bulbous liver are covered by iridophores; (3) absent humeral spines; (4) white bones in life; (5) males call from the undersides of leaves, (6) females place the eggs on the undersides of leaves; (7) males provide extended parental care; and (8) tympanum with an orientation that places it almost on a horizontal plane (instead of a more lateral plane as observed in other glassfrog genera). All the aforementioned characteristics are present in Hyalinobatrachium nouns sp. nov. We note that we have observed males on the same leaves as egg clutches for consecutive days, suggesting the possibility of parental care, but additional studies are necessary to confirm that these observations actually represent extended paternal care as observed in other Hyalinobatrachium species (see Delia, Bravo-Valencia & Warkentin, 2017).

Diagnosis. Hyalinobatrachium nouns sp. nov. is distinguished from other species in the genus mainly by its dorsal coloration (i.e., head with light yellow spots that may form an interorbital bar; dorsum lime green with small light yellow spots) and by its transparent pericardium. Hyalinobatrachium nouns sp. nov. is most similar to H. aureoguttatum , H. mashpi sp. nov., H. talamancae , H. valerioi , and H. vireovittatum . Differences among these species are indicated in Table 1 and Figs. 2–4 . The new species is morphologically cryptic with Hyalinobatrachium mashpi sp. nov. (described above), but they exhibit a considerable genetic distance (16S; 4.6–4.7%), which is remarkable given that they are found at relatively close geographic proximity (straight distance = 18.9 km), but separated by the Intag-Guayllabamba river valley.

Characterization. The following combination of characters are found in Hyalinobatrachium nouns sp. nov.: (1) dentigerous process of the vomer lacking teeth; (2) snout truncate in dorsal view and slightly protruding in lateral view; (3) tympanum oriented almost horizontally; tympanic annulus barely visible, hidden under skin; tympanic membrane differentiated, 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 and pericardium translucent (in life, red heart visible in ventral view); liver, viscera and testes covered by iridophores; (7) liver bulbous; (8) humeral spines absent; (9) hand webbing formula: I (2 + –2)—(2–2 1/2) II (1 + –1 1/2)—(3–3 +) III (2–2 +)—(1 –1 3/4) IV; (10) foot webbing moderate; webbing formula: I (1–1 +)—(2 – –2) II (1–1 +)—(2 + –2 1/2) III 1—(2 + –2 1/3) IV (2 1/4 –2 1/3)—(1 + –1 1/3) V; (11) fingers and toes with thin lateral fringes; ulnar and tarsal folds absent; (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 2 times wider than disc on Finger III; (15) coloration in life: dorsal surfaces lime green with small light yellow spots; (16) coloration in preservative: dorsal surfaces creamish white, with minute lavender melanophores; (17) eye coloration in life: iris yellow to golden-yellow; pupil surrounded by lavender ring; (18) melanophores absent from fingers and toes, except Toes IV and V; (19) males call from underside of leaves; advertisement call unknown; (20) parental care unknown; clutch size unknown; (21) SVL in adult males 19.1–21.3 mm (mean = 20.3; n = 4), females unknown; and (22) enameled tubercles absent from sides of head.

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Description of the holotype. MZUTI 3299, adult male with SVL 19.1 mm. Head wider than long (head width 39% of SVL; head length 80% of head width). Snout truncate in dorsal view and slightly protruding in lateral view. Loreal region concave, nostrils slightly protuberant, elliptical; internarial region concave; canthus rostralis not well defined. Eyes small, directed anterolaterally, eyes about 50 Ǫ relative to midline (where anterior-facing eyes would be 90 Ǫ relative to midline). Tympanum visible, oriented almost horizontally; 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; posterior border of tongue slightly notched; vocal slits present, extending along floor of mouth lateral to tongue; enameled glands absent from lower part of upper jaw. Ulnar fold absent; humeral spine absent. Relative length of fingers: II <I <IV <III; finger discs rounded, about the same size as discs on toes, disc on Finger III 41% of eye width; hand webbing reduced between Fingers I–III, moderate between Fingers III and IV, with formula I 2 + —2 II 1 1/2 —3 + III 2 + —1 3/4 IV. Prepollex concealed; subarticular tubercles round, faint; few small supernumerary tubercles present, palmar tubercle round, of moderate size and difficult to see, thenar tubercle ovoid; nuptial excrescences present as a small pad on external edge of Finger I (Type V). Hind limbs slender, tibia length 59% of SVL; tarsal fold absent; discs of toes round; inner metatarsal tubercle small, outer metatarsal tubercle round, both very difficult to distinguish. Webbing formula of feet: I 1— 2 – II 1—2 1/2 III 1—2 1/3 IV 2 1/4 —1 1/3 V. In preservative, dorsal skin creamish white, with minute dark lavender melanophores (only visible under the stereomicroscope); dorsal skin shagreen; skin on venter areolate; cloacal opening at level of upper thighs, small and non-enameled cloacal warts present. Parietal peritoneum and pericardium translucent (in life, the red heart is visible ventrally); urinary bladder lacking iridophores; liver, viscera, and tested fully covered by iridophores; kidneys rounded, approximately bean-shaped; liver bulbous.

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Coloration in life. Dorsal surfaces apple green to yellowish green with diffuse yellow spots; head with light yellow spots that may form an interorbital bar. Melanophores absent from fingers and toes, except Toes IV and V. Ventrally, parietal peritoneum and pericardium transparent, with a red heart always visible. Gall bladder and urinary bladder covered by translucent peritonea; hepatic and visceral peritonea covered by white iridophores; ventral vein red. Iris yellow, with numerous minute lavender spots. Bones white.

