Gastrotheca aguaruna, Duellman, William E., Barley, Anthony J. & Venegas, Pablo J., 2014

Duellman, William E., Barley, Anthony J. & Venegas, Pablo J., 2014, Cryptic species diversity in marsupial frogs (Anura: Hemiphractidae: Gastrotheca) in the Andes of northern Peru, Zootaxa 3768 (2), pp. 159-177 : 164-170

Gastrotheca aguaruna new species

Holotype: KU 212022, an adult female, from Molinapampa, 6˚10'50"S, 77˚37'01"W, 2400 m, Provincia Chachapoyas, Departamento Amazonas, Peru, one of a series collected by S. S. Barantes, F. M. Cuadros, W. E. Duellman, M. E. Morrison, and J. J. Wiens on 26 January 1989.

Paratypes: KU 212023–212025, adult males, 212026–212027, adult females, 212028 and 212030–31, adult males collected with the holotype, and KU 212021, adult male, from 5 km N Levanto, 6˚17'59"S, 77˚53'55"W, 2850 m, Provincia Chachapoyas, Departamento Amazonas, Peru, collected by W. E. Duellman on 25 January 1989.

Referred specimens: CORBIDI 380, adult female, from ACP Huiquilla, 6˚22'45"S, 77˚58'42"W, 2935 m, Provincia Luya, Departamento Amazonas, Peru, collected by G. Chávez 1 February 2008. CORBIDI 592, adult female, from Camino Leimebamba–Los Chilchos, 6˚39'51.2"S, 77˚41'23.9"W, 3240 m, Provincia Mariscal Caceres, Departamento San Martín, Peru, collected by P. J. Venegas on 23 January 2008; CORBIDI 10933, adult male, from Tragadero–Las Piñas, 6˚39'45.5"S, 77˚44'28.8"W, 3235 m, Provincia San Martín, Departamento San Martín, Peru, collected by P. J. Venegas and L. Echevarría on 10 May 2012; CORBIDI 11747, 11752, 11763, 11767, 11770, adult males, 11773, juvenile, 11774, adult male, 11788–89, adult females, 11792–93, adult males, 11794, adult female from Hornillo, 6˚08'30"S, 77˚29'04.9"W, 3308 m, Distrito de Vista Alegre, Provincia Rodríguez de Mendoza, Departamento Amazonas, Peru, collected by P. J. Venegas and V. Duran on 23 August–2 September 2012; KU 138238–40, adult males, and 128241, juvenile, from Chachapoyas, 6°12'63"S, 77°51'22" W, 2340 m, Provincia Chachapoyas, Departamento Amazonas, Peru, collected by T. H. and P. R. Fritts on 1 May 1970; KU 181741, juvenile, from 20.5 km (by road) WSW of Leimebamba, 6°55'40"S, 77°54'48" W, 3220 m, Provincia Chachapoyas, Departamento Amazonas, Peru, collected by D. C. Cannatella on 6 March 1979; KU 212029, adult female (skeleton), MUSM 6116–21, adult males and MUSM 6292, juvenile, all from the type locality, collected with the holotype; KU 215627, juvenile, from Chachapoyas, 6°12'63"S, 77°51'22" W, 2360 m, Provincia Chachapoyas, Departamento Amazonas, Peru, collected by F. M. Cuadros and J. J. Wiens on 25 January 1989.

Diagnosis. A moderately large species (SVL 41.6–46.8 mm in males, 49.4–50.8 mm in females) with (1) tibia length 45–54% SVL, about same length as foot; (2) interorbital distance about equal to width of upper eyelid; (3) skin on dorsum weakly granular to smooth, not co-ossified with skull, lacking transverse ridges; (4) supraciliary processes absent; (5) heel lacking calcar or tubercle; (6) tympanic annulus smooth; (7) Finger I> II, with discs slightly wider than digits; (8) fingers unwebbed; (9) webbing extending maximally to antepenultimate subarticular tubercle on Toe IV and nearly to penultimate subarticular tubercle on Toe V; (10) dorsum green with or without faintly darker paravertebral marks; (11) head markings consisting of a pale labial stripe and dark canthal stripe in some; (12) pale dorsolateral stripe present or not; (13) flanks and anterior surfaces of thighs lacking dark markings, but black spots or reticulations present in groin; (14) venter cream with dark flecks or spots; (15) brood pouch single, dorsal.

