Boana cinerascens ( Spix, 1824 )

Sturaro, Marcelo José, Costa, João Carlos Lopes, Maciel, Adriano O., Lima-Filho, Geraldo R., Rojas-Runjaic, Fernando J. M., Mejia, Daniela Pareja, Ron, Santiago R. & Peloso, Pedro L. V., 2020, Resolving the taxonomic puzzle of Boana cinerascens (Spix, 1824), with resurrection of Hyla granosa gracilis Melin, 1941 (Anura: Hylidae), Zootaxa 4750 (1), pp. 1-30 : 11-14

Boana cinerascens ( Spix, 1824)

( Figs. 3 , 6–7 )

Hyla cinerascens Spix, 1824: 35 (Syntypes: ZSM 2498/0 [two specimens], type-locality: “Ecgá prope flumen Teffe” (= Tefé, state of Amazonas, Brazil, according to Vanzolini [1981, 1996], both lost, according to Duellman [1977], Hoogmoed & Gruber [1983], and Glaw & Franzen [2006]); Lutz 1951a “1949”: 315; Lutz 1951b “1949”: 331; Duellman 1977: 26; Barrio-Amorós 2004: 13; Glaw & Franzen 2006: 166.

Hyla granosa Boulenger, 1882: 358 (BMNH 1947.2.12.99 [formerly 80.12.5.181] (type-locality: Ecuador: Canelos), according to Condit [1964], designated lectotype by Duellman [1974: 8], restricting the type-locality to Canelos by lectotype designation); Lutz 1951a “1949”: 310; Lutz 1951b “1949”: 326; Hoogmoed, 1979: 5 (partly); Hoogmoed & Gruber (1983): 366; Galatti et al, 2007: 83.

“ Hyla inornata ” (nomen nudum) Lutz 1951a “1949”: 311; Lutz 1951b “1949”: 328.

Hypsiboas cinerascens Duellman et al., 2016 (partly).

Boana cinerascens Dubois, 2017: 28 .

Neotype ( MPEG 40282 , field number PLVP 402 ). An adult male, from Tefé (03°16’47”S and 64°45’09”W), Amazonas, Brazil ( Fig. 10 ), collected by Adriano Oliveira Maciel, Marcelo J. Sturaro and Pedro L. V. Peloso, on January 15, 2017 ( Fig. 6–7 ).

Diagnosis. Based on the molecular phylogenetic analysis, Boana cinerascens should be considered a member of the B. punctata group. Boana cinerascens is defined, morphologically by the following combination of characters: (1) medium sized Boana (SVL males 32.3–37.5, mean 34.9 mm, N = 8); (2) snout truncate in both dorsal and lateral views; (3) skin on dorsum granular; (4) forearm moderately hypertrophied; (5) prepollex small and nonprotruding as a prepollical spine; (6) mental gland present; (7) in life, dorsum green with small yellow spots and numerous reddish-brown dots (melanophores); (8) in preservative, dorsum cream with numerous white spots, and numerous brown and reddish-brown small dots (melanophores); (9) dorsolateral stripe absent; (10) subgular, single vocal sac.

Description of the neotype. An adult male, SVL 32.3 mm. Head wider than long (HW/HL = 1.18), widest at corner of the mouth; snout truncate in both dorsal and lateral views; interorbital distance more than two and a half times the distance between the nostrils (IOD/IND = 2.57) ( Fig. 6A ); eye diameter slightly greater than eye-nostril distance (ED/END = 1.05); canthus rostralis indistinct, rounded in cross-section; nostrils protuberant, nearly elliptical, directed dorsolaterally; internarial area slightly concave, interorbital area flat, loreal area concave. Eyes large and protuberant, directed laterally, larger than tympanum diameter (ED/TD = 1.77); pupil horizontally elliptical; nictitating membrane transparent without any trace of reticulation, its border with brown spots ( Fig. 7A ).

Supratympanic fold present; tympanum small (TD/ED = 0.56), round, completely covered by skin but tympanic annulus evident. Vocal sac subgular, single, extending slightly over the forearms. Choanae small, elliptical, not concealed by palatal shelf, larger than vomerine odontophores; a pair of vomerine odontophores present (four vomerine teeth on right side, six on left side); tongue cordiform, nearly one fourth of posterior end free; vocal slits present, extending diagonally from lateral base of tongue (anterior third) almost to angle of jaw.

