Pristimantis boucephalus, Lehr & Moravec & Cusi & Gvoždík, 2017

Lehr, Edgar, Moravec, Jiří, Cusi, Juan Carlos & Gvoždík, Václav, 2017, A new minute species of Pristimantis (Amphibia: Anura: Craugastoridae) with a large head from the Yanachaga-Chemillén National Park in central Peru, with comments on the phylogenetic diversity of Pristimantis occurring in the Cordillera Yanachaga, European Journal of Taxonomy 325, pp. 1-22 : 7-15

Pristimantis boucephalus sp. nov.

urn:lsid:zoobank.org:act:BCF78234-F3F2-4A81-AE80-1B4BE26B1E1F

Figs 3–7 , Tables 1 – 4

Pristimantis sp. 4 – Angulo et al. 2016: 4, figs 76–77.

Suggested English name: Bigheaded Rubber Frog.

Suggested Spanish name: Rana cutín cabezona.

Fig. 2 (opposite page). The Bayesian phylogenetic tree of selected South American Pristimantis ; for taxon sampling design see Material and methods. Nodes were collapsed if they appeared in less than 50% of the post burn-in tree samples. Support values of posterior probabilities (pp) given only for discussed lineages (stars indicate full support, pp = 1.00). Taxa in red occur in the Cordillera Yanachaga region and represent six divergent lineages/species groups (uncorrected p -distance 13–17%). The new species, P. boucephalus sp. nov., is a member of a speciose clade, an as yet unnamed species group, comprising both montane taxa from the Andes and Guiana Shield, and lowland taxa from the intervening Amazon Basin. Species-group names follow Padial et al. (2014). DNA sequences of taxa retrieved from GenBank are labelled by standard GenBank accession numbers, all other codes stand for our new material.

Etymology

The species epithet boucephalus is derived from the Greek prefix “ bou -“ meaning large, huge, or great, and the Greek noun “ cephalo ” meaning head. The name refers to the disproportionally large head of the new species.

Material examined

Holotype

PERU: ♂, adult ( Figs 3–5 ), Yanachaga-Chemillén National Park (Sector San Daniel), Distrito de Huancabamba, Provincia de Oxapampa , Región Pasco, Quebrada Yanachaga , 10°22′46.3 S, 75°27′43.0 W, 2950 m a.s.l., Edgar Lehr, Juan C. Cusi and Jiři Moravec leg., 19 Jan. 2012 at 20h30 ( MUSM 31102 , GenBank 16S rRNA barcode: KY006091 ).

Paratypes (n = 4)

PERU: 2 ♂♂ ( MUSM 24477–78), 1 subadult ♀ ( MUSM 24479) and 1 juvenile ( MUSM 24474), all from the Yanachaga-Chemillén National Park (based on field numbers, detailed collecting data missing), collected during the 1990s, Javier Icochea leg., see Fig. 6 .

Generic placement

We assign this species to Pristimantis based on its general morphological similarity to other members of the genus and our molecular data (Fig. 2).

Definition

A new species of Pristimantis , not assigned to any species group, having the following combination of characters: (1) Skin on dorsum smooth with few low scattered tubercles, skin on venter areolate with low scattered tubercles; discoidal and thoracic folds absent; dorsolateral folds absent; (2) tympanic membrane and tympanic annulus absent; (3) snout short, rounded in dorsal and lateral views; (4) upper eyelid with one enlarged conical tubercle at its center and one enlarged conical tubercle at its posterior end; EW slightly shorter than IOD; cranial crests absent; (5) dentigerous processes of vomers absent; (6) males with vocal slits, nuptial pads absent; (7) Finger I shorter than Finger II; discs of digits expanded, rounded; (8) fingers with lateral fringes; (9) small conical ulnar and tarsal tubercles present; (10) heel with a conical tubercle; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, 2.5 times as large as outer; outer metatarsal tubercle small, rounded; numerous low, supernumerary plantar tubercles; (12) toes with lateral fringes; basal toe webbing present; Toe V longer than Toe III; toe discs slightly smaller than those on fingers; (13) in life, dorsal ground coloration greenish gray with reddishbrown blotches and scattered brown flecks surrounded by black; canthal and supratympanic stripes absent; groin and anterior surfaces of thighs greenish yellow with black blotches; venter gray with pale reddish and greenish brown mottling and scattered dark gray flecks; iris reddish copper with fine black vermiculation and black narrow vertical streak from pupil across lower half of iris; (14) SVL in adult males 13.4–14.5 mm (n = 3), in adult females unknown (12.5 mm in single subadult female).

