Oreobates crepitans ( Bokermann, 1965 ) Padial & Chaparro & Castroviejo-Fisher & Guayasamin & Lehr & Delgado & Vaira & Teixeira & Aguayo & Riva, 2012

Padial, Jose M., Chaparro, Juan C., Castroviejo-Fisher, Santiago, Guayasamin, Juan M., Lehr, Edgar, Delgado, Amanda J., Vaira, Marcos, Teixeira, Mauro, Aguayo, Rodrigo & Riva, Ignacio De La, 2012, A revision of species diversity in the Neotropical genus Oreobates (Anura: Strabomantidae), with the description of three new species from the Amazonian slopes of the Andes, American Museum Novitates 2012 (3752), pp. 1-56 : 29-38

Oreobates crepitans ( Bokermann, 1965) , new combination

Figure 7

Eleutherodactylus crepitans Bokermann, 1965: 262 .

Pristimantis crepitans: Heinicke et al., 2007 : Supplementary information table 2

Pristimantis (Pristimantis) crepitans: Hedges et al., 2008a: 165 .

Oreobates crepitans ( Bokermann, 1965) was described from a tableland of the Brazilian shield near São Vicente, a locality located in the Cerrado forest of Mato Grosso, Brazil, not far from the northeastern Bolivian border (map

1). The original description of the species is very accurate and the species is readily distindB 0 guishable, but it was placed in the synonymy of Eleutherodactylus fenestratus by Lynch

(1980), from where it was resurrected by

Heyer and Muñoz (1999), a position later sup- 12 ported by Padial and De la Riva (2005). Sub-) 11 sequently, it was transferred to Pristimantis kHz 10 9 ( Hedges et al., 2008a). Recent examination of (Frequency 5 8 6

7 2

3 4 7 the lum Oreobates ) and paratype at the MNRJ by holotype of Padial Eleutherodactylus (a Cerrado et of al Telatrema., 2008 species a) crepitans has heterodactyplaced led us (fig to in.

1 conclude that the species indeed belongs to

0

0 1.0 Oreobates . Oreobates crepitans has enlarged

Time (s)

conical and subconical tubercles on plantar FIG. 6. Oscillogram and sound spectrogram of the surfaces, and lacks circumferential grooves on advertisement call of Oreobates ayacucho , recorded on finger discs. Nonetheless, it has a characteristic

28 February 2008

at

12:15 h in the Andean

puna

that differentiates it from all other Oreobates between Punki and Anco, 3850 m, Ayacucho, Peru (temperature not recorded). The specimen voucher is described to date: it has a subgular vocal sac the one depicted in figure 6A–B. only slightly developed. The only other direct-

developing frogs from the lowlands (i.e., not from the Andes or from the Mata Atlantica) that are similar to O. crepitans are members of Ischnocnema and Pristimantis from the P. conspicillatus group. Members of the P. conspicillatus group east of the Andes have disc structures with circumferential grooves, and supernumerary tubercles are absent or are not large and conical ( Padial and De la Riva, 2009). Some species of Ischnocnema resemble members of Oreobates and some also have expanded discs, but when these are present they have circumferential grooves ( Hedges et al., 2008a). Moreover, no species of Ischnocnema is known to reach the Cerrado in western Brazil. In addition, O. crepitans has some characteristics that distinguish it from O. heterodactylus , which also inhabits the Cerrado in the same region. Although the type of O. heterodactylus is poorly preserved, strongly enlarged finger discs (FIII, FIV) are still evident, where O. crepitans has moderately enlarged discs. The type localities of both species are far apart (ca. 300 km; Miranda-Ribeiro, 1937; Heyer and Muñoz, 1999). Moreover, Bolivian populations assigned by Padial and De la Riva (2005) to O. heterodactylus might indeed represent a third species. Bolivian populations inhabit a distant outcrop of the Brazilian shield, ca. 500 km southwest (map 1); they have smooth skin (warty in nominal O. crepitans ) and less-developed finger discs than the type of O. heterodactylus . However, a rigorous reassessment of the identity of the Bolivian populations would require gathering additional specimens from the type localities of O. crepitans and O. heterodactylus to assess intraspecific variation.

