Pristimantis humboldti, 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 : 317-322

Pristimantis humboldti sp. nov.

Figs 8 & 9

Pristimantis sp. nov. C in Lehr and von May (2017)

Common name. English: Humboldt’s Rubber Frog. Spanish: Rana cutín de Humboldt.

Holotype. MUSM 31190 (IWU 168, Figs 8 , 9 ), adult male from the Pui Pui Protected Forest, Quebrada Tarhuish , left bank of Antuyo River , " Shiusha ", upper cloud forest, 11° 21' 21.4''S, 74° 56' 10.8''W, 3318 m a.s.l. ( Figs 2 , 16 D, E), Provincia Satipo, Región Junín, collected on 14 May 2012 by E. Lehr and R. von May.

Paratypes. A total of 8 ( Figs 10 , 11 ), all collected with the holotype: 6 females (MUSM 31189, 31191, 31192, 31194 [GenBank accession numbers KY962798 , KY962791 , KY962775 ], NMP 6 V 75095, 75538 [GenBank accession numbers KY962799 , KY962792 , KY962776 ]), 2 males (NMP 6 V 75096, 75539).

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; 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 expanded, rounded, having circumferential grooves; (8) fingers with narrow lateral fringes; (9) small conical ulnar and tarsal tubercles present; (10) heel with a small conical tubercle; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, twice as large as outer; outer metatarsal tubercle small, rounded; few low supernumerary plantar tubercles; (12) toes with narrow lateral fringes; basal toe webbing absent; Toe V longer than Toe III; discs of digits expanded, rounded, having circumferential grooves, toe discs slightly smaller than those on fingers; (13) in life, dorsal and lateral ground coloration orange brown with brownish-olive blotches, orange brown with grayish-browm blotches and flecks, reddish brown with grayish-browm blotches or grayish brown with orange brown blotches; interorbital bar brownish olive or grayish brown, often followed by grayish-brown or brownish-olive marks in shape of a W or X or a combination of both on scapular region; dark grayish-brown canthal and supratympanic stripes present; groin blackish brown with white or pale gray spots and usually with an orange tint; throat, chest, belly, anterior and ventral surfaces of thighs, tibia and axilla dark gray and pale gray mottled with white and pale gray spots of different sizes and density; iris pale golden with fine black vermiculation and reddish tint horizontally across lower half of iris; (14) SVL in males 17.2–20.6 mm (n = 3), in females 19.7–25.7 mm (n = 6).

Comparisons. Pristimantis humboldti 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, and an areolate venter which is dark gray and pale gray mottled with white and pale gray spots. Pristimantis humboldti sp. nov. and P. phalaroinguinis ( Lehr & Duellman, 2007b) from elevations between 1800 and 2600 m a.s.l. in northern Peru have the groin dark brown with white spots, but P. humboldti sp. nov. is much smaller (SVL in males 25.0– 31.4 mm in P. phalaroinguinis, Lehr & Duellman 2007b ), has venter areolate (smooth), dorsolateral folds present (absent), males with vocal slits (absent), and throat, chest, belly, ventral surfaces of tibia, and axilla dark gray and pale gray mottled with white and pale gray spots (white spots restricted to groin). Pristimantis humboldti sp. nov. and P. ventriguttatus from 1800 m a.s.l. in northern Peru have dorsum shagreen, dorsolateral folds, areolate venter with pale spots, and have males of similar size (male SVL 17.8–21.8 mm, n = 3 in P. ventriguttatus, Lehr & Köhler 2007 ), but have digits moderately expanded (broadly expanded), and inner tarsal fold absent (present). Pristimantis humboldti sp. nov. and P. phoxocephalus ( Lynch, 1979) from elevations between 1850 and 2770 m in southern Ecuador and northern Peru ( Duellman & Lehr 2009) have a polymorphic dorsal coloration (dorsum gray to red or brown with few or no darker markings in P. phoxocephalus vs. dorsum orange brown, reddish brown or grayish brown with brownish olive, grayish brown or orange brown blotches and flecks in P. humboldti sp. nov.). However, P. humboldti sp. nov. has smaller males (male SVL 22.3– 29.9 mm [n = 29] in P. phoxocephalus, Lynch 1979 ), has dorsolateral folds (absent in P. phoxocephalus ), males without nuptial pads (present), and venter dark gray and pale gray mottled with white and pale gray spots (venter cream).