Coloration in preservative. Dorsal surfaces creamish white dotted with minute dark lavender melanophores; venter uniform cream, with partial translucence; pericardium translucent; visceral peritoneum covered by iridophores. Iris white with minute lavender melanophores. Melanophores absent from hands and feet, except from some few present on dorsal surfaces of Toes IV and V.

Measurements of holotype. MZUTI-3299, adult male. SVL = 19.1, femur length = 11.2, tibia length = 11.3, foot length = 8.8, head length = 5.9, head width = 7.4, interorbital distance = 2.2, upper eyelid = 1.5, internarial distance = 1.5, eye diameter = 2.2, tympanum diameter = 0.6, radioulna length = 4.0, hand length = 6.0, Finger I length = 4.4, Finger II length = 3.9, width of disc of Finger III = 0.9.

Natural History. At Bosque Protector Los Cedros, individuals were found on the underside of riparian leaves 1–5 m above stream level during the months of November and March. At Río Manduriacu Reserve, during the rainy season (February), a male was found on the underside of a leaf 6 m above a stream; the male was calling next to an egg clutch. At the same reserve, metamorphs have been found perched on leaves 50–150 cm above streams in October and November.

Distribution. Hyalinobatrachium nouns sp. nov. is only known from Río Manduriacu Reserve and Bosque Protector Los Cedros at elevations of 1,177–1,420 m a.s.l. The reserves are located adjacent to one another and are situated within the Toisán Mountain Range, Imbabura Province, Ecuador ( Fig. 10 ), and protect premontane wet tropical forest and cloud forest ( Fig. 11 ) in an area where illegal deforestation and mining are constant threats (see Discussion).

Evolutionary relationships. Our phylogenetic analyses ( Fig. 2 ) place Hyalinobatrachium nouns sp. nov. as sister to a clade formed by H. mashpi sp. nov. and unidentified haplotypes from the Colombian Andes (MAR 2147, 2222). However, this relationship has low support (bootstrap support = 60). Other closely related taxa are endemic to Central America: H. vireovittatum and H. talamancae ( Fig. 2 ).

Etymology. The specific epithet honors Nouns DAO, a global decentralized autonomous organization (“DAO”) composed of owners of Nouns characters, which are digital art creations that live on the blockchain. The mission of Nouns DAO is to promote and build the Nouns brand throughout the physical and digital world. One of the ways Nouns DAO accomplishes this is by building public works and funding philanthropic projects that support the wonder of nature.

Conservation status. We recommend that Hyalinobatrachium nouns sp. nov. be listed as Endangered, following IUCN (2012) criteria B1ab(iii): extent of occurrence estimated to be less than 5,000 km 2; known to exist at no more than five localities; and continuing decline, observed, inferred or projected, in area, extent, and/or quality of habitat. The main threats for this species are habitat loss and contamination due to cattle ranching, agriculture, and mining activities (see below).

Figures

Figure 2 Phylogenetic position of Hyalinobatrachium mashpi sp. nov. and H. nouns sp. nov. Phy- logenetic relationships of Hyalinobatrachium inferred from the 16S mitochondrial gene under ML cri- terion. All sequences were downloaded from GenBank, except those in red (Material S2). Genbank codes are listed next to each terminal. Associated locality data is available at Genbank, as well as in Guayasamin et al. (2008, 2020), Castroviejo-Fisher et al. (2014), and Twomey, Delia & Castroviejo-Fisher (2014). Full-size DOI: 10.7717/peerj.13109/fig-2

Figure 3 Dorsal and ventral photos of glassfrogs in life. (A) Male of Hyalinobatrachium mashpi sp. nov., CJ11642 (holotype). (B) Gravid female of H. mashpi sp. nov., Mashpi Reserve, Ecuador. (C) Male of H. nouns sp. nov., ZSFQ0537. (D) Male of H. nouns sp. nov., MZUTI3299 (holotype). (E) Male of H. aureoguttatum, Ecuador. (F) Gravid female of H. aureoguttatum, Ecuador. Photos by Jaime Culebras (A, B, D, E, F) and Ross Maynard (C). Full-size DOI: 10.7717/peerj.13109/fig-3

Figure 4 Dorsal and ventral photos of glassfrogs in life. (A, B) Male of Hyalinobatrachium vireovittatum, Costa Rica. (C, D) Male of H. talamancae, Costa Rica. (E, F) Male of H. valerioi, Costa Rica. Photos by Jaime Culebras (A, C, D, E, F) and Josué Alberto Vargas (B). Full-size DOI: 10.7717/peerj.13109/fig-4

Figure 10 Distribution of Hyalinobatrachium mashpi sp. nov. and H. nouns sp. nov. in Ecuador. Note that localities of the two new taxa are separated by the Intag-Guayllabamba valley. Full-size DOI: 10.7717/peerj.13109/fig-10

Figure 11 Habitat of Hyalinobatrachium nouns sp. nov. (A) Tributary of the Manduriacu River, Río Manduriacu Reserve, Imbabura Province, Ecuador. (B) Tributary of the Manduriacu River, Río Manduriacu Reserve, Imbabura Province, Ecuador. (C) Río Manduriacu Reserve, Imbabura Province, Ecuador. (D) Habitat loss in the vicinity of Los Cedros Reserve, Imbabura Province, Ecuador. Photos by Jaime Culebras. Full-size DOI: 10.7717/peerj.13109/fig-11