Pristimantis bounides, Lehr & May & Moravec & Cusi, 2017

Lehr, Edgar, May, Rudolf Von, Moravec, Jiří & Cusi, Juan Carlos, 2017, Three new species of Pristimantis (Amphibia, Anura, Craugastoridae) from upper montane forests and high Andean grasslands of the Pui Pui Protected Forest in central Peru, Zootaxa 4299 (3), pp. 301-336 : 310-317

Pristimantis bounides sp. nov.

Figs 4 & 5

Pristimantis sp. nov.

D in Lehr & von May (2017)

Common name. English: Hill Dweller Rubber Frog. Spanish: Rana cutín de montaña.

Holotype. MUSM 31197 (IWU 182; Figs 4 , 5 ), adult male from the buffer zone of the Pui Pui Protected Forest, Quebrada Tasta , " Runda ", 11° 26' 51.9'' S, 74° 53' 11.9''W, 3463 m a.s.l. ( Fig. 2 , 16 B), Provincia Satipo, Región Junín, collected on 19 May 2012 by E. Lehr and R. von May.

Paratypes. A total of 6 ( Figs 6 , 7 ), from Provincia Satipo, Región Junín: 2 males ( MUSM 31970 , NMP 6 V 75097 [ GenBank accession numbers KY962797 , KY962790 , KY962774 ]) collected with the holotype; 4 females ( MUSM 31198 [ GenBank accession numbers KY962794 , KY962789 , KY962771 ], 31971, NMP 6 V 75066 [ GenBank accession numbers KY962796 , KY962773 ]), 75540 [ GenBank accession numbers KY962795 , KY962772 ], from Sector Carrizal, Satipo-Toldopampa Road at km 134 on left side of street coming from Satipo ( Fig. 16 A), 11° 29' 03.5'' S, 74° 53' 27.3''W, 3350 m a.s.l., collected on 23 June 2013 by E. Lehr, J. C. Cusi, and J. Moravec.

Generic placement. We assign this species to Pristimantis based on molecular evidence ( Fig. 3 ).

Diagnosis. A new species of Pristimantis assigned to the Pristimantis danae species Group having the following combination of characters: (1) Skin on dorsum shagreen with scattered tubercles, skin on flanks tuberculate, skin on venter areolate with scattered low tubercles; discoidal fold and thoracic fold present; irregularly shaped, discontinuous dorsolateral folds present; (2) tympanic membrane and tympanic annulus present; (3) snout moderate, rounded in dorsal and in lateral views; (4) upper eyelid with few enlarged conical tubercles; EW shorter than IOD; cranial crests absent; (5) dentigerous processes of vomers present; (6) males with vocal slits and visible subgular vocal sac, nuptial pads absent; (7) Finger I shorter than Finger II; discs of digits slightly expanded, round, having circumferential grooves; (8) fingers with narrow lateral fringes; (9) minute low ulnar and tarsal tubercles present; (10) heel with a small conical tubercle; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, 1.5 times as large as outer; outer metatarsal tubercle small, rounded; few low supernumerary plantar tubercles; (12) toes with narrow lateral fringes; basal toe webbing present; Toe V longer than Toe III; discs of digits slightly expanded, round, having circumferential grooves, toe discs slightly smaller than those on fingers; (13) in life, dorsal and lateral ground coloration pale grayish brown, orange brown, yellowish brown or reddish brown with dark grayish-brown marmorations, flanks paler than dorsum; canthal and supratympanic stripes grayish brown, not well defined, diffuse; groin pale grayish brown, orange brown, yellowish brown or reddish brown with or without gray flecks; venter pale gray, pale greenish gray or creamish white with or without dark gray mottling; iris pale grayish green with fine black vermiculation, a short vertical black streak from pupil across lower half of iris and a reddish tint horizontally across lower half of iris; (14) SVL in males 18.2–21.0 mm (n = 3), in females 21.6–24.4 mm (n = 4).

Comparisons. Pristimantis bounides sp. nov. is readily distinguished from its congeners in Ecuador (181 species), Peru (130 species), and Bolivia (17 species); AmphibiaWeb (2017), by having discontinuous dorsolateral folds, tuberculate flanks, an areolate venter, slightly expanded digits, and a polymorphic dorsal coloration consisting of pale grayish brown, orange brown, yellowish brown or reddish brown with dark grayish brown marmorations.

