Hypsiboas almendarizae, Caminer, Marcel A. & Ron, Santiago R., 2014

Caminer, Marcel A. & Ron, Santiago R., 2014, Systematics of treefrogs of the Hypsiboas calcaratus and Hypsiboas fasciatus species complex (Anura, Hylidae) with the description of four new species, ZooKeys 370, pp. 1-68 : 20-26

Hypsiboas almendarizae sp. n.

Common name.

English: Almendariz’s treefrog; Spanish: Rana arbórea de Almendáriz

Holotype.

(Fig. 14E) QCAZ 39650 (field no. SC-PUCE 23213), adult male from Ecuador, Provincia Morona Santiago, General Leonidas Plaza, “Limón”, on the road to Gualaceo (2.9796°S, 78.4415°W), 1237 m above sea level, collected by Marcel A. Caminer on 17 January 2009.

Paratopotypes.

(Fig. 8B) QCAZ 39638-40, 39645-49, adult males, collected with the holotype.

Paratypes.

(Figs 4B, 6) ECUADOR: PROVINCIA NAPO: Pacto Sumaco (0.6339°S, 77.5922°W), 1560 m, QCAZ 10910, adult male, collected by L. E. López on 1 January 1996; Río Hollín (0.6998°S, 77.6665°W), 1068-1950 m, QCAZ 22365-66, adult males, collected by M. R. Bustamante on 27 January 2002; Río Hollín, on the road Jondachi-Loreto (0.7707°S, 77.7820°W), 1100 m, QCAZ 6905, 6910, adult males, 6889, juvenile, collected by P. Ordoñez, P. Guarderas, J. F. Freile, M. C. Terán and O. Torres-Carvajal on 3 December 1994; Río Hollín, on the road Hollín-Loreto (0.9666°S, 77.7632°W), 600 m, QCAZ 283, 782, 4177-78, adult males, collected by A. Flachier, F. Campos-Yánez, L. A. Coloma and G. Onore on 5 December 1987 and 1 February 1988; Río Hollín (0.6998°S, 77.6665°W), 1068-1950 m, QCAZ 21942, 22364, adult males, 17944, collected by M. R. Bustamante, I. G. Tapia, G. Onore, F. Ayala-Varela, S. Valdivieso, D. Tirira and J. J. Wiens on 20 March 1990 and 9 December 2001; Archidona, Estacíon Sarayacu (0.6910°S, 77.8208°W), 1320 m, QCAZ 51809, juvenile female, collected by D. Rivadeneira and X. Salazar on 23 August 2011; PROVINCIA TUNGURAHUA: Baños, Río Lagarto (1.4025°S, 78.2980°W), 1472 m, QCAZ 24392, 24394, adult males, collected by I. G. Tapia and D. Hill on 5 May 2001; Río Verde (1.4026°S, 78.2979°W), 1514 m, QCAZ 47047-48, adult males, collected by S. Poe, F. Ayala-Varela, L. Gray, J. Davis and I. Latella on 14 December 2009; Río Negro (1.4135°S, 78.2110°W), 1220 m, QCAZ 4029-30, 4907, 21273-74, adult males, 24357, adult female, 4034, metamorph, collected by F. Campos-Yánez, L. A. Coloma, C. Proaño and J. J. Camacho on 1 May 1993 and 24 September 2002; mouth of the Pastaza river (1.4128°S, 78.2688°W), 1440 m, QCAZ 31449, adult male, 31450, adult female, collected by D. Paucar on 9 March 2006; Baños, Río Lagarto (1.4025°S, 78.2980°W), 1472 m, QCAZ 24386-91, 24393, 24395, adult males, collected by I. G. Tapia and D. Hill on 5 May 2001; mouth of the Pastaza river (1.4128°S, 78.2687°W), 1440 m, QCAZ 31452, juvenile, collected by D. Paucar on 8 March 2006; PROVINCIA PASTAZA: Pomona, Reserva de Bosque Tropical Hola Vida (1.6250°S, 77.9072°W), 831 m, QCAZ 37163, adult male, collected by I. G. Tapia, L. A. Coloma, C. Proaño and M. Páez on 9 July 2007; PROVINCIA MORONA SANTIAGO: 2.2 km N San Juan Bosco (2.0070°S, 77.9348°W), 1013 m, QCAZ 26438, adult male, collected by L. A. Coloma on 12 August 2003; Parque Nacional Sangay, Sardinayacu river (2.0597°S, 78.1564°W), 1600 m, EPN 7740, adult male, collected by A. Almendáriz; Central Hidroeléctrica Abanico (2.2457°S, 78.1958°W), 1600 m, EPN 11435-36, 11438, adult males, 11437, adult female, collected by Y. Sagredo and J. Brito; 7.6 km W from Nueve de Octubre, along the road Guamote-Macas (2.2163°S, 78.2898°W), 1571 m, QCAZ 32638-39, 32645, adult females, collected by A. Pounds, L. A. Coloma, M. R. Bustamante and I. G. Tapia on 30 November 2006; 4.8 km N from Rosario (2.8858°S, 78.3880°W), 841 m, QCAZ 26474-77, adult males, 26480, metamorph, collected by L. A. Coloma, A. Merino and E. R. Wild on 13 August 2003; N from Mendez, 4 km NW from Patuca (airline distance) on the road to Logroño (2.7291°S, 78.2849°W), 600 m, QCAZ 23810, adult male, collected by S. R. Ron and G. E. Romero on 6 April 2003; El Rosario (2.9282°S, 78.4082°W), 1100 m, QCAZ 30590-92, adult males, collected by I. G. Tapia, M. R. Bustamante and A. Merino on 23 March 2004; N from General Leonidas Plaza, “Limón”, on the road Limón-Méndez (2.9046°S, 78.3869°W), 879 m, QCAZ 26300, adult male, collected by S. R. Ron, M. Guerra and I. G. Tapia on 13 January 2004; Limón Indanza, on the road to Ayanza (2.9899°S, 78.4260°W), 994 m, QCAZ 39642, adult male, collected by M. A. Caminer on 17 January 2009; near General Leonidas Plaza, “Limón”, km 74 on the road to San Antonio (2.9266°S, 78.4070°W), 1070 m, QCAZ 8573, adult male, collected by N. Acosta-Buenaño and J. Bosch on 16 July 1995.