Pristimantis humboldti 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 humboldti sp. nov. is larger than P. albertus (female SVL 19.7–25.7 [n = 6] vs. 19.7–20.7 [n = 2] in P. albertus ; Duellman & Hedges 2007) and has the belly colored dark gray and pale gray mottled with white and pale gray spots of different sizes and density (cream with brown mottling in P. albertus ). Pristimantis humboldti sp. nov. has dorsal skin shagreen with scattered tubercle (smooth in P. aniptopalmatus ) and ventral skin areolate (smooth in P. aniptopalmatus and P. ornatus ). Pristimantis humboldti sp. nov. easily can be distinguished from P. stictogaster which has a white belly with prominent dark brown to black, irregularly shaped spots. Pristimantis humboldti sp. nov. is most similar to three other species of the Pristimantis danae species Group from the upper montane forests and puna of the PPPF and its surroundings ( Figs 2 , 3 ): P. attenboroughi , P. bounides sp. nov., and P. puipui sp. nov. All have discontinuous dorsolateral folds, tuberculate flanks, and an areolate venter. Pristimantis humboldti sp. nov. and P. bounides sp. nov. are sister taxa ( Fig. 3 ), and are of similar size (male SVL 17.2–20.6 mm, n = 3 in P. humboldti sp. nov. vs. 18.2–21.0 mm, n = 3 in P. bounides sp. nov.). Furthermore, P. humboldti sp. nov. and P. bounides sp. nov. have a tympamum (absent in P. attenboroughi and P. puipui sp. nov.), have expanded discs with circumferential grooves (absent in P. attenboroughi and P. puipui sp. nov.), and male P. humboldti sp. nov., P. bounides sp. nov., and P. puipui sp. nov. have vocal slits (absent in P. attenboroughi ). However, P. humboldti sp. nov. has well defined canthal and supratympanic stripes (diffuse canthal and supratympanic stripes in P. bounides sp. nov.), interorbital bar present (interorbital bar absent in P. bounides sp. nov.), scapular with W- or X-shaped marks (scapular without W- or X-shaped marks in P. bounides sp. nov.), has ventral coloration of throat, chest, belly, and anterior ventral surfaces of thighs dark gray and pale gray mottled with white and pale gray spots (venter pale gray, pale greenish gray or creamish white with or without gray mottling in P. bounides sp. nov.), and has ventral coloration of throat, chest, belly, and anterior ventral surfaces of thighs dark gray and pale gray mottled with white and pale gray spots (venter pale gray, pale greenish gray or creamish white with or without gray mottling in P. bounides sp. nov.).

Description of holotype. Head slightly shorter than wide; head length 37% of SVL; head width 38% of SVL; cranial crests absent; snout short, rounded in dorsal view, rounded in lateral view ( Figs 8 A, B); eye-nostril distance 76% of eye diameter; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis short, rounded in lateral view, weakly concave in dorsal view; loreal region slightly concave; lips rounded; upper eyelids with enlarged conical tubercles (three on right, four on left upper eyelid); upper eyelid width 74% of IOD; supratympanic fold short and broad, extending from posterior margin of upper eyelid curved around posterior margin of tympanum; tympanic membrane present, tympanic annulus distinct, its upper and posterior margin concealed by supratympanic fold; conical postrictal tubercles present (two right, one left). 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, widely separated; tongue short, oval, about 1.5 times as long as wide, not notched posteriorly, posterior half 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 low scattered tubercles, skin on flanks weakly tuberculate, irregularly shaped, discontinuous dorsolateral folds extending from posterior level of arm insertion with a distinct conical tubercle at its anterior end to level of hind limb insertion; skin on throat smooth, skin on chest and belly areolate; discoidal and thoracic folds weakly defined; cloacal sheath short.