Oreobates gemcare , new species Figures 3C–D, 8, and 9A HOLOTYPE: MHNC 6687 (field number IDlR 4826), an adult male from Esperanza (13.1824°S, 71.6036°W; 2700 m above the sea level), Kosñipata Valley, Departamento Cusco,

FIG. 7. Male paratopotype of Eleutherodactylus crepitans Bokermann, 1965 from São Vicente, Cuiba, Mato Grosso, Brazil ( MNRJ 3985 , SVL 27.7 mm) .

Peru (map 2), one of a series collected on 11th February 2007 by I. De la Riva, J.M. Padial, S. Castroviejo-Fisher and J.C. Chaparro (fig. 3C–D, fig. 8A).

PARATYPES: AMNH 11831, an adult male from Pillahuata (13°09′52″S, 71°35′46″W; 2430 m) between Puente Kosñipata and road, Departamento Cusco, Peru (map 2), collected by L.O. Rodríguez on 15 January 1998. MNCN 44230 (field number IDlR 4827) an adult male from Esperanza (13.1824°S, 71.6036°W; 2700 m), Kosñipata Valley, Departamento Cusco, Peru (map 2), collected on 11th February 2007 by I. De la Riva, J.M. Padial, S. Castroviejo-Fisher and J.C. Chaparro. New museum numbers for MHNC are provided here (old museum numbers used for the original description of O. lehri in parenthesis): MHNC 4557 (MHNC 3223), 4564–4567, (MHNC 3224–3227) MHNC 4583–4586 (MHNC 3228–3231), MHNC 4587 (MHNC 3232), MHNC 4589 (MHNC 3233), MHNC 4601–4602 (MHNC 3234–3235) MHNC 4682–4683 (MHNC 3236–3237) MHNC 4389 (MHNC 3238), MHNC 4218 (MHNC 3239) and MNCN 43740–1, Esperanza (13° 10′ 56″ S, 71° 36′ 227″ W; 2600–2800 m), Kosñipata Valley, Departamento Cusco, Peru (map 2), collected by Juan C. Chaparro and A. Mendoza between 26th January to 23rd February 2003 (MHNC 4557, 4564, 4602, 4683 and MNCN 43741, adult males; FIG. 8. A. Adult male holotype of Oreobates gemcare from Esperanza, Kosñipata Valley, 2700 m, Cusco, Peru (MHNC 6687, SVL 33.5). B. Adult male paratype of O. gemcare from Esperanza, Kosñipata Valley, 2700 m, Cusco, Peru (MNCN 44230, SVL 33.6). C. Adult male of O. gemcare from Esperanza, Kosñipata Valley, 2790 m, Cusco, Peru (MHNC 10792, SVL 28.2). D. Adult male paratype of O. gemcare from Esperanza, Kosñipata Valley, 2700 m, Cusco, Peru (MHNC 4564, SVL 32.1).

MHNC 4683 and MNCN 43740, adult females; MHNC 4565, 4601, subadult females; MHNC 4566–4567, 4583–4586, juveniles).