Pristimantis bounides sp. nov. is similar to members of the former Pristimantis orestes species Group (considered to be not monophyletic by Duellman & Lehr 2009, not recognized by Padial et al. 2014). This group contained 17 species at high elevations in southern Ecuador and in Peru ( Guayasamin &Artega 2013; Duellman & Lehr 2009), which have narrow digits usually with circumferential grooves (except P. simonsii [ Boulenger, 1900]), and all (except P. simonsii ) have a tympanum. The following five species are morphologically similar to P. bounides sp. nov.: Two species have discontinuous dorsolateral folds ( P. chimu Lehr, 2007 ; P. cordovae [ Lehr & Duellman, 2007b]), whereas three have continuous dorsolateral folds ( P. seorsus Lehr, 2007 ; P. simonsii , P. ventriguttatus Lehr & Köhler, 2007 ). However, P. bounides sp. nov. lacks cranial crests (present in P. chimu ), has males with vocal slits (absent in P. chimu , P. seorsus and in P. simonsii ), discs on digits slightly expanded, round (notched in P. cordovae , broadly expanded, truncate in P. ventriguttatus ), and tarsal fold absent (present in P. seorsus and in P. ventriguttatus ). Furthermore, P. bounides sp. nov. is phylogenetically distant from members of the former P. orestes Group ( P. melanogaster [ Duellman & Pramuk, 1999], P. orestes [ Lynch, 1979], P. simonbolivari [ Wiens & Coloma, 1992], P. simonsii , Fig. 3 ).

Pristimantis bounides sp. nov. shares with other members of the Pristimantis danae species Group ( Fig. 3 ), dorsolateral folds and males (unknown for P. albertus ) which have vocal slits present (absent in P. attenboroughi ) and nuptial pads absent. Furthermore, all but P. attenboroughi and P. puipui sp. nov. have a tympanum and discs with circumferential grooves. Pristimantis bounides sp. nov. is larger than P. albertus (female SVL 21.6–24.4 [n = 4] vs. 19.7–20.7 [n = 2] in P. albertus ; Duellman & Hedges 2007) and has the belly colored pale gray, pale greenish gray or creamish white with or without dark gray mottling (cream with brown mottling in P. albertus ). Pristimantis bounides sp. nov. has dorsal skin shagreen with scattered tubercle (smooth in P. aniptopalmatus ) and ventral skin areolate with scattered low tubercles (smooth in P. aniptopalmatus and P. ornatus ). Pristimantis bounides sp. nov. easily can be distinguished from P. stictogaster which has a white belly with prominent dark brown to black, irregularly shaped spots. Pristimantis bounides sp. nov. is most similar to three other species of the Pristimantis danae species Group from upper montane forests and puna of the PPPF and its surroundings ( Figs 2 , 3 ): P. attenboroughi , P. humboldti sp. nov., and P. puipui sp. nov. All have discontinuous dorsolateral folds, tuberculate flanks, and an areolate venter. Pristimantis bounides sp. nov. and P. humboldti sp. nov. are sister taxa ( Fig. 3 ), and are of similar size (male SVL 18.2–21.0 mm, n = 3 in P. bounides sp. nov. vs. male SVL 17.2–20.6 mm, n = 3 in P. humboldti sp. nov.). Furthermore, P. bounides sp. nov. and P. humboldti sp. nov. have a tympamum (absent in P. attenboroughi and P. puipui sp. nov.), and have expanded discs with circumferential grooves (absent in P. attenboroughi and P. puipui sp. nov.). Males of P. bounides sp. nov., P. humboldti sp. nov., and P. puipui sp. nov. have vocal slits (absent in P. attenboroughi ). However, P. bounides sp. nov. has diffuse canthal and supratympanic stripes (well defined canthal and supratympanic stripes in P. humboldti sp. nov.), interorbital bar absent (present in P. humboldti sp. nov.), scapular without W- or X-shaped marks (W- or X-shaped marks present in P. humboldti sp. nov.), and the venter pale gray, pale greenish gray or creamish white with or without gray mottling (ventral coloration of throat, chest, belly, and anterior ventral surfaces of thighs dark gray and pale gray mottled with white and pale gray spots in P. humboldti sp. nov.).

Description of holotype. Head about as long as wide; head length 38% of SVL, head width 37% of SVL; cranial crests absent; snout moderate, rounded in dorsal and lateral views ( Figs 4 A, B); eye-nostril distance 89% of eye diameter; nostrils slightly protuberant, directed dorsolateral; canthus rostralis rounded in lateral view, straight in dorsal view; loreal region slightly concave; lips rounded; outer margin of upper eyelid with few enlarged conical tubercles; upper eyelid width 54% of IOD; supratympanic fold short and narrow, extending from posterior margin of upper eyelid curved around posterior margin of tympanum; tympanic membrane present, tympanic annulus weakly defined, its upper and posterior margin concealed by supratympanic fold; two conical, slightly fused postrictal tubercles on each side of head. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers positioned posterior to level of choanae, vomerine teeth minute, embedded in buccal mucosa, narrowly separated; tongue long, narrow, about three times as long as wide, not notched posteriorly, posterior half one third free; vocal slits slightly curved, located at posterior half of mouth floor between tongue and margin of jaw; subgular vocal sac distinct.