Differential diagnosis

Pristimantis boucephalus sp. nov. is readily distinguished from its congeners in Ecuador and Peru by its minute SVL, short snout, absence of a tympanum, large head, groin and anterior surfaces of thighs greenish yellow with black blotches, and reddish-copper iris. It is currently one of the smallest of the 130 species of Pristimantis from Peru (AmphibiaWeb 2017) and the 199 species of Pristimantis from Ecuador ( Ron et al. 2017, see Table 2 ).

Pristimantis boucephalus sp. nov. can be distinguished from other minute Andean species of Pristimantis from Ecuador ( P. andinognomus , P. minimus , P. trachyblepharis ) and Peru ( P. caeruleonotus ,

P. coronatus , P. minutulus , P. trachyblepharis ) as follows (characters of P. boucephalus in parenthesis, if not otherwise stated):

Pristimantis minutulus Duellman & Hedges, 2007 from elevations of 250–1200 m a.s.l. in central Peru has larger males (SVL 13.1–17.6 mm [n = 7] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.; Duellman & Hedges 2007). Pristimantis minutulus and P. boucephalus sp. nov. lack dorsolateral folds, discoidal folds, a tympanum, and dentigerous processes of vomers and both have a smooth dorsum and areolate venter, but P. minutulus has the snout moderately long (short), males without vocal slits (present), groin with large yellow spot (greenish yellow with black blotches), and iris reddish gray (reddish copper with fine black vermiculation). Pristimantis caeruleonotus Lehr, Aguilar, Siu-Ting & Jordán, 2007 from elevations of 2500–2900 m a.s.l. of humid montane forests in northern Peru has males of similar size (SVL 11.6–14.6 mm [n = 4] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.; Lehr et al. 2007). Both P. caeruleonotus and P. boucephalus sp. nov. have fingers and toes with lateral fringes, heel with conical tubercle, and males that have vocal slits, but lack nuptial pads. However, P. caeruleonotus has a distinct tympanum (absent), dorsolateral folds (absent), small dentigerous processes of vomers (absent), a discoidal fold (absent), prominent dorsolateral folds ending in a sacral tubercle (absent), and a long snout with terminal papillae (short snout without papillae). Furthermore, P. caeruleonotus has the groin blackish brown with yellow and pale blue blotches (greenish yellow with black blotches). Pristimantis coronatus Lehr & Duellman, 2007 is known from a single female specimen of 15.3 mm SVL from 2850 m a.s.l. in northern Peru ( Lehr & Duellman 2007). It shares with P. boucephalus sp. nov. the absence of dorsolateral folds and a tympanum, and the presence of conical tubercles on the upper eyelid and fingers and toes with lateral fringes. However, P. coronatus has dentigerous processes of vomers (absent), groin red and black (greenish yellow with black blotches), and the iris dark brown (reddish copper). Pristimantis trachyblepharis ( Boulenger, 1918) from elevations of 100–1250 m a.s.l. in southern Ecuador and northern Peru and P. boucephalus sp. nov. have smooth dorsum, areolate venter, dorsolateral folds absent, and males that lack nuptial pads. However, P. trachyblepharis tends to have larger males (SVL 12.1–15.8 mm [n = 20] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.), tympanum present (absent), males without vocal slits (present), dentigerous processes of vomers (absent), and fingers and toes without lateral fringes (present) ( Lynch & Duellman 1980). Pristimantis andinognomus Lehr & Coloma, 2008 from 2450–2800 m a.s.l. in the Cordillera Oriental in southern Ecuador (Zamora Chinchipe) has males of similar size (SVL 10.0– 14.5 mm [n = 20] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.), males that have vocal slits but lack nuptial pads, fingers and toes with lateral fringes, and supernumerary plantar tubercles ( Lehr & Coloma 2008). However, Pristimantis andinognomus has short dorsolateral folds that end in a conical sacral tubercle (absent), tympanic membrane and tympanic annulus present (absent), a short snout with terminal tubercle (terminal tubercle absent), minute dentigerous processes of vomers (absent), flanks with tubercles coalescing into short ridges (ridges absent), heel with two enlarged tubercles (one heel tubercle), and inner tarsal fold present (absent). Pristimantis minimus Terán-Valdez & Guayasamin, 2010 from the Cordillera del Condor in Ecuador at elevations between 1250 and 1685 m a.s.l. has smaller males on average (SVL 9.5–13.7 mm [n = 46] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.; Terán-Valdez & Guayasamin 2010). Pristimantis minimus and P. boucephalus sp. nov. lack dorsolateral, discoidal and thoracic folds, have a short snout, and males have vocal slits present and nuptial pads absent. However, P. minimus has dentigerous processes of vomers (absent), fingers and toes without lateral fringes (present), heel without tubercles (heel with a conical tubercle), upper eyelid without enlarged tubercles (enlarged upper eyelid tubercles present), and has red iris with black reticulations (iris reddish copper with fine black vermiculation and narrow black vertical streak from pupil across lower half of iris).