Outer ulnar surface of right arm with three minute low tubercles, that of left arm with two minute low tubercles; palmar tubercle bifid; thenar tubercle ovoid; subarticular tubercles distinct, most prominent on base of fingers, round in ventral view, subconical in lateral view; few, low supernumerary tubercles present, about one third the size of subarticular tubercles; fingers with narrow lacking lateral fringes, Finger I shorter than Finger II; nuptial pads absent; discs on digits of fingers expanded, round, having circumferential grooves ( Fig. 9 A).

Hind limbs moderate, slender; tibia length 46% of SVL; foot length 47% of SVL; dorsal surfaces of hind limbs tuberculate; inner surface of thighs smooth, posterior surfaces of thighs tuberculate, ventral surfaces of thighs areolate; heels with minute conical tubercles; outer surface of tarsus with few scattered minute low tubercles; inner tarsal fold absent; inner metatarsal tubercle ovoid, three times the size of round outer metatarsal tubercle; subarticular tubercles weakly defined, more distinct 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 expanded, round, less expanded than those on fingers, having circumferential grooves; relative length of toes: 1<2<3<5<4; discs on Toe III and Toe V not reaching distal subarticular tubercle on Toe IV ( Fig. 9 B).

Measurements of the holotype (in mm). SVL 19.0; tibia length 8.8; foot length 9.0; head length 7.0; head width 7.2; eye diameter 2.1; TY 0.9; inter orbital distance 2.3; upper eyelid width 1.7; internarial distance 2.0; eye– nostril distance 1.6.

Coloration of the holotype in life ( Fig. 8 ). Dorsal and lateral ground coloration orange brown with brownish olive flecks. Brownish-olive interorbital bar and W-shaped mark on scapular region. Dark grayish-brown canthal and supratympanic stripes outlined by a narrow pale brownish yellow margin. Labial bars on upper lip brownish olive, diffuse. Groin grayish brown with white and pale gray spots and an orange tint. Throat, chest, belly and anterior ventral surfaces of thighs dark gray, pale gray, and orange brown mottled. Anterior and posterior surfaces of thighs, tibia, dorsal surfaces of thighs and axilla mottled with white and pale gray spots. Iris pale golden with fine black vermiculation and reddish tint horizontally across lower half of iris.

Coloration of the holotype in preservative. Dorsal and lateral ground coloration pale tan and pale gray mottled. Dark brown interorbital bar and W-shaped mark on scapular region. Dark grayish-brown canthal and supratympanic stripes outlined by a narrow pale tan margin. Labial bars on upper lip pale grayish brown, diffuse. Groin grayish brown with white spots. Throat, chest, belly and anterior ventral surfaces of thighs dark gray, and tan brown mottled. Anterior and posterior surfaces of thighs, tibia, dorsal surfaces of tarsi and axilla with white and pale tan spots. Iris pale gray with fine black vermiculation.

Variation. All paratypes ( Figs 10 , 11 ) are similar to the holotype regarding morphology and proportions ( Tables 3, 4). The dorsal and lateral ground coloration is orange brown with brownish-olive blotches (NMP 6 V 75096; Figs 10 A, B, D), orange brown with grayish-brown blotches and flecks (MUSM 31192; Figs 11 I–K), reddish brown with grayish-brown blotches (MUSM 31194, NMP 6 V 75095, 75538, 75539; Figs 10 E, 11E, F) or grayish brown with orange-brown blotches (MUSM 31189; Figs 11 A–C). The interorbital bar is brownish olive or grayish brown, often followed by grayish-brown or brownish-olive mark in shape of a W (MUSM 31194) or X (NMP 6 V 75096; Fig. 10 B) or a combination of both (MUSM 31189, 31191; Fig. 11 B) on scapular region. Dark grayish-brown canthal and supratympanic stripes present, outlined by a narrow pale gray margin (e.g., MUSM 31189, NMP 6 V 75096; Figs. 10 A, 11A) or without such an outline (e.g., NMP 6 V 75095, 75538; Fig. 11 E). Labial bars on upper lip are brownish olive, pale or dark grayish brown with or without pale tan outline, mostly diffuse (e.g., NMP 6 V 75095, 75539; Figs 10 E, 11E), sometimes distinct (MUSM 31189, 31191, NMP 6 V 75096; Figs 10 A, 11A) or absent (MUSM 31194). The groin is blackish brown with white or pale gray spots and usually with an orange tint (e.g., MUSM 31189, NMP 6 V 75096; Figs 10 A, 11C). The throat, chest, belly and anterior ventral surfaces of thighs are dark gray and pale gray mottled with white and pale gray spots of different sizes and density (NMP 6 V 75095, 75538, 75539; Figs 10 C, F, 11D, H, L), a pattern which seems to resemble lichens growing on a dark rock. Two specimens have anterior throat with a dark gray blotch (MUSM 31194, NMP 6 V 75096; Fig. 10 C) and three specimens have a narrow dark grayish-brown midventral line across throat, chest, and belly (MUSM 31189, 31192, NMP 6 V 75095; Figs 11 D, H, L).

