Pristimantis puipui, 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 : 324-330

Pristimantis puipui sp. nov.

Figs 12 & 13

Pristimantis sp. nov. E in Lehr & von May (2017)

Common name. English: Pui Pui Rubber Frog. Spanish: Rana cutín de Pui Pui.

Holotype. MUSM 31982 (IWU 303; Figs 12 , 13 ), adult male from the Pui Pui Protected Forest, Laguna Sinchon , puna, 11° 16' 56.3''S, 75° 03' 11.7''W, 3890 m a.s.l. ( Figs 16 F, G), Provincia Satipo, Región Junín, collected on 30 June 2013 by E. Lehr, J.C. Cusi, and J. Moravec.

Paratypes. A total of 6 ( Figs 14 , 15 ), all collected with the holotype: 4 females (NMP 6 V 75056, 75541, 75542 [GenBank accession numbers KY962800 , KY962777 ], MUSM 31981), 2 males (MUSM 31983, NMP 6 V 75057).

Generic placement. We assign this species to Pristimantis based on molecular evidence ( Fig. 2 ).

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 low scattered tubercles, skin on flanks tuberculate, skin on venter areolate; discoidal fold absent, thoracic fold present; irregularly shaped, discontinuous dorsolateral folds present; (2) tympanic membrane and tympanic annulus absent; (3) snout short, rounded in dorsal and in lateral views; (4) upper eyelid without enlarged conical tubercles; EW shorter than IOD; cranial crests absent; (5) dentigerous processes of vomers present; (6) males with vocal slits, subgular vocal sac not discernible, nuptial pads absent; (7) Finger I shorter than Finger II; tips of digits narrow, rounded, lacking circumferential grooves; (8) fingers without lateral fringes; (9) small conical ulnar and tarsal tubercles present; (10) heel without tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, half the size of outer; outer metatarsal tubercle prominent, rounded; supernumerary plantar tubercles absent; (12) toes without lateral fringes; basal toe webbing absent; Toe V longer than Toe III; tips of digits narrow, rounded, lacking circumferential grooves, toe discs slightly smaller than those on fingers; (13) in life, dorsum and flanks pale orange brown, reddish brown or grayish brown with or without grayish-brown mottling, flanks paler than dorsum; canthal and supratympanic stripes absent; groin colored as flanks; venter pale cream and pale gray mottled; iris pale grayish green with fine black vermiculation and dark brown horizontal streak across pupil and lower half of iris; (14) SVL in males 16.1– 17.1 mm (n = 3), in females 20.6–22.4 mm (n = 4).

Comparisons. Pristimantis puipui sp. nov. shares having narrow digits without circumferential grooves and the absence of a tympanic annulus and tympanic membrane with the Andean genera Phrynopus Peters, 1873 (except for Phrynopus auriculatus Duellman & Hedges, 2008 , and P. peruanus Peters, 1873 , 32 species between 2200 and 4400 m a.s.l. in central and northern Peru; Duellman & Lehr 2009, Frost 2017) and Bryophryne Hedges, Duellman & Heinicke, 2008 (except for B. flammiventris Lehr & Catenazzi, 2010 and B. gymnotis, Lehr & Catenazzi, 2009 , 9 species between 2900 and 4120 m a.s.l. in southern Peru; Duellman & Lehr 2009, Frost 2017).