Skin on dorsum shagreen with scattered tubercles, skin on flanks tuberculate, irregularly shaped, discontinuous dorsolateral folds extending continuously from posterior level of tympanic area to level of mid body, extending discontinuously (separated into tubercles) to level of hind limb insertion; skin on throat smooth, chest and belly areolate with scattered low tubercles; discoidal fold and thoracic fold weakly defined; cloacal sheath short.

Outer ulnar surface of right arm with row of five minute low tubercles, outer ulnar surface of left arm bearing four tubercles; palmar tubercle bifid; thenar tubercle ovoid; subarticular tubercles weakly defined, most prominent on base of fingers, round in ventral view, subconical in lateral view; few, low supernumerary tubercles present, about one third size of subarticular tubercles; fingers with narrow lateral fringes, Finger I shorter than Finger II; nuptial pads absent; discs on digits of fingers slightly expanded, round, having circumferential grooves ( Fig. 5 A).

Hind limbs short, slender, tibia length 45% of SVL; foot length 48% of SVL; dorsal surfaces of hind limbs tuberculate; inner surface of thighs smooth, posterior surfaces of thighs tuberculate, ventral surfaces of thighs areolate; heels each with a small conical tubercle; outer surface of tarsus with few scattered minute low tubercles; inner tarsal fold absent; inner metatarsal tubercle ovoid, one and a half times the size of round outer metatarsal tubercle; subarticular tubercles weakly defined, most prominent on base of toes, round in ventral view, subconical in lateral view; few low plantar supernumerary tubercles, about one third the size of subarticular tubercles; toes with narrow lateral fringes; basal webbing present; discs slightly expanded, round, less expanded than those on fingers, having circumferential grooves; relative length of toes: 1<2<3<5<4; discs on Toe III reaching middle of penultimate subarticular tubercle on Toe IV, Toe V surpassing penultimate subarticular tubercle on Toe IV, but not reaching distal subarticular tubercle on Toe IV; Fig. 5 B).

Measurements of the holotype (in mm). SVL 18.2; tibia length 8.2; foot length 8.8; head length 6.9; head width 6.8; eye diameter 1.8; tympanum diameter 0.9; inter orbital distance 2.4; upper eyelid width 1.3; internarial distance 2.1; eye–nostril distance 1.6.

Characters Pristimantis bounides sp. nov. Pristimantis humboldti sp. nov.

Males (n = 3) Females (n = 4) Males (n = 3) Females (n = 6)

SVL 18.1–21.0 (20.0 ± 1.3) 21.6–24.4 (22.9 ± 1.3) 17.2–20.6 (18.9 ± 1.4) 19.7–25.7 (22.5 ± 1.9) TL 8.2–9.2 (8.8 ± 0.4) 9.9–10.8 (10.3 ± 0.4) 7.8–8.7 (8.3 ± 0.4) 9.2–10.6 (10.1 ± 0.4) FL 8.8–9.9 (9.2 ± 0.5) 9.9–12.0 (10.8 ± 0.9) 8.3–9.0 (8.9 ± 0.5) 9.5–11.2 (10.4 ± 0.5) HL 6.9–7.9 (7.5 ± 0.4) 7.6–8.9 (8.4 ± 0.5) 6.8–8.5 (7.4 ± 0.8) 7.5–8.7 (8.2 ± 0.4) HW 6.8–8.0 (7.6 ± 0.5) 7.7–8.5 (8.0 ± 0.3) 6.1–7.5 (6.9 ± 0.6) 6.9–8.7 (7.8 ± 0.5) ED 1.8–2.2 (2.0 ± 0.2) 2.1–2.5 (2.3 ± 0.2) 2.1–2.2 (2.1 ± 0.0) 2.2–2.6 (2.4 ± 0.2) TY 0.9–1.0 (0.9 ± 0.0) 1.0–1.1 (1.1 ± 0.1) 0.6–0.9 (0.8 ± 0.1) 0.8–1.0 (0.9 ± 0.1) IOD 2.4–2.7 (2.5 ± 0.1) 2.7–3.0 (2.8 ± 0.1) 2.3–2.7 (2.4 ± 0.2) 2.5–3.3 (2.9 ± 0.2) EW 1.3–2.0 (1.7 ± 0.3) 1.4–1.7 (1.6 ± 0.1) 1.3–1.7 (1.5 ± 0.2) 1.4–2.0 (1.7 ± 0.2) IND 2.0–2.3 (2.1 ± 0.1) 2.2–2.5 (2.3 ± 0.1) 1.9–2.3 (2.1 ± 0.2) 2.0–2.6 (2.4 ± 0.2) E–N 1.4–1.8 (1.6 ± 0.2) 1.6–1.9 (1.8 ± 0.1) 1.4–1.7 (1.6 ± 0.1) 1.5–2.2 (1.8 ± 0.2) TL/SVL 0.43–0.45 0.44–0.46 0.42–0.45 0.40–0.49