DIAGNOSIS: A robust Oreobates (SVL of adult females 35.5–39.9; adult males 31.8–34.3) characterized as follows: (1) skin on dorsum shagreen with enlarged granules and low warts, granules regular in size, small, round, flat, some slightly enlarged; granules scarce on flanks, but slightly larger than those of dorsum; venter smooth; posterior surfaces of limbs smooth; discoidal fold present; dorsolateral folds irregular, formed by connected granular warts, or absent; postrictal glands present, large, prominent; (2) tympanic membrane and annulus distinct, their length about half eye length; supratympanic fold present, conspicuous; (3) head large, as long as wide or longer; snout round in dorsal and lateral views; canthus rostralis straight in dorsal view, round in profile; (4) cranial crests absent; upper eyelid covered by small granules; (5) dentigerous process of vomers large, situated posteromedial to choanae; (6) males with vocal slits, nuptial pads absent; (7) hands with long and slender fingers, first finger about same length as second; subarticular tubercles round to conical, well developed; supernumerary tubercles prominent, round to conical, smaller than subarticular tubercles; terminal discs of fingers truncate to round, not enlarged, lacking circumferential grooves and ungual flap; lateral fringes and keels on fingers absent; (8) ulnar tubercles absent, round, low; (9) tubercles absent on heel and tarsus; (10) inner metatarsal tubercle ovate to round, prominent, outer smaller, round, prominent; supernumerary tubercles absent; (11) toes long, slender (foot length 60%– 70% SVL), lacking lateral fringes or keels (or very weak at the base of toe III), webbing absent; toe III and V reaching midpoint of second subarticular tubercle of toe IV; tips of toes moderately enlarged, rounded, with ungual flap not indented; (12) axillary glands present; (13) dorsal FIG. 9. Details of the dorsal skin of A. Oreobates gemcare , B. O. lehri , and C. O. machiguenga . FIG. 10. Cloud forests around the type locality of Oreobates gemcare in the Kosñipata Valley, 2700 m, Cusco, Peru.

coloration in life pale to dark brown or grayish brown with darker color marks and bold spots, pair of cream dorsolateral stripes, and short longitudinal sacral stripe in some specimens; snout dark brown with darker bars; throat and chest light grey to dark brown; belly cream with brown mottling or reticulations on anterior margin; hidden surfaces of arms and shanks orange or with orange or yellow blotches.

Oreobates gemcare is distinguished from all other species of the genus (except O. lehri ) by the combination of long feet (≥ 60% SVL), presence of supratympanic fold, absence of supernumerary tubercles on feet, round not enlarged fingertips, shagreen dorsal skin with enlarged granules, and by having orange hidden surfaces of extremities. Oreobates gemcare and O. lehri are morphologically similar and the only conspicuous difference between them is skin texture (compare fig. 9A and 9B). In O. lehri , the dorsal skin is homogeneously granular, with small, low granules covering every spot on the dorsal skin. In O. gemcare granules do not cover all areas of flanks and dorsum, and granules are irregular in size. In addition, large warts appear in the dorsum, which are covered with granules, some of them forming incomplete dorsolateral folds. In life, they differ in coloration; O. gemcare is mostly brown, whereas in O. lehri green patterns prevail (fig. 5C). Also, O. gemcare is more robust and larger than O. lehri (adult females 35.5–39.9 in O. gemcare vs. 31.0– 32.9 in O. lehri ). Oreobates gemcare also is similar to O. machiguenga (character of O. machiguenga in parentheses), from which it can be distinguished by longer feet, FL/SVL = 60–70% (50%), by lacking basal membrane between toes III and IV (present), by having a well developed supratympanic fold (absent), by having a dorsal skin shagreen with most granules being poorly elevated and poorly defined (skin coarsely shagreen, granules very conspicuous and elevated), and by lacking prominent conical supernumerary tubercles on hands (well developed). In addition, O. gemcare can be distinguished from O. barituensis , O cruralis , O. discoidalis , O. heterodactylus , O. ibischi , O. lundbergi , and O. remotus by having fingertips not enlarged (enlarged on finger III and IV), and from O. ayacucho and O. pereger , by lacking well-defined dorsolateral folds (present), and by having a smooth belly (areolate in O. ayacucho ), and lacking papillae on finger discs (present in O. pereger ).

FIG. 11. Adult female holotype of Oreobates machiguenga from Río Kimbiri , 1400 m, Cusco, Peru ( MHNC 6809 , SVL 32.7 ) .

