Boana nigra, Caminer & Ron, 2020

Caminer, Marcel A. & Ron, Santiago R., 2020, Systematics of the Boana semilineata species group (Anura: Hylidae), with a description of two new species from Amazonian Ecuador, Zoological Journal of the Linnean Society 190, pp. 149-180 : 166-171

BOANA NIGRA SP. NOV.

( FIGS 7A, 10; TABLE 5)

Lsid: urn:lsid:zoobank.org:act:FE5D2127-D2BD-4F4D-A4E5-4CE742A32F21

Holotype ( Figs 7A, 10): QCAZ 58786 (field no. SC 48236), adult male from Ecuador, Provincia Morona Santiago, Parque Nacional Sangay, Sardinayacu (2.1028° S, 78.1521° W), 1348 m a.s.l., collected by

Daniel Rivadeneira, David Velalcázar, Javier Pinto, Francy Mora, Darwin Núñez, Juan Carlos Sánchez and Andrea Correa on 29 January 2015.

Paratopotypes: QCAZ 58783–85 , 58787–89 , 58791– 97 , adult males, 58790, 58798, adult females, same collectors as the holotype, 15–29 January 2015 ; QCAZ 59110–12 , 59114 , 59116–17 , adult males, 59113, metamorph, 59115, 59118, tadpoles, 61881–87, juveniles, collected by S . R. Ron, D. Paucar, P. Venegas, P. Baldeón, M. Caminer and E. Nusirquia, 27 February 2015 ; QCAZ 58337–8 , tissues, collected by J. Brito on 29 October 2014 ; DHMECN 12130 , adult male, collected by D . R. Batallas and P. Bejarano on 16 June 2014 .

Paratypes: ECUADOR: PROVINCIA MORONA SANTIAGO: Bosque Protector Abanico (2.2583° S, 78.1983° W), 1560 m, QCAZ 48984, adult female, collected by D. Morocho on 1 June 2007; bridge N of Macas (2.3017° S, 78.1137° W), 944 m, QCAZ 47044, collected by S. Poe, F. Ayala, L. Gray, J. Davis and I. Latella, on 15 December 2009; Parque Nacional Sangay (1.786° S, 77.979° W), 982 m, QCAZ 54605–6, 51776, 51780, tissues, collected by L. MacLean and A. Almendáriz, on 4 December 1991 and 29 August 2011; PROVINCIA PASTAZA: Centro Ecológico Zanja Arajuno, km 6 on the road San Ramón-El Triunfo (1.373° S, 77.860° W), 910 m, QCAZ 36929, 36931, 40959, 45282, adult males, 45283, female, 37903, 37988, tadpoles, 40265, 40958, subadult females, collected by S. R. Ron, I. Tapia, L. Coloma, A. Carvajal, A. Merino, E. Arbeláez, A. Tapia, D. Salazar, D. Acosta and C. Korfel, on 29 April 2004 and 2 February 2009.

Common names : Proposed standard English name: black-flanked treefrog. Proposed standard Spanish name: rana arbórea de flancos negros.

Diagnosis ( Figs 7A, 10): Boana nigra is characterized by: (1) mean SVL 42.2 mm in males (range 38.5–46.3; N = 26), 64.8 mm in females (range 56.4–76.7; N = 5; Table 5); (2) thighs long (TL/SVL 0.44–0.53); (3) dorsal skin finely granular; (4) dorsum coloration brown, dark brown, cream or grey usually with an X- shaped mark on scapular region or rounded marks over the entire dorsum; (5) flanks and hidden surfaces of thighs vary from uniform black to dark vertical bars; (6) areolate skin on the posterior surface of throat, belly and ventral surfaces of thighs; (7) venter creamy white to pale orange, plain or spotted with dark brown; (8) in life, webbing pale orange, orange or black; (9) palpebrum reticulated; (10) nuptial excrescences present in breeding males; (11) projecting prepollices absent in both sexes; (12) tympanum large with distinct tympanic ring; (13) small triangular calcar on heel, often coloured with a cream spot; (14) advertisement call with one note; (15) pulses per note varying from 21 to 37; and (16) call dominant frequency varying from 996 to 1063 Hz.

Comparisons with other species: Boana nigra can be distinguished from B. ventrimaculata sp. nov., B. hutchinsi , B. diabolica and B. semilineata by having uniform black or dark vertical stripes (in females) on flanks (speckled pattern or blotches in all the four species; Fouquet et al., 2016). In addition, the hidden surfaces of thighs and webbing in life are red in B. diabolica (uniform black in B. nigra , sometimes with dark vertical bars on the hidden surfaces of thighs). The individuals of B. nigra with dark vertical bars pattern on flanks and hidden surfaces of the thighs can be confused with B. geographica and B. appendiculata . However, B. nigra differs in having orange or black webbing in life (red webbing except between fingers III–IV and toes IV–V in B. geographica ) and a cream to pale orange ventral coloration in life (yellow or orange in B. appendiculata ).