Referred specimens.

ECUADOR: PROVINCIA MORONA SANTIAGO: 2.2 km N San Juan Bosco (2.0070°S, 77.9348°W), 1013 m (QCAZ 26429-37, 26439); Nueve de Octubre, on the road Guamote-Macas (2.2445°S, 78.2074°W), 1527 m (QCAZ 32268, 37639); Méndez (2.7145°S, 78.3153°W), 500 m (QCAZ 1006-07); Km 65 on the road Macas-Méndez (2.68083°S, 78.23341°W), 540 m (QCAZ 15904-06, 15999); 13 km N from Limón (2.8895°S, 78.3952°W), 800 m (QCAZ 27317-23, 27325); Limón Indanza (2.9796°S, 78.4414°W), 800-1560 m (QCAZ 8572, 25958, 26407, 26555, 26562, 31866, 32831, 32834, 32836, 32842, 39642, 40027, 41932-33, 41992, 42001, 42017-18, 42022, 42026, 42037, 42039-40, 42055, 42236); Plan de Milagro-Limón, 4.3 km WSW Limón (3.0118°S, 78.4784°W), 1373-1560 m (QCAZ 26376-85, 26400-01, 41894, 41897, 41898); 3 km Limón-Indanza, on the road to Gualaquiza (3.0489°S, 78.5007°W), 950 m (QCAZ 48176-78); on the road Indanza-Gualaquiza (3.1435°S, 78.5359°W), 1277 m (QCAZ 26421-22); Bosque Protector Abanico, 1646-1720 m (QCAZ 49029, 49034).

Diagnosis.

A member of the genus Hypsiboas characterized by: (1) mean SVL 37.64 mm in males (range 34.31-44.56; n = 23), 48.11 mm in females (range 37.80-51.94; n = 4); (2) basal webbing on fingers; (3) calcar large, conical; (4) dorsal coloration varying from cream to reddish brown, grayish brown or pale brown, sometimes with dark marks (e.g., broad transversal bands or narrow longitudinal lines); (5) dark brown middorsal line often present; (6) flanks pale cream or creamy white (in life, blue in large females and light blue or white in males) with thin dark brown vertical bars; (7) hidden surfaces of thighs pale cream or creamy white (in life, blue in large females and light blue or white in males) with thin dark brown transversal bars; (8) ventral surfaces of thighs creamy white or yellowish white; (9) venter creamy white or yellowish white; (10) webbing on feet; (11) in life, iris cream or creamy silver with an upper yellow to orange band; (12) prepollical spine present in males.