Pristimantis puipui sp. nov. is readily distinguished from its congeners in Ecuador (181 species), Peru (130 species), and Bolivia (17 species); AmphibiaWeb (2017), by having tips of digits narrow without circumferential grooves, by lacking a tympanic annulus and tympanic membrane, and by having irregularly shaped, discontinuous dorsolateral folds. In Peru 19 species of Pristimantis lack a tympanum. These are P. academicus Lehr, Moravec & Gagliardi Urrutia, 2010 , P. altamazonicus ( Barbour & Dunn, 1921) , P. ashaninka , P. attenboroughi , P. colodactylus ( Lynch, 1979) , P. coronatus Lehr & Duellman, 2007a , P. croceoinguinis ( Lynch, 1968) , P. cruciocularis (Lehr, Lundberg, Aguilar & von May, 2006), P. flavobracatus (Lehr, Lundberg, Aguilar & von May, 2006), P. imitatrix ( Duellman, 1978b) , P. lirellus ( Dwyer, 1995) , P. leucorrhinus Boano, Mazzotti & Sindaco, 2008 , P. martiae ( Lynch, 1974) , P. minutulus Duellman & Hedges, 2007 , P. rhabdocnemus ( Duellman & Hedges, 2005) , P. simonsii , P. tantanti ( Lehr, Torres-Gastello & Suárez-Segovia, 2007) , P. ventrimarmoratus ( Boulenger, 1912) , and P. vilcabambae Lehr, 2007 . Of these, only P. attenboroughi and P. simonsii (member of the former Pristimantis orestes species Group, not recognized by Padial et al. 2014) share with P. puipui sp. nov. the characteristics of having narrow digits without circumferential grooves. Besides digit morphology and absence of a tympanum, P. puipui sp. nov. shares with P. attenboroughi , from the upper montane forests and puna of the PPPF and its buffer zone, a similar SVL (16.1–17.1 mm vs. 14.6–19.2 mm in males of P. attenboroughi, Lehr & von May 2017), tuberculate flanks, irregularly shaped, and discontinuous dorsolateral folds. However, males of P. puipui sp. nov. have vocal slits (absent in P. attenboroughi ), and dorsum and flanks pale orange brown, reddish brown or grayish brown (pale or dark gray, reddish brown or brownish olive with dark gray scattered flecks), and venter pale cream and pale gray mottled (dark gray, pale gray, grayish brown or pale grayish green with or without dark gray mottling). Pristimantis puipui sp. nov. is smaller than P. simonsii from northern Peru (SVL in males 19.3–25.9 mm in P. simonsii, Lynch 1975 ), lacks an inner tarsal fold (present), and has males with vocal slits (absent) which lack nuptial pads (present).

Pristimantis puipui 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. However, P. puipui sp. nov. and P. attenboroughi are the only members of the Pristimantis danae species Group that lack both a tympanum and discs with circumferential grooves.

Description of holotype. Head about as long as wide; head length and head width 35% of SVL; cranial crests absent; snout short, rounded in dorsal and in lateral views ( Figs 12 B, C); eye-nostril distance 56% of eye diameter; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis short, rounded in lateral view, weakly concave in dorsal view; loreal region concave; lips rounded; upper eyelid with few small tubercles; upper eyelid width 57% of IOD; supratympanic fold broad, extending from posterior margin of upper eyelid slightly diagonally to insertion of arm; tympanic membrane and annulus absent; postrictal tubercles fused into a low ridge 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, oval, about two times as long as wide, not notched posteriorly, posterior third free; vocal slits short, slightly curved, located at posterior fifth of mouth floor between tongue and margin of jaw; subgular vocal sac not discernible.

Skin on dorsum shagreen with low scattered tubercles, skin on flanks tuberculate, irregularly shaped, discontinuous dorsolateral folds extending from level of arm insertion to anterior level of hind limb insertion; skin on throat smooth, skin on chest, and belly areolate; discoidal fold absent, thoracic fold present; cloacal sheath short. Outer ulnar surfaces each with a row of three minute low tubercles; palmar tubercle bifid; thenar tubercle ovoid; subarticular tubercles weakly defined, more distinct on base of fingers, round in ventral and lateral views; supernumerary tubercles absent; fingers short and stout lacking lateral fringes, Finger I shorter than Finger II; tips of digits of fingers narrow, round, lacking circumferential grooves ( Fig. 13 A).

Hind limbs short, slender, tibia length 40% of SVL; foot length 39% of SVL; dorsal surfaces of hind limbs tuberculate; inner surface of thighs smooth, posterior surfaces of thighs tuberculate, ventral surfaces of thighs areolate; heels lacking conical tubercles; outer surface of tarsus with few scattered minute low tubercles; inner tarsal fold absent; inner metatarsal tubercle ovoid, one and a half times smaller than round outer metatarsal tubercle; subarticular tubercles weakly defined, round in ventral and lateral views; plantar supernumerary tubercles absent; toes without lateral fringes; basal webbing absent; tips of digits narrow, round, slightly smaller than those on fingers, lacking circumferential grooves; relative length of toes: 1<2<3<5<4; Toe V slightly longer than Toe III (tips on Toe III and Toe V reaching penultimate subarticular tubercle on Toe IV; Fig. 13 B). Left foot has four toes, lacking Toe II. Ectoparasitic mite ( Trombiculidae ) infestations are present with mite capsules on upper left arm (2 capsules), on upper right arm (1), posterior surface of left thigh (1), and on ventral right tibia (1).

Measurements of the holotype (in mm): SVL 16.1; tibia length 6.5; foot length 6.2; head length 5.7; head width 5.6; eye diameter 1.8; inter orbital distance 2.3; upper eyelid width 1.3; internarial distance 1.7; eye–nostril distance 1.0.