Gastrotheca aguaruna most closely resembles four other species in northern Peru. In contrast to the much larger G. monticola— SVL 49.0– 55.7 mm (x = 51.7 ± 2.62, n = 11 males), 48.0– 66.3 mm (x = 58.4 ± 5.11, n = 16 females)— G. aguaruna lacks a pale supracloacal stripe and black spots on the flanks and anterior surfaces of the thighs (Table 1; Fig. 3 ). The slightly larger G. aratia— SVL 42.8–55.7 mm (x = 48.1 ± 4.6, n = 8 males), 56.8 (n = 1 female)—differs by lacking black marks in the groin, having unpigmented nuptial excrescences, a brown vocal sac, and by having slightly more webbing on the foot; the web extends to the penultimate subarticular tubercle of Toe IV. In addition, G. aratia differs from G. aguaruna by having a tarsal fold extending the full length of the tarsus. Gastrotheca dysprosita Duellman differs from G. aguaruna by having a green dorsum with a narrow, diffuse, yellow middorsal stripe, green flanks with small yellow spots, and a granular tympanic annulus. Gastrotheca lateonota Duellman and differs from G. aguaruna by having a truncate snout in profile, smooth skin on the dorsum, and a nearly uniform grayish brown venter. Six other species of Gastrotheca in the Andes in northern Peru include G. peruana (Boulenger) , G. phalarosa Duellman and Venegas , and G. phelloderma Lehr and Catenazzi , all of which have pustular skin on the dorsum. In G. ossilaginis Duellman and Venegas the skin on the skull is co-ossified with the underlying dermal bones. Gastrotheca abdita Duellman , differs by having an acuminate snout in dorsal view. Lastly, G. galeata Trueb and Duellman differs from all the others by having a spatulate labium; the latter two also produce eggs that undergo direct development. The Ecuadorian G. pseustes Duellman and Hillis differs from G. aguaruna by having an anteroventrally inclined snout in profile and a pale supracloacal stripe.

Description of holotype. Adult female; body robust; SVL 50.8 mm; head as wide as long; snout rounded in dorsal view and in profile, extending slightly beyond margin of lower lip; canthus rostralis acutely rounded in section; loreal region concave; lips rounded; top of head flat; interorbital distance equal to width of upper eyelid; internarial area flat; nostrils not protuberant near terminus of canthus rostralis, posterior to level of anterior margin of lower jaw; diameter of eye much greater than its distance from nostril; tympanum round, separated from eye by distance about one and a half times length of tympanum; tympanic annulus distinct (barely evident on left side), smooth; supratympanic fold moderately heavy, extending from posterior corner of orbit to point posterior to tympanum, obscuring upper edge of tympanum. Arm robust; row of ulnar tubercles absent; hand moderately large; fingers short, unwebbed; discs small, rounded, slightly wider than digits; width of disc on Finger III about equal to half length of tympanum; relative lengths of fingers I> II <IV <III; subarticular tubercles low, rounded, none bifid; supernumerary tubercles small, present only on proximal segments of digits; palmar tubercle absent; prepollical tubercle elongate. Hind limb robust; tibia length 45.9% SVL; foot length 45.9% SVL; calcar and tarsal tubercles absent; inner tarsal fold prominent on distal half of tarsus; outer metatarsal tubercle absent; inner metatarsal tubercle large, elliptical, barely visible from above; toes long; relative length of toes I <II <III <V <IV; webbing basal between Toes I and II; webbing formula for other toes: II 1— 2 III 1.5— 2 IV 2— 1 V; subarticular tubercles small, rounded; supernumerary tubercles present on proximal segments of digits. Skin on dorsum and flanks weakly granular to smooth; skin on throat, belly, and ventral surfaces of thighs granular, on other surfaces of smooth; cloacal tubercles and folds absent; pouch opening puckered; pouch filled with eggs. Dentigerous processes of the vomers inclined posteromedially, narrowly separated medially, between round choanae, bearing five teeth each.

Coloration in preservative: The dorsum of the head, body, and limbs are gray. A pair of slightly darker paravertebral marks are barely discernible. The flanks are dull brown; the groin is gray with irregular black markings. A fragmented, faint pale gray dorsolateral stripe is bordered below by a fragmented, narrow black stripe; these stripes extend from the thoracic region and the groin. A dark brown canthal stripe is present; a white labial stripe borders the entire margin of the upper lip and extends posteriorly to the base of the forelimb. The posterior surfaces of the thighs are gray with faintly darker small spots or irregular markings. All ventral surfaces are dull tan with small gray spots on the throat and chest.