Hypsiboas almendarizae is most similar to Hypsiboas fasciatus and Hypsiboas calcaratus . It can be distinguished from Hypsiboas calcaratus by the shape of the calcar (large and conical in Hypsiboas almendarizae vs. large and triangular in Hypsiboas calcaratus ; Fig. 14 C–D), width of the transversal lines on the flanks (thin in Hypsiboas almendarizae vs. wide in Hypsiboas calcaratus ), and advertisement call (Fig. 12 C–F). Hypsiboas almendarizae differs from Hypsiboas fasciatus in having narrower transversal dark bars on the flanks and thighs (mean width of bars on thighs = 5.05% of femur length in Hypsiboas almendarizae vs. 8.58% in Hypsiboas fasciatus ; differences are significant: t = 7.05, df = 12, P <0.001) and in color of the upper band of the iris (red to reddish brown in Hypsiboas fasciatus vs. yellow to orange in Hypsiboas almendarizae ; Fig. 14 A–B).

Hypsiboas almendarizae differs from Hypsiboas maculateralis sp. n. in advertisement call (Figs 12 C–D and 13 A–B) and in the presence of vertical lines on the flanks and hidden surfaces of the thighs (dark blotches instead of lines in Hypsiboas maculateralis sp. n.) Hypsiboas almendarizae can be distinguished from Hypsiboas alfaroi sp. n. and Hypsiboas tetete sp. n. by the presence of a calcar (instead of a small tubercle on the heel) and by the absence of dark flecks on the gular region and chest (present in Hypsiboas alfaroi sp. n. and Hypsiboas tetete sp. n.) Morphological characters useful to differentiate Hypsiboas almendarizae from other species are shown in Table 6.

Description of the holotype.

Adult male, 36.72 mm SVL, foot length 15.93 mm, head length 9.18 mm, head width 11.95 mm, eye diameter 4.26 mm, tympanum diameter 2.41 mm, tibia length 21.78 mm, femur length 20.03 mm, calcar length 1.10 mm, arm length 6.17 mm, eye-nostril distance 2.7 mm, head wider than long and wider than body; snout round in lateral view, truncate in dorsal view; distance from nostril to eye shorter than diameter of eye; canthus rostralis indistinct, rounded; loreal region concave; internarial area convex; nostrils not protuberant, directed laterally; interorbital area slightly convex; eye large, strongly protuberant; diameter of eye 1.8 times diameter of tympanic annulus; tympanum concealed beneath skin;tympanic annulus evident, ovoid, longer dorsoventrally, concealed dorsally by supratympanic fold, separated from eye by ca. 1.2 times its diameter; posterior end of supratympanic fold reaches anterior border of arm insertion. Arm slender, axillary membrane absent; indistinct low tubercles present along ventrolateral edge of forearm; relative length of fingers I<II<IV<III; fingers bearing large, oval discs, that of third finger about three fourths of tympanum diameter; subarticular tubercles prominent, round to ovoid, single; supernumerary tubercles present; palmar tubercle small, elongated; prepollical tubercle large, flat, elliptical; prepollex enlarged, claw shaped; nuptial excrescences absent; webbing absent between fingers. Large conical calcar on tibiotarsal articulation; ill defined, scattered tubercles on tarsus and along ventrolateral edge of foot; toes bearing discs slightly wider than long, smaller than those of fingers; relative length of toes I<II<V<III<IV; outer metatarsal tubercle ill defined, small, round; inner metatarsal tubercle large, elliptical; subarticular tubercles single, round, flat; supernumerary tubercles restricted to the soles; webbing formula of toes I2- 2¾II1¾ -3-III2--3+IV3+-2-V. Skin on dorsum, head, and dorsal surfaces of limbs smooth; skin on flanks smooth with weak longitudinal wrinkles posterior to the arm; skin on venter coarsely granular; skin on ventral surfaces of head and thighs granular, those of shanks smooth. Cloacal opening directed posteriorly at upper level of thighs; cloacal sheath short simple, covering cloacal opening; round tubercles below and on the sides of vent, larger proximally. Tongue cordiform, widely attached to mouth floor; vomerine odontophores triangular, narrowly separated, posteromedial to choanae, bearing six vomerine teeth on each side; choanae trapezoidal, oblique.