Some small adult B. appendiculata (<42 mm) can also have a cream venter with uniform black flanks. Ventral and webbing bright coloration fade to cream in preservative and become indistinguishable among the three species. Boana nigra and B. appendiculata also differ in environmental envelope ( Fig. 3D; for details see ‘Comparisons with other species’ in the description of B. appendiculata ). Despite being separated by high genetic distances (Table 6), they occur in sympatry, which indicates the existence of non-geographic reproductive barriers.

Boana nigra is easily distinguished from B. boans , B. icamiaba , B. pombali and B. wavrini by its prepollex not modified into a projecting spine and by the presence of pigmented nuptial excrescences. Boana boans further differs from B. nigra in having diffuse vertical bars on the flanks and barely distinguishable on the hidden surfaces of the thighs (well-defined vertical bars or uniform black in B. nigra ) and by its fully webbed hands (webbing extends to about the middle of the outer finger in B. nigra ).

Description of the holotype: Adult male, 42.5 mm SVL, foot length 16.5 mm, head length 9.9 mm, head width 14.5 mm, eye diameter 4.5 mm, tympanum diameter 3.7 mm, tibia length 22.4 mm, femur length 22.2 mm, calcar length 0.9 mm, arm length 7.7 mm, eye–nostril distance 4.3 mm, head wider than long and wider than body; snout sloping in lateral view, subacuminate in dorsal view; distance from nostril to eye shorter than diameter of eye; canthus rostralis rounded; loreal region concave; internarial region subtly depressed; nostrils not protuberant, directed laterally; interorbital area slightly convex; eye large, protuberant; lower eyelid finely reticulated; diameter of eye 1.2 times diameter of tympanic annulus; supratympanic fold inconspicuous; tympanic membrane roundish, slightly longer than high; tympanic annulus evident, rounded, separated from eye by c. 0.5 times its diameter. Arm slender, axillary membrane absent; relative length of fingers I <II <IV <III; finger discs broadly expanded, round, as wide as long; subarticular tubercles prominent, round to ovoid, single; supernumerary tubercles absent; palmar tubercle inconspicuous; large and rugose dark P-shaped nuptial pad on dorsal surface of finger I; prepollex not modified into a projecting spine; webbing formula of fingers I basal II1½—3 – III2½— 2IV. Toes bearing discs broadly expanded, rounded and slightly smaller than those of fingers; relative length of toes I <II <V <III <IV; inner metatarsal tubercle large, elliptical; outer metatarsal tubercle absent; subarticular tubercles single, round, large and protuberant; supernumerary tubercles small, round; webbing formula of toes I1 + —2 – II1—2 – III1 + —2 + IV2 + — 1 + V. Vocal sac single and subgular. Skin on dorsum, head and dorsal surfaces of limbs finely granular; throat smooth anteriorly without mental gland; posterior surface of throat, belly and ventral surfaces of thighs areolate, those of shanks smooth. Cloacal opening directed posteriorly at upper level of thighs, round tubercles below and on sides of vent. Tongue slightly cordiform, widely attached to mouth floor; vomerine odontophores situated parallel to choanae, in two oblique series narrowly separated, each bearing 9–11 vomerine teeth; choanae trapezoidal, oblique.

Colour of holotype in preservative ( Fig. 10): Dorsum light grey with extensive dark brown rounded marks, sometimes interconnected; faint brown transversal bands on the dorsal surfaces of shanks; flanks, hidden surfaces of limbs and dorsal surfaces of thighs, upper arms, hands and feet black; venter cream with dark, diffuse, minute dots on the belly; ventral surfaces of thighs, forearms and hands cream; ventral surfaces of shanks and upper arms black; discs and webbing grey.

Colour of holotype in life ( Fig. 7A): Dorsum brown with dark brown rounded marks over the entire dorsum; dorsal and hidden surfaces of limbs and flanks black; faint brown transversal bands on the dorsal surface of hindlimbs; venter and ventral surfaces of thighs and hands cream; belly cream with brown diffused dots; ventral surfaces of upper limbs, shanks and feet black; discs and webbing black; iris bronze.

Etymology: The specific epithet nigra is a Latin adjective in the nominative case meaning black, and refers to the black coloration on the flanks of these frogs.

Variation in preservative: Morphometric data for adult specimens are summarized in Table 5, and variation in dorsal and ventral coloration of preserved specimens is shown in Figure 10. Sexual dimorphism is observed in SVL, with 38.5–46.3 mm (42.2 ± 2 mm, N = 26) in males and 56.4–76.7 mm (64.8 ± 7.9 mm, N = 5) in females. Females are significantly larger than males (t = –6.40, d.f. = 4.1, P = 0.002).

Head shape varies between subacuminate and rounded in dorsal view; in lateral view it varies between truncate and short, rounded. The head is wider than long and slightly wider than the body in most of the specimens. Breeding males have keratinized nuptial excrescences on the inner surfaces of the thumbs. Calcar size ranges from inconspicuous (e.g. QCAZ 58783) to prominent (e.g. QCAZ 45283). Webbing on the hand varies slightly among specimens: fingers I basal II (1 + –2 –)—(2½–3 –) III (2 –– 2½)—(2–2 +) IV. Variation of webbing between toes is I (1–2 –)—(1–2 –) II (1–1 +)—(1–2 +) III (1–1½)—(1 + –2 +) IV (2 –– 2 +)—(1–1 +) V. Vomerine teeth (N = 15): 8–12 (right = 9.14) and 7–12 (left = 9.71).