Arms robust, moderately hypertrophied; axillary membrane absent ( Fig. 6B ). Lateral margins of arm and forearm with small tubercles, but not forming a fringe; finger tips round; finger disks present on all fingers, disk on FI smallest; relative lengths of fingers I <II <IV <III; subarticular tubercles round, narrower than finger width; subarticular tubercles on FI and FIV of nearly the same size, larger than those of FII and FIII; supernumerary tubercles present; inner metacarpal tubercle flat, elliptical; prepollex small with prepollical spine not protruding out of skin; outer metacarpal tubercle small, heart shaped. Hand webbing between FI and FII absent, present but not extensive between FII–FIII and FIII–FIV. Webbing formula I–II2-–3-III 2½–2+IV on both sides. Details of hand shown in Figure 7B .

Legs long and slender, lacking appendages (e.g. fringes, folds, or tubercles). Ankle without appendices or tubercles. All toes well developed, disks present on all toes, disks on TI and TII smallest; relative lengths of toes I <II <V <III <IV. Subarticular tubercles round; inner metatarsal tubercle flat, slightly elliptical; outer metatarsal tubercle hardly visible, elliptical. Webbing formula: I 2-–2+II1+–2½III1+–3-IV2+–1V on left foot and I2-–2+II1- –2½III1+–3-IV2+–1+V on right foot. Details of foot shown in Figure 7C . Skin on dorsum, head, dorsal surfaces of limbs, flanks, and groin granular; skin on chest, belly and undersurfaces of thigh areolate; oval mental gland; skin on vocal sac granular; skin on ventral parts of fore limb and tibia smooth. Cloacal opening directed posteriorly; cloacal region with tubercles.

Measurements of the neotype (in mm): SVL = 32.3; HL = 11.3; HW = 13.3; ED = 3.9; ELW = 2.4; IOD = 7.2; IND = 2.8; END = 3.7; THL = 18.6; TBL = 16.8; FL = 23.0; TD = 2.2.

Color in preservative. Dorsum cream with white spots, and brown and reddish-brown small melanophores ( Fig. 6A ). Flanks predominantly cream with brown and reddish-brown melanophores on upper region. Inguinal region, anterior, and posterior region of thighs cream. Thigh dorsally cream with white spots and brown and reddish-brown small melanophores; anteriorly and posteriorly cream. Upper arms, forearms, and tibiae dorsally cream with white spots and brown and reddish-brown small melanophores. Gular region cream with light-brown melanophores. Chest and belly translucent cream, with light-brown melanophores and white visceral peritonea covering the organs visible. Ventral surface of forearms and hindlimbs cream with light brown spots. Ventral surface of hands and feet cream ( Fig. 6B ).

Color in life. Dorsum yellowish green with light yellow spots and brown and reddish-brown small melanophores. Flanks predominantly yellow with brown and light yellow blotches and reddish-brown melanophores on upper region. Inguinal region, anterior and posterior region of the thighs light lemon green. Dorsal surface of thighs, forearms, and tibiae same as dorsum ( Fig. 3 ). Gular region, chest and belly translucent light lemon green.