Color of holotype in preservative. Dorsum pale grayish brown with five to seven broad brown transversal bands and scattered minute black dots; few small cream dots on the posterior one third of the dorsum; dark brown middorsal line from tip of the snout to the mid-dorsum; brown transversal bars on dorsal surfaces of the limbs (two on the upper arm, five on the thigh, and three on the shank and foot); flanks pale cream with ten thin dark brown transversal bars; hidden surfaces of thighs pale cream with seven to nine thin dark brown transversal bars; narrow cream stripe present above the anus; venter yellowish white becoming creamy white on its posterior half; ventral surfaces of hindlimbs, forelimbs, and webbing yellowish white; faint narrow to wide pale brown stripe on the outer edge of the hands and forearms; minute brown blotches on lips; bones white.

Color of holotype in life. (Fig. 14E). Dorsum pale yellow tan with pale broad brown transversal marks and scattered minute black and white dots; dark brown middorsal line is present; pale brown transversal bars on the dorsal surfaces of the limbs; flanks white with faint thin dark brown vertical bars; hidden surfaces of thighs white with thin dark brown transversal bars; venter creamy white; ventral surfaces of hindlimbs and forelimbs translucent pinkish; discs and webbing yellowish; iris cream with upper yellow band; bones white.

Etymology.

The specific name is a noun in the genitive case and is a patronym for Ana Almendáriz, Ecuadorian herpetologist who for more than three decades has contributed to the study of Ecuadorian amphibians and reptiles. Ana Almendáriz is curator of Herpetology in the Museo de Historia Natural Gustavo Orcés at Escuela Politécnica Nacional del Ecuador.

Variation.

Variation in dorsal and ventral coloration of preserved specimens is shown in Figure 6. Background dorsal coloration varies from creamy white (e.g., QCAZ 32638, 32645) to reddish brown, grayish brown (e.g., QCAZ 24394, 39647), pale grayish brown (e.g., QCAZ 24392, 39650) or pale brown (e.g., QCAZ 24386). A dark middorsal line extends from the tip of the snout to the middle of the sacrum (e.g., QCAZ 39647) or to the vent (e.g., QCAZ 32645), but in some specimens is restricted to the head (e.g., QCAZ 26429) or to the anterior half of the body (e.g., QCAZ 39650). In few specimens, the middorsal line is faint or absent (e.g., QCAZ 24392). Irregular dorsal marks may be present in varying number, size, and shape. Five to seven broad transversal bands (sometimes interconnected) can be present on the dorsum. Some individuals (e.g., QCAZ 24394, 39650, 39647) have narrow brown transversal bars 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). Faint to well-defined narrow longitudinal lines may be present on the dorsum (e.g., QCAZ 32638, 32645). In some individuals (e.g., QCAZ 32645), there are few scattered brown or white dots on the dorsum, and dorsal surfaces of forearms, shanks and tarsi. The coloration of the flanks and hidden surfaces of the thighs vary from pale cream to creamy white, with thin dark brown transversal bars. The number of bars on the flanks and thighs varies from six to ten on each flank and six to thirteen on each thigh; the area with vertical bars extends from the groin to the mid-flank. In few individuals, the dark transversal bars of the thighs and flanks are faint (e.g., QCAZ 32645).

Ventral surfaces of preserved specimens vary from creamy white (e.g., QCAZ 39650) to yellowish white (e.g., QCAZ 39647). A narrow to wide faint pale brown stripe is present in some individuals on the outer edge of the hands, forearms, feet, thighs, and tarsal folds (e.g., QCAZ 39647). In some individuals, scattered minute pale brown blotches may be present on the lips (e.g., QCAZ 32638, 39647). Coloration of webbing and discs vary from yellowish white to brown or gray. Vomerine odontophores are triangular (with arched base in some specimens). Bones white.

In the adult type series, the largest male has a SVL 44.56 mm, and the largest female 51.94 mm; mean male SVL = 37.64 mm (n = 23; SD = 2.01), mean female SVL = 48.11 mm (n = 4; SD = 6.88). Females were not significantly larger than males (t = -3.02, df = 3, P = 0.055). Inter-population variation in size and other morphometric variables is shown in Tables 1 and 2.

Coloration in life.