DESCRIPTION OF THE HOLOTYPE: Head longer than wide; snout round in dorsal view and in profile; nostrils slightly protuberant, oriented laterally; canthus rostralis sinuous in dorsal view, round to slightly sharp in frontal profile; loreal region slightly concave, sloping gradually to lips; lips not flared; upper eyelid without tubercles but covered by small granules; cranial crests absent. Supratympanic fold distinct, conspicuous; tympanic membrane and its annulus distinct; tympanic membrane nearly round, its length about half length of eye; postrictal gland large, sharp and elongated. Choanae not concealed by palatal shelf of the maxillary arch when roof of mouth is viewed from below; choanae large, round, medial,

separated by distance equal to 6–7 times diameter of choana; dentigerous processes of vomers large,

prominent, triangular in shape, situated posteromedial to choanae (posterior margin at level of choanae), their width about 1.5 times diameter of choanae, bearing 3–2 vomerine teeth; vocal slits short, placed posterolaterally. Skin of dorsal surfaces and posterior parts of hind limbs shagreen with enlarged granules and low warts also covered with granules; dorsolateral folds low and inconspicuous, incipient, formed by granular warts;

ventral surfaces smooth; W-shaped occipital fold weak; discoidal fold conspicuous, posterior surfaces of thighs areolate.

Ulnar tubercles present; palmar tubercle large, cordiform, flat, larger than elongate, prominent thenar tubercle; supernumerary tubercles prominent, round to conical; subarticular tubercles round to subconical, larger than supernumerary tubercles; fingertips round, not enlarged, of same width as corresponding digits; fingers FIG. 12. Montane forests of Río Kimbiri at ca.

1400 m, near the type locality of Oreobates lacking lateral fringes and keels; relative length

machiguenga , on the western slopes of Cordillera of fingers: III> I> IV ≈ II. Vilcabamba, Cusco, Peru. Toes long and slender (foot length 60% of

SVL); heel and tarsus lacking tubercles or folds; inner metatarsal tubercle large, oval prominent,

larger than outer metatarsal tubercle; metatarsal tubercle prominent, inclined, conical; supernumerary tubercles absent; subarticular tubercles prominent, round to conical, inclined; toes without lateral fringes and keels, except thin, short keel at base of internal side of toe III; toe tips rounded, slightly enlarged; ungual flap not indented; relative length of toes IV> III> V≈

II> I; toe III and V reaching penultimate subarticular tubercle of toe IV.

In preservative, dorsal surfaces brown with one dorsolateral pale brown stripe on each side of dorsum, from posterior margin of eyelid almost to groin; dorsum brownish gray with black blotches, and W-shaped occipital black mark, an interocular dark color triangle, and two sym-

metrical middorsal black marks (occipital W-shaped, and middorsal inverted Y-shaped); dorsolateral folds cream; granules on dorsum gray; short cream stripe on sacrum; flanks yellowish gray with dark gray to black blotches; canthus dark brown, almost black; three black labial bars,

two of them subocular; tympanic membrane dark brown; tympanic fold black. Limbs pale brown with diffuse transverse bars; hands and feet slightly paler brown; plantar surfaces gray.

Throat brownish-gray with cream mottling; chest, belly, and groin cream with fine brown mottling; posterior and anterior surfaces of hind limbs cream with dense brown mottling. FIG. 13. Adult female holotype of Hylodes philippi from San José de Moti (= San José de Mote o Nuevo), Napo, Ecuador ( MNCN 1599 , formerly MNCN 1155 , SVL 49.5 ). This is the specimen figured on plate 3bis, figure 1 of Jiménez de la Espada (1875) .

MEASUREMENTS OF THE HOLOTYPE: SVL, 33.5; HL, 11.2; HW, 12.5; EL, 3.2; END, 3.7; IND, 3.3; EE, 5.7; TYH, 2.7; TYL, 2.4; FA, 8.8; TL, 20.6; TH, 18.85; FL, 19.6.