Etymology. We dedicate this species to Alexander von Humboldt (1769–1859), German geographer, explorer, naturalist, in recognition of his exploration of the New World, especially the Andes, and whose legacy continues to inspire generations.

Distribution, natural history, and threat status. The type locality at 3318 m a.s.l. on the border of the PPPF ( Figs 2 , 16 D, E) is in the Quebrada Tarhuish on the left bank "Shiusha" of the Antuyo River and belongs to the upper montane forest ( Brack 1986). The vegetation consists of small bushes, small trees, forest patches, Peruvian feather grass, fern, and moss layers. Pristimantis humboldti sp. nov. was found inside Peruvian feather grass bunches (MUSM 31189) in the early afternoon and at night (1900–2100 hrs) on low vegetation up to 1 m from ground (MUSM 31190, 31191, 31194, NMP 6 V 75095, 75096) and on ground (MUSM 31192) inside a forest patch. Males called during rain in late morning and afternoon, and at night. Sympatric anurans are Gastrotheca griswoldi (MUSM 31193), and Pristimantis attenboroughi (MUSM 31186, 31187, NMP 6 V 75522, 75523). Four specimens had ectoparasitic mite ( Trombiculidae ) infestations (MUSM 31192, 31194, NMP 6 V 75096, 75539; Fig. 10 ) ranging from one (MUSM 31192) to 17 (NMP 6 V 75096) mite capsules distributed on the flanks and posterior surfaces of thighs. We propose that P. humboldti sp. nov. should be classified as "Data Deficient" according to the IUCN Red List criteria and categories (IUCN Standards and Petitions Subcommittee 2016). Given that P. humboldti sp. nov. occurs inside the PPPF, the long-term protection of this species should be supported by this nationally recognized protected area. However, other factors such as fungal infections, climate change, and pollution continue to threaten many Andean amphibians even inside protected areas (Catenazzi & von May 2014).

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 8. Life male holotype (MUSM 31190, SVL 19.0 mm) of Pristimantis humboldti sp. nov. in dorsolateral view (A), dorsal view (B), flanks, groin, anterior surfaces of thighs (C), and ventral view (D). Photos by E. Lehr

FIGURE 9. Ventral views of right hand (A) and right foot (B) of holotype of Pristimantis humboldti sp. nov. (MUSM 31190). Drawings by E. Lehr.

FIGURE 10. Variation of male paratypes of Pristimantis humboldti sp. nov. in dorsolateral, dorsal, and ventral views. A – D (NMP 6 V 75096, SVL 17.2 mm), E, F (NMP 6 V 75539, SVL 20.6 mm). Blue arrows indicate mite infestations. Photos by E. Lehr.

FIGURE 11. Variation of female paratypes of Pristimantis humboldti sp. nov. in dorsolateral, dorsal, lateral, and ventral views. A – D (MUSM 31189, SVL 21.1 mm), E – H (NMP 6 V 75095, SVL 23.2 mm), I – L (MUSM 31192, SVL 22.8 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).