Coloration of the holotype in life ( Fig. 12 ). Dorsal and lateral ground coloration pale orange brown, flanks slightly paler than dorsum. Canthal, supratympanic stripes, and labial bars absent, but rim of canthus rostralis and outer edge of upper eyelid pale gray. Groin colored as flanks. Anterior surfaces of thighs pale grayish brown, posterior surfaces of thighs colored as flanks. Throat pale cream, chest, belly, and thighs pale creamish white and gray mottled. Pale grayish-brown line ventrally across arms and chest, and midventrally across throat, chest, and belly. Iris pale grayish green with fine black vermiculation and dark brown horizontal streak across pupil and lower half of iris.

Coloration of the holotype in preservative. Dorsum pale tan and brown mottled, flanks pale gray and brown mottled. Throat pale cream with tiny brown spots, chest and belly pale cream and gray mottled, posterior surfaces of thighs pale cream and brown mottled. Fine dotted brown narrow line ventrally across arms and chest and midventrally across throat, chest, and belly. Iris gray with black vermiculation.

Variation. All paratypes ( Figs 14 , 15 ) are similar to the holotype regarding morphology and proportions ( Tables 3, 4). Coloration in life is weakly polymorphic. Dorsum and flanks are pale orange brown (MUSM 31981, NMP 6 V 75542; Figs 15 D, E), reddish brown (MUSM 31983, NMP 6 V 75056, 75057; Figs 14 A, B, D, E, 15G, H) or grayish brown (NMP 6 V 75541; Figs 15 A, B) with grayish-brown mottling. Flanks are paler than dorsum (e.g., MUSM 31983; Fig. 14 A). Canthal and supratympanic stripes absent, but one specimen (MUSM 31983; Fig. 14 A) has a dark brown blotch on canthus rostralis and a dark brown line along upper lip. Three specimens have the rim of the canthus rostralis pale gray (MUSM 31981, NMP 6 V 75057, 75542; Figs 14 D, E, 15D, E) and upper eyelids gray and brown mottled. Four specimens have a pale grayish-brown line ventrally across arms and chest, and midventrally across throat, chest, and belly as distinct as in the holotype (MUSM 31981, NMP 6 V 75541; Figs 15 C) or weakly defined (MUSM 31983, NMP 6 V 75056, 75542; Figs 15 F, 14C), and one specimen (NMP 6 V 75057; Fig. 14 F) only has a weak midventral line.

Etymology. The species epithet " puipui " is derived from the Quechua name Pui Pui meaning eyes of water in reference to the many lagunas in the Pui Pui Protected Forest and is used as noun in apposition. The type locality of P. puipui sp. nov. is in proximity of Laguna Sinchon which marks the approximate center of the Pui Pui Protected Forest.

Distribution, natural history, and threat status. Pristimantis puipui sp. nov. is only known from the type locality at Laguna Sinchon inside the PPPF at 3880 m a.s.l, where it co-occurs with Phrynopus sp. A (MUSM 31984, 31985). Specimens of Pristimantis puipui sp. nov. were found during early afternoon inside moss ( Figs 16 F, G). Two females ( Fig. 16 H) guarding eggs were found on 30 June 2013. The eggs of the two clutches were pale cream colored and had an average diameter of 4.0 ± 0.2 mm (3.6–4.3 mm, n = 13, MUSM 31981) and 3.7 ± 0.1 mm (3.5–3.9 mm, n = 20, NMP 6 V 75542).

We propose that P. puipui sp. nov. should be classified as "Data Deficient" according to the IUCN Red List criteria and categories (IUCN Standards and Petitions Subcommittee 2016).

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 12. Life male holotype (MUSM 31982, SVL 16.1 mm) of Pristimantis puipui sp. nov. in dorsolateral view (A), dorsal view (B), lateral view (C), and ventral view (D). Blue arrows indicate mite infestations. Photos by E. Lehr (A, C, D), and by J. C. Cusi (B).

FIGURE 13. Ventral views of right hand (A) of paratype (NMP 6 V 75057) and right foot (B) of holotype (MUSM 31982) of Pristimantis puipui sp. nov. Drawings by E. Lehr.

FIGURE 14. Variation of male paratypes of Pristimantis puipui sp. nov. in dorsolateral, dorsal, and ventral views. A – C (MUSM 31983, SVL 17.0 mm), D – F (NMP 6 V 75057, SVL 17.1 mm). Photos by E. Lehr.

FIGURE 15. Variation of selected female paratypes of Pristimantis puipui sp. nov. in dorsolateral, dorsal, and ventral views. A – C (NMP 6 V 75541, SVL 22.4 mm), D – F (NMP 6 V 75542, SVL 21.3 mm), G – I (NMP 6 V 75056, SVL 20.8 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).