(based on photographs; Figs 4B and 8B). Dorsal surfaces vary from pale yellowish tan (e.g., QCAZ 39640) to reddish brown (e.g., QCAZ 32638) with a middorsal dark brown line (e.g., QCAZ 42055); sometimes broad pale brown transversal bands are present on the dorsum; the dorsal surfaces of the limbs often have pale brown transversal bars (e.g., QCAZ 39640); in some specimens, the dorsum has faint to well-defined narrow brown longitudinal lines (e.g., QCAZ 39649); scattered minute black, yellow or white dots can be present on the dorsum (e.g., QCAZ 39648); flanks and hidden surfaces of thighs white, light blue or blue with thin dark brown vertical bars (e.g., QCAZ 39646, 42055); in some individuals there are thin dark brown transversal bars on the hidden surfaces of the shanks (e.g., QCAZ 42055); venter creamy white with yellowish white belly (e.g., QCAZ 48177); ventral surfaces of hindlimbs and forelimbs translucent pinkish (e.g., QCAZ 39650) or yellowish (e.g., QCAZ 39638); in some specimens, ventral surfaces of the thighs creamy white (e.g., QCAZ 49029); discs and webbing yellowish (e.g., QCAZ 48177); iris cream (e.g., QCAZ 39648) or creamy silver (e.g., QCAZ 39639) with upper yellow to orange band (e.g., QCAZ 39646); bones white (e.g., QCAZ 48177).

Advertisement call.

We recorded calls from five males at Limón Indanza (Provincia Morona Santiago) on 17 January 2009 (Table 7). The advertisement call consists of three to four quack notes (Fig. 12 C–D). Mean call duration is 0.48 s (SD = 0.007) and mean rise time is 0.30 s (SD = 0.10). Sound frequency increases from the beginning to the end of the note; mean dominant frequency is 1954.43 Hz (SD = 128.43) and mean fundamental frequency is 951.76 Hz (SD = 61.38). The advertisement calls of Hypsiboas almendarizae and Hypsiboas fasciatus are similar to each other (Fig. 12 A–D). The distribution ranges of these species are parapatric with a small area of sympatry in the surroundings of Leonidas Plaza (Provincia Morona Santiago). The analyzed calls from Hypsiboas fasciatus were from a region of allopatry. Future studies should aim to compare calls from the region of sympatry to explore the possibility of reproductive character displacement.

Distribution and ecology.

Hypsiboas almendarizae occurs on the eastern Andean slopes of central and southern Ecuador (Morona Santiago, Napo, and Tungurahua provinces) (Fig. 15). Localities with known elevation range from 500 to 1950 m above sea level. The elevation at Río Hollín (1950 m) is the highest known locality for Hypsiboas almendarizae , while Méndez (500 m) is the lowest.

Most specimens of Hypsiboas almendarizae were collected at Río Napinaza, a river surrounded by secondary forest, pastures, and agricultural lands. Frogs were perching on vegetation 25 to 80 cm above the ground. Individuals from Limón Indanza, Río Hollín, Río Lagarto, Méndez, Río Pastaza, and Nueve de Octubre were found in flooded areas with pastures, on vegetation 30 to 70 cm above the ground. Few individuals were found near river Hollín, in small ponds in primary and secondary forest, roosting on branches and leaves 20 to 150 cm above the ground. All the specimens from Rosario and Plan de Milagro were found next to a highway, in swamps and streams with grass.

Vegetation types are: (1) Amazonian Evergreen Foothill Forest, characterized by a mixture of Amazonian and Andean vegetation with a canopy of 30 m, (2) Evergreen Lower Montane Forest of the Amazonian Range, characterized by trees reaching 20 -30 m of height and abundant epiphytes and hemiepiphytes, with dense vegetation, and Dictyocaryum lamarckianum ( Arecaceae ) as dominant species, (3) Evergreen Lower Montane Forest of the East of the Southern Andes, characterized by abundant epiphytes, trees reaching 30 m of height with Podocarpus trees as dominant species, (4) Evergreen Lower Montane Forest of the East of the Northern and Central Andes, characterized by a canopy of 25 to 30 m, with abundant epiphytes and by the absence of species of trees characteristic of the lowlands like the family Bombacaceae and Myristicaceae , and (5) Amazonian Lowland Evergreen Forest, characterized by high plant alpha-diversity and a canopy of 30 m with emergent trees that reach 40 m.

Conservation status.

Its distribution polygon has 14,983 km2. Within this area, 4,864 km2 (32.4%) of its habitat has been degraded by human activities, especially agriculture and cattle raising (estimated from Ministerio de Ambiente del Ecuador 2013). Current habitat degradation within the range of Hypsiboas almendarizae is extensive and its increase may threaten its survival in the future. Therefore, we propose that Hypsiboas almendarizae is assigned to the Near Threatened category. Its distribution polygon overlaps with Parque Nacional Sangay, Parque Nacional Llanganates, and Parque Nacional Sumaco Napo-Galeras.