FL/SVL 0.42–0.48 0.46–0.50 0.46–0.48 0.41–0.49

HL/SVL 0.38 0.35–0.37 0.37–0.41 0.34–0.38

HW/SVL 0.37–0.38 0.33–0.36 0.35–0.38 0.33–0.36

HW/HL 1.00 0.9–1.0 0.9–1.0 0.92–1.0

E–N/ED 0.64–0.95 0.72–0.79 0.64–0.81 0.58–0.88

TY/ED 0.45–0.50 0.40–0.52 0.27–0.43 0.35–0.42

EW/IOD 0.54–0.76 0.50–0.63 0.48–0.74 0.50–0.71 Coloration of the holotype in life ( Fig. 4 ). Dorsal and lateral ground coloration pale yellowish brown with dark grayish-brown marmorations dorsally, flanks paler than dorsum. Canthal and supratympanic stripes grayish brown, not well defined, diffuse. Tympanum creamish white. Interorbital bar narrow grayish brown. Groin pale yellowish brown, anterior surfaces of thighs with a reddish tint. Throat and vocal sac pale yellowish brown, anterior half of chest pale grayish brown, posterior half of chest and belly pale creamish white, thighs pale grayish brown. Iris pale grayish green with fine black vermiculation, a short vertical black streak from pupil across lower half of iris and a reddish tint horizontally across lower half of iris.

Coloration of the holotype in preservative. Dorsal and lateral ground coloration pale tan with grayish-brown marmorations dorsally, flanks paler than dorsum. Canthal and supratympanic stripes grayish brown, not well defined, diffuse. Narrow grayish brown interorbital bar. Groin pale tan, anterior surfaces of thighs pale tan, posterior surfaces of thighs pale grayish brown. Throat, chest, and belly pale tan with small gray dots, and narrow gray midventral line across chest and belly. Lower arms pale tan with narrow gray midventral line, tarsi and ventral surfaces of thighs pale grayish brown and tan mottled. Iris pale gray with fine black vermiculation.

Variation. All paratypes ( Figs 6 , 7 ) are similar to the holotype regarding morphology and proportions ( Tables 3, 4). Besides differences in SVL, notable morphological variation includes prominence of dorsolateral folds. Two females (MUSM 31971, NMP 6 V 75540; Figs 7 E, H) have prominent dorsolateral folds of pale grayish coloration on dark grayish brown dorsum. Most striking is the coloration polymorphism which resembles the color range of plants the frogs inhabit ( Fig. 16 C). The dorsal and lateral ground coloration is pale grayish brown (MUSM 31971, NMP 6 V 75540; Figs 7 D, G), orange brown (NMP 6 V 75097; Fig. 6 B), pale yellowish brown (MUSM 31198; Fig. 7 B) or reddish brown (MUSM 31970; Fig. 6 E) with dark grayish-brown marmorations. The dorsum and flanks have reddish brown flecks in one male (MUSM 31970; Fig. 6 E), pale yellowish brown in one female (MUSM 31198; Fig. 7 B), and orange in one female (NMP 6 V 75540; Fig. 7 E). Flanks are paler than dorsum. Males have the throat and vocal sac pale grayish orange (MUSM 31970; Fig. 6 F) or salmon ((NMP 6 V 75097; Fig. 6 C). The venter is pale gray (NMP 6 V 75540, Fig. 7 F; MUSM 31970, Fig. 6 F; MUSM 31971, Fig. 7 I; NMP 6 V 75066), pale greenish gray (NMP 6 V 75097; Fig. 6 C) or creamish white (MUSM 31198; Fig. 7 C) with or without dark gray mottling.

Etymology. The species epithet bounides is derived from the Greek noun “bounos” and means "dweller in the hills". The name refers to the habitat of montane forests where the new species was found.