Most variation involves dorsal coloration and pattern. Background dorsal coloration varies from brown (e.g. QCAZ 45282), dark brown (e.g. QCAZ 48984), cream (e.g. QCAZ 45283) to grey (e.g. QCAZ 47044) with a dark brown, X- shaped mark on the scapular region or dark brown rounded marks over the entire dorsum (e.g. QCAZ 59114); sometimes rounded marks are interconnected (e.g. QCAZ 59117). Scattered, minute, black or white flecks are present on the dorsal surfaces (e.g. QCAZ 40958). A dark mid-dorsal line extends from the tip of the snout to the mid-sacrum (e.g. QCAZ 45283). Dark brown or grey transversal bands are present on the dorsal surfaces of the limbs (one or two on the upper arm and forearm and three to five on the thigh, shank and foot). The coloration of flanks and hidden surfaces of thighs and shanks are uniform black in males (e.g. QCAZ 58783) or grey with dark vertical bars in females (e.g. QCAZ 48984). However, in some cases males can present dark vertical bars on the flanks (e.g. QCAZ 6478). The heels have usually the same colour as the rest of the body (e.g. QCAZ 45282), but in some individuals heels are cream, contrasting with the background dorsal coloration (e.g. QCAZ 40958).

Ventral surfaces of preserved specimens vary from creamy white (e.g. QCAZ 40958) to yellowish white (e.g. QCAZ 48984). In some individuals, there are dark brown spots on the belly (e.g. QCAZ 58783). Coloration of webbing and discs vary from yellowish white to cream, black or grey.

Coloration in life ( Fig. 7A): Dorsal surfaces vary from brown (e.g. QCAZ 58783) to dark brown (e.g. QCAZ 59110) or reddish brown (e.g. QCAZ 59111) with brown marks on the dorsum; brown transversal bands on dorsal surfaces on limbs; brown rounded spots and blotches over the entire dorsum (e.g. QCAZ 59110, 59111). In some individuals, there are scattered minute black or white flecks on dorsal surfaces (e.g. QCAZ 36929, 58783). Flanks and hidden surfaces of thighs are uniform black (in males) or grey with dark vertical bars (in females); belly and ventral surfaces of limbs vary from cream to pale orange (e.g. QCAZ 59111, 59114); throat cream white or pale orange; webbing vary from pale orange to orange or black; fingers and toes dorsally vary from black to grey or have the same coloration of webbings; iris brown (e.g. QCAZ 58797) or bronze (e.g. QCAZ 36929); palpebrum finely reticulated with golden yellow.

In recently metamorphosed individuals, flanks, hidden surfaces of thighs, dorsal surfaces of the limbs, sides of the head and webbing are black; venter is grey sometimes with scattered dark brown spots; dorsum is cream with black spots and irregular blotches ( Fig. 8B).

Vocalization: Based on one male ( DHMECN 12130 ) recorded at Sardinayacu ( Provincia Morona Santiago) by D. R. Batallas on 16 June 2014 at 22:30 h, air temperature 14.8 ° C. The call ( Fig. 9E, F; Table 2) consists of one groan-like note with a mean duration of 0.33 s and dominant frequency of 1044.2 Hz. Other parameters are available in Table 2. The individual was perched on vegetation 40 cm above the ground near a lake .

Distribution and ecology: Boana nigra occurs on the eastern Andean slopes of Ecuador (provinces of Morona Santiago, Napo, Pastaza, Sucumbíos and Zamora Chinchipe) ( Fig. 6). Localities with known elevation range from 910 to 1847 m a.s.l. The elevation at Sardinayacu (1847 m) is the highest known for B. nigra , while Centro Ecológico Zanja Arajuno (910 m) is the lowest. It is generally found next to streams, swamps, ponds and lakes. Individuals have been recorded at night perching on vegetation 30 to 400 cm above ground or water. The specimen from 9 de Octubre was found next to a highway on the leaf litter.

Vegetation types at known localities include: (1) Amazonian evergreen foothill forest, characterized by a mixture of Amazonian and Andean vegetation with a canopy of 30 m; (2) montane cloud forest of the eastern Andes, characterized by trees covered by mosses and abundant epiphytes; (3) evergreen lower montane forest of the east of the northern and central Andes, characterized by a canopy height of 25 to 30 m, with abundant epiphytes, and by the absence of species of trees characteristic of the lowlands (e.g. species from the family Bombacaceae and Myristicaceae ); and (4) lowland floodplain forest of white-waters, characterized by periodical flooding with white-waters from large rivers, with the vegetation reaching 35 m in height, and several horizontal strata of vegetation ( Sierra et al., 1999).