Coloration in life: No color notes were recorded for the holotype. The coloration is most similar to the individual in Figure 4 C.

Measurements (in mm): SVL 50.8, tibia length 23.3, foot length 23.3, head length 14.8, head width 16.5 interorbital distance 5.0, eyelid width 5.0, internarial distance 3.1, eye–nostril 4.9, eye diameter 5.3, tympanum diameter 4.0, orbit–jaw 2.2, nostril–jaw 4.0, thumb length 10.3, third finger length 17.3, width of disc on third finger 2.3.

G. aguaruna (6 ♂, 3 ♀) G. aratia (8 ♂, 1 ♀)

Character Sex Mean Range SD Mean Range SD

Snout-vent ♂ 45.1 41.6–46.8 2.17* 48.1 42.8–55.7 4.6

length ♀ 50.1 49.4–50.8 – 56.8 – –

Tibia length ♂ 21.8 20.0–22.8 1.17* 22.4 19.7–27.7 2.72 ♀ 25.0 23.3–26.8 – 25.4 – –

Foot length ♂ 22.0 20.1–24.0 1.39 22.4 20.1–26.3 2.33 ♀ 24.4 23.3–25.8 – 25.1 – –

Head length ♂ 16.5 13.9–25.4 4.41 16.3 15.0–18.0 1.09 ♀ 15.8 14.8–16.6 – 18.8 – –

Head width ♂ 17.4 14.8–26.4 4.43 16.8 14.6–19.0 1.54 ♀ 17.2 16.5–18.0 – 19.5 – –

Thumb length ♂ 8.4 7.9–9.5 0.56* 9.0 8.0–10.4 1.03 ♀ 9.9 9.3–10.3 – 10.7 – –

Third finger ♂ 14.9 13.2–15.8 1.10* 15.5 13.5–18.5 1.92 length ♀ 17.2 17.2–17.3 – 18.0 – –

Interorbital ♂ 4.6 4.3–4.8 0.26 4.6 3.8–5.5 0.34

distance ♀ 5.1 5.0–5.3 – 5.3 – –

Internarial ♂ 3.3 2.9–3.7 0.33 3.5 2.9–3.9 0.34

distance ♀ 2.9 2.7–3.1 – 3.4 – –

Eye-nostril ♂ 4.0 3.8–4.2 0.13 4.4 3.5–5.8 0.74 ♀ 4.7 4.1–5.0 – 5.0 – –

Eye diameter ♂ 4.7 4.3–5.5 0.43*** 5.5 5.0–5.9 0.31 ♀ 5.4 5.3–5.5 – 6.9 – –

Tympanum ♂ 2.9 2.5–3.3 0.33** 3.6 3.1–4.5 0.49

diameter ♀ 3.3 2.8–4.0 – 4.4 – –

Eyelid width ♂ 4.4 4.1–5.0 0.34 5.0 4.4–5.9 0.60 ♀ 5.0 4.9–5.0 – 6.3 – –

Orbit-jaw ♂ 2.1 1.9–2.3 0.15** 2.3 2.2–2.4 0.10 ♀ 2.4 2.2–2.6 – 2.6 – –

Nostril-jaw ♂ 3.1 2.7–3.7 0.35* 3.0 2.8–3.5 0.23 ♀ 3.9 3.8–4.0 – 4.1 – –

Disc width ♂ 1.7 1.5–1.9 0.14*** 2.1 1.8–2.5 0.23 ♀ 2.3 2.2–2.3 – 2.2 – –

* Differences between means of sexes in G. aguaruna significant (ANOVA, P<0.01) ** Differences between means for males of the two species significant (ANOVA, P<0.01) *** Differences between means of sexes in G aguaruna significant and differences between means for males of the two species significant (ANOVA, P<0.01).