Advertisement call. Calls from one adult male (MPEG 40290) from PNJ, Novo Airão, Amazonas, Brazil (02°18’04”S, 62°28’07”W) and one adult male (MPEG 40282, neotype) from Tefé, Amazonas, Brazil ( Fig. 8 ). Specimens were calling perched 3 m above the ground near the edge of the river. The call of the PNJ specimens consists of one to two notes (mean duration of 0.034 s, SD=0.0016) separated by short intervals (mean inter-note interval = 0.11 s). The advertisement call has a mean duration of 0.19 s (SD = 0.05) with an average dominant frequency of 1814 Hz (SD = 96.99), mean rise time of 0.095 s (SD = 0.026), and mean frequency bandwidth of 1616.96 Hz (SD = 17.25) ( Fig. 8 ). The call from Tefé consists of two to three notes (mean duration of 0.037 s, SD = 0.0019) separated by short intervals (mean inter-note interval = 0.12 s). The advertisement call has a mean duration of 0.26 s (SD = 0.080) with an average dominant frequency of 1874 Hz (SD = 127.31), mean rise time of 0.13 s (SD = 0.041), and mean frequency bandwidth of 1762 Hz (SD = 17.09) According to Hoogmoed (1979), Crawford & Jones (1933), firstly described the call of Hyla granosa as a medium-pitched “pink”, however for him this call was more similar to that of H. punctata and for him, specimens of both species were confused. He provided sonograms of calls of both species from Suriname, without comments on temporal or spectral parameters. Later, the advertisement call of Hyla granosa was described by Duellman (1978) as a two- to four-note call, usually: “boop-boop-boop”. The duration of the notes was 0.078 seconds and the average dominant frequency was 1390 Hz. Subsequently, De la Riva et al. (1997) described the call as a series of two to seven short notes that decrease in intensity, with one average dominant frequency of 1327 Hz. Calls from studies in Ecuador (Pareja et al., unpublished) show values close to those found by Duellman and De la Riva et al.; the dominant frequency varies between 1560.41 Hz up to 1839.50 Hz. Boana cinerascens from the Guyanes has a call of 1–2 notes with a dominant frequency between 1260–2500 Hz (Lescure and Marty, 2000). The call of Boana cinerascens differs from the other advertisement calls of the group: Boana jimenezi´ s advertisement call is composed of 3–4 notes with a dominant frequency at 3010–3488 Hz., and Boana punctata calls with 5–15 notes and a dominant frequency between 689–1540 Hz (Hödl, 1977; Lescure and Marty, 2000; Marquez et al., 1993; Señaris and Ayarzaguëna, unpublished data). Finally, the mating call of Boana sibleszi usually consists of one note, occasionally two, with the dominant frequency at 1680–2231 Hz. Information regarding the advertisement calls of the Boana punctata group are summarized in Table 1 .

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Distribution. Boana cineracens is known with certainty from the type locality Tefé, Amazonas, Brazil; Parque Nacional do Jaú, Novo Airão, Amazonas, Brazil; and Canelos, Ecuador ( Fig. 10 ). This species occurs syntopically with B. gracils and may occur more widely.

Figures

FIGURE 3. Recently collected specimens of green tree frogs included in this study—Boana cinerascens. (A) Dorsolateral and (B) frontal profiles of MPEG 40282 (neotype), from Tefé, Amazonas, Brazil. (C) Dorsolateral and (D) frontal profiles of MPEG 40287 from Parque Nacional do Jaú, Amazonas, Brazil. (E) Dorsolateral and (F) frontal profiles of QCAZ-A 56580 from quebrada Pupalyacu, Canelos, Pastaza, Ecuador.

FIGURE 6. Neotype of Hyla cinerascens Spix, 1824 (= Boana cinerascens) (MPEG 40282). (A) Dorsal and (B) ventral views of male specimen from Tefé, Amazonas, Brazil. Scale bar = 10 mm.

FIGURE 7. Neotype of Hyla cinerascens Spix, 1824 (= Boana cinerascens) (MPEG 40282). (A) Lateral view of head, (B) palm of hand, and (C) palm of foot of male specimen, from Tefé, Amazonas, Brazil. Scale bar = 1 mm.

FIGURE 8. Advertisement calls of Boana cinerascens— oscillogram (above) and spectrograms (below). (A) Tefé, Amazonas, Brazil (MPEG 40282, neotype). (B) Parque Nacional do Jaú, Novo Airão, Amazonas, Brazil (MPEG 40290).

FIGURE 10. Geographic distribution of Boana cinerascens and Boana gracilis based on the localities of type specimens and samples included in our analyses. Black-star = Tefé, Amazonas, Brazil (type-locality of Boana cinerascens). White-star = Rio Uaupés (north of Ipanoré), Amazonas, Brazil (type-locality of Boana gracilis). White-rhombus = Canelos, Ecuador (type-locality of Hyla granosa). Circles = Boana gracilis. Triangle = both species. 1 = Parque Nacional do Jaú, Novo Airão, Amazonas, Brazil. 2 = Parque Nacional de Anavilhanas, Novo Airão, Amazonas, Brazil. 3 = Muri, Scrub Camp, Iwokrama, Guyana. 4 = San José de Chipiro, Boca del río Ventuari, Alto Orinoco, Amazonas, Venezuela. 5 = Macuruco, confluencia Orinoco-Ventuari, Alto Orinoco, Amazonas, Venezuela. White-ball = Canaripó, río Ventuari, Amazonas, Venezuela.