VARIATION: Females are larger than males, and proportions are almost identical (see table 4). Males have posterolateral vocal slits but no nuptial pads. Skin texture is homogeneous, although there are more enlarged granules in some specimens than in others. A faint middorsal fold is present in some individuals, as in the holotype. The degree of development of W-shaped occipital fold and)(-shaped middorsal ridges is variable. Dorsal color patterns vary from dark brown with some irregular bold marks to pale reddish brown with irregular brown marks, some of which are outlined with cream. Common dorsal marks are an occipital W-shaped mark, an arrow-shaped middorsal mark, and a transversal irregular ellipse in the presacral region. A vertical pale color sacral stripe is present in all but some specimens. Some specimens have a dorsolateral cream stripe on each side of dorsum, from posterior margin of eye to the level of middorsum or to groin. Bold spots and lines usually outline the W-shaped occipital fold, the supratympanic fold, the) (-shaped middorsal fold, and the upper marging of flanks. Labial bars also vary; darker individuals have less conspicuous bars. The tympanic membrane and annulus are brown in all specimens. The throat pattern varies from pale gray to dark brown. Some specimens have a fine light cream line in the middle of the throat. The chest usually is mottled which diminishes on the belly. The belly varies from white to cream and usually has fine brown mottling on the sides and anterior margin. Transversal irregular bars or irregular ellipses are present on the dorsal surfaces of the Table 4. Morphometrics of two adult females and seven adult males of Oreobates gemcare . Mean ± standard deviation in parentheses follows range (in mm). For abbreviations see Material and Methods.

hind limbs, irregular brown marks are present on the arms. Plantar surfaces vary from dark gray to dark brown with gray or cream plantar tubercles.

In life (based on MHNC 3224, and MNCN 44230) the dorsum is pale brown to dark brown or reddish brown, with irregular dark brown or black spots and marks surrounded by beige, and some small red or orange spots. Some of the dorsolateral warts are black, and the flanks are mostly pale brown to gray with black blotches. The lips have three bold black bars, two subocular separated by cream spots. The tympanic membrane is pale brown. The belly is white, and the throat has brown mottling. The inner surfaces of limbs are red to orange. The axillae and shoulders have yellow and/or orange blotches, and the hind limbs and arms are brown with dark brown irregular bars. The iris is golden dorsally and ventrally, with a bronze transverse stripe. The pupil has a black ventral notch.

DISTRIBUTION AND ECOLOGY: Oreobates gemcare is known from cloud forests in the Kosñipata Valley, Departamento Cusco, Peru (map 2) at elevations of 2400–2800 m (fig. 10). The frogs were active at night on the ground during the rainy season, and males called from the leaf litter. The call consisted of a single pulsed note.

ETYMOLOGY: The species epithet is used as a substantive in apposition and refers to the company name GEMCare (Golden Empire Managed Care) , a medical group that supported J.C.C.’s taxonomic research in southern Peru.

COMMENTS: Except for the specimens MHNC 6687 and MNCN 44230, all specimens of the type series of O. gemcare were originally part of the type series of O. lehri ( Padial et al., 2007) . The name O. lehri was initially ascribed to two distant populations (200 km airline distance), one in Cordillera Vilcabamba, which is now considered typical O. lehri , and one in the Andean hills of the Kosñipata Valley, to which we now assign the name O. gemcare . Although Padial et al. (2007) were aware of differences between specimens from both populations, they refrained from recognizing them as different species until living individuals of both populations were available for more accurate comparisons and genetic analysis. Because the diagnosis of O. lehri ( Padial et al., 2007, 2008a) was based on specimens of what are now recognized as O. lehri and O. gemcare , we provide a new diagnosis and distributional account for O. lehri .

Figures

FIG. 1. Main tree (left and right pages): one of 16 equally optimal maximum parsimony trees with branch length depicting phylogenetic relationships of species of Oreobates (3936 steps; differences with the strict consensus only affect unresolved intraspecific relationships). Schematic tree (far left): maximum likelihood best tree topology for 145 terminals of Strabomantid frogs inferred from the 16S rRNA barcode fragment of amphibians (see methods). Numbers above nodes for both trees are maximum parsimony bootstrap values followed by maximum likelihood bootstrap values.