Distribution, natural history, and threat status. Pristimantis bounides sp. nov. is known from two locations in the humid montane forest ecoregion ( Brack 1986, Figs 2 , 16 A, B): the type locality in the Tasta valley, "Runda" at 3463 m a.s.l (7.5 km [airline] from the border of PPPF), and the Satipo-Toldopampa Road at km 134 on left side of street coming from Satipo at 3350 m a.s.l. (4.2 km [airline] from the type locality). The vegetation at the type locality consists of Peruvian feather grass ( Stipa ichu), large layers of mosses, small bushes, trees, and forest patches ( Fig. 16 B). The vegetation is disturbed by cattle breeding and deforestation. The male holotype was found calling from the center of Peruvian feather grass in the early afternoon on 19 May 2012 during light rain. No sympatric anuran species were found at the type locality.

At km 134 of the Satipo-Toldopampa Road, calling males were heard from the moss layer in the early afternoon on 23 June 2013. On the same day a female P. bounides sp. nov. (NMP 6 V 75540; Fig. 16 C) guarding 20 eggs was found there inside moss. The eggs were pale cream colored and had an average diameter of 3.4 ± 0.1 mm (3.2–3.7 mm, n = 20). Sympatric anurans include Phrynopus sp. A (IWU 285) and Gastrotheca griswoldi Shreve, 1941 (MUSM 31972).

We propose that Pristimantis bounides sp. nov. should be classified as "Data Deficient" according to the IUCN Red List criteria and categories (IUCN Standards and Petitions Subcommittee 2016) based on the low number of specimens known. Threats include agriculture and cattle breeding in both valleys, more acute in the Toldopampa valley than in the Tasta valley.

Figures

FIGURE 2. Pui Pui Protected Forest indicated in red outline with type localities of Pristimantis bounides sp. nov., P. humboldti sp. nov., and P. puipui sp. nov.

FIGURE 3. Bayesian maximum clade-credibility tree for species included in this study based on a 2181 - bp concatenated partitioned dataset (16 S, 12 S, COI, RAG 1) analyzed in MrBayes (posterior probabilities are indicated at each node). Photographed frogs (from top to bottom): Pristimantis puipui sp nov., P. attenboroughi, P. humboldti sp. nov., and P. bounides sp. nov.

FIGURE 4. Life male holotype (MUSM 31197, SVL 21.0 mm) of Pristimantis bounides sp. nov. in dorsolateral view (A), dorsal view (B), flanks, groin, anterior surfaces of thighs (C), and ventral view (D). Photos (A, B, D) by E. Lehr and (C) by R. von May.

FIGURE 5. Ventral views of left hand (A) and left foot (B) of holotype of Pristimantis bounides sp. nov. (MUSM 31197). Drawings by E. Lehr.

FIGURE 6. Variation of male paratypes of Pristimantis bounides sp. nov. in dorsolateral, dorsal, and ventral views. A – C (NMP 6 V 75097, SVL 21.0 mm), D – F (MUSM 31970, SVL 20.8 mm). Photos (A – C) by R. von May, (D, E) by E. Lehr, and (F) by J. C. Cusi.

FIGURE 7. Variation of female paratypes of Pristimantis bounides sp. nov. in dorsolateral, dorsal, and ventral views. A – C (MUSM 31198, SVL 23.9 mm), D – F (NMP 6 V 75540, SVL 21.7 mm), G – I (MUSM 31971, SVL 21.6 mm). Photos by E. Lehr.

FIGURE 16. Type localities and habitats of Pristimantis bounides sp. nov. (A – C), P. humboldti sp. nov. (D, E), and P. puipui sp. nov. (F – H). A: Satipo-Toldopampa Road at km 134 on left side of street coming from Satipo, 3350 m a. s. l., 23 June 2013; B: type locality Quebrada Tasta, " Runda ", 3463 m a. s. l., 19 May 2012; C: female P. bounides sp. nov. (NMP 6 V 75540) guarding 20 eggs inside a moss pad at Satipo-Toldopampa Road at km 134, in the early afternoon on 23 June 2013; D, E: type locality Pui Pui Protected Forest, Quebrada Tarhuish, left bank of Antuyo River, " Shiusha ", 3318 m a. s. l., 14 May 2012; F, G: type locality Pui Pui Protected Forest, Laguna Sinchon, 3890 m a. s. l., 30 June 2013; H: female P. puipui sp. nov. (NMP 6 V 75542) guarding eggs inside a moss pad (G). Photos by E. Lehr, J. C. Cusi (G), and R. von May (B).