Variation. The maximum SVL in six males is 46.7 mm and 50.8 mm in three females ( Table 2). The basic dorsal color is green with or without creamy yellow labial and dorsolateral stripes. The dorsum is green with or without faintly distinct darker green or brown paravertebral marks ( Fig. 4 ). Small black flecks are present on the dorsum in some individuals. There is a faint tinge of pale blue on the posterior surfaces of the thighs and in the groin, where small black marks are present. The venter is cream with or without black spots ( Fig. 4 ); the vocal sac in calling males is pale green. The iris is a copper color. The distinctness of a dorsal pattern of a pair of paravertebral marks is shown in figure 3, in which no pattern is evident in KU 212021 ( Fig. 4 A); a faint outline is present in KU 212022 ( Fig. 4 B). The paravertebral marks are faint green, slightly darker than the rest of the dorsum in KU 212024 ( Fig. 4 C); and distinct brown paravertebral marks are evident in KU 212025 ( Fig. 4 D). Breeding males have small brown nuptial excrescences on the medial surface of the thumb; the vocal slits extend posterolaterally from the base of the tongue.

In juveniles from the type locality, the dorsum is uniform green, green with darker green or brown paravertebral marks, or tan with dark brown paravertebral marks The venter is dirty white; the iris is copper. A juvenile from Chachapoyas had a tan dorsum with pale brown blotches edged with dark brown. A subadult found at the edge of a grassy pond 20 km WSW of Leimebamba had a tan dorsum with bright green markings; the venter was cream, and the labial stripe was creamy white.

Distribution and ecology: Gastrotheca aguaruna is known from several localities at elevations of 2360–3308 m in the northern part of the Cordillera Central in Peru ( Fig. 5 ). The type locality is in a valley where the frogs were found on bushes along, and on emergent vegetation in, a sluggish slowly moving marshy stream in a pasture by day. At Chachapoyas three individuals were found on low bushes, and under a clod of dirt by day. At the locality north of Levanto one adult was found under sod in a potato field in cloud forest. Hyloxalus leucophaeus and Scinax oreites were syntopic with G. aguaruna at the type locality; the latter and Pristimantis schultei were found in bromeliads at the locality where G. aguaruna was found north of Levanto.

The referred specimen CORBIDI 380 from the Área de Conservación Privada Huiquilla was in a small pond by day in humid puna above the tree line. CORBIDI 509 and 10933 from Camino Leimebamba-Los Chilchos were basking on leaves of terrestrial bromeliads by day in the humid puna. All specimens from Hornillo were in humid puna above the tree line. Gravid females (CORBIDI 11788–89 and 11794) were basking on the ground by day. At night, males were calling on bushes close to streams. Hornillo and Camino Leimebamba-Los Chilchos are in grassy regions dominated by bunch grass ( Stipa ) with scattered bushes, terrestrial bromeliads, and some scattered patches of elfin forest. In ACP Huiquilla and Camino Leimebamba-Los Chilchos, G. aguaruna was sympatric with Pristimantis melanogaster . At Hornillo, G. aguaruna was sympatric with G. phalarosa , G. phelloderma , and an unidentified species of Pristimantis of the P. orestes group.

Life history: The large number of small eggs in the brood pouches of two brooding females are indicative of eggs that hatch as tadpoles that complete their development in ponds ( Duellman et al. 2001). Metamorphosing young with tail stubs collected at the type locality substantiate this mode of life history.

Etymology. The specific name is a noun in apposition. Aguaruna is the name of the indigenous people of the Andes of northern Peru including the Departamento Amazonas; they never were successfully conquered by the Inca.

Remarks. This species was first discovered at Chachapoyas in May 1970 (KU 138238–41). Subsequently, a few green Gastrotheca were found throughout the geographic range of G. monticola in northern Peru. These specimens were considered to be a color variant of G. monticola until genetic data revealed that they were a separate species. This species apparently is abundant in agricultural areas, as well as in high Andean regions not suitable to agriculture. Thus, we suggest that Gastrotheca aguaruna should be categorized as Least Concern.

Figures

FIGURE 3. Dorsal and ventral coloration of preserved specimens of three species of Gastrotheca. A and D. G. monticola, KU 219771, 57.2 mm SVL, B and E. G. aguaruna, KU 212022, 50.8 mm SVL. C and F. G. aratia, KU 212067, 56.8 mm SVL.

FIGURE 4. Variation in dorsal color pattern among living adults of Gastrotheca aguaruna from the type locality, Molinopampa, Amazonas, Peru. A. KU 212021, male, 42.7 mm SVL. B. KU 212022, female, 50.8 mm SVL. C. KU 212024, male 43.3 mm SVL. D. KU 212025, subadult, 36.8 mm SVL.

FIGURE 5. Topographic map of the Andean region of northern Peru showing localities of known occurrence of Gastrotheca aguaruna (black dots) and G. aratia (red dots), and names of political regions and major mountain ranges discussed in the text.