Pristimantis boucephalus sp. nov. can be distinguished from other species of Pristimantis from Ecuador and Peru that are on average larger but have males of similar size as follows:

Pristimantis carvalhoi (Lutz, 1952) from the Amazonian lowlands and P. boucephalus sp. nov. both have males of similar size (SVL 13.4–14.8 mm vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.; Lynch 1980), no dorsolateral folds, and a groin with yellow coloration. However, P. carvalhoi has a long snout (short), tympanic annulus present (absent), prominent dentigerous processes of vomers (absent), vocal slits absent (present), and fingers and toes without lateral fringes (present). Pristimantis imitatrix ( Duellman, 1978) from the Amazonian lowlands has slightly smaller males (SVL 13.0–14.0 mm [n = 9] vs 13.4–14.5 mm [n = 3] in P. boucephalus sp. nov.; Duellman 2005) and shares with P. boucephalus sp. nov. the absence of a tympanum, dorsolateral folds, dentigerous processes of vomers, and nuptial pads, and both species have fingers and toes with lateral fringes. However, P. imitatrix lacks vocal slits (present), has the groin mottled black and white (greenish yellow with black blotches) and the iris is bronze (reddish copper). Pristimantis lirellus (Dwyer, 1995) from elevations of 470–1200 m a.s.l. in northern Peru and P. boucephalus sp. nov. both have males with vocal slits, and fingers and toes with lateral fringes, and both species lack a tympanum, dorsolateral folds, and nuptial pads, but P. lirellus has low longitudinal dermal ridges (absent), prominent dentigerous processes of vomers (absent), groin with single pale yellow to orange-yellow spot (greenish yellow with black blotches), and iris bronze to reddish brown (reddish copper). Pristimantis martiae (Lynch, 1974) from the Amazonian lowlands up to 1330 m a.s.l. and P. boucephalus sp. nov. lack dorsolateral folds, a tympanum, and nuptial pads, and both species have males with vocal slits, fingers and toes with lateral fringes. However, P. martiae has larger males (SVL 11.8–16.8 mm vs 13.4–14.5 mm [n = 3], Lynch 1980), small dentigerous processes of vomers (absent), a groin that is dull cream, pale orange or tan with brown to black bars or mottling (greenish yellow with black blotches), and bronze iris (reddish copper). Pristimantis croceoinguinis ( Lynch, 1968) from the Amazonian lowland forests in Ecuador and Peru has larger males (13.9–18.2 mm vs 13.4–14.5 mm [n = 3], Lynch 1968) which lack vocal slits (present). Pristimantis llosintuta ( Köhler & Lötters, 1999) from 2000–2200 m a.s.l. in Bolivia has a tympanum (absent) and much larger males (SVL 20.3–21.2 mm [n = 7] vs 13.4–14.5 mm [n = 3], Köhler & Lötters 1999). Pristimantis cruciocularis ( Lehr, Lundberg, Aguilar & von May, 2006) from the YCNP and its surroundings and P. boucephalus sp. nov. are of similar size (SVL 11.4–15.4 [n = 7] vs 13.4–14.5 mm [n = 3]; Lehr et al. 2006) and share the absence of a tympanic annulus and membrane, but male P. cruciocularis lack vocal slits (present). Furthermore, P. cruciocularis has the iris with a cruciform mark (absent) and a groin that is orange-red (greenish yellow with black blotches). Pristimantis sp. Pui Pui and P. boucephalus sp. nov. share the absence of a tympanic annulus and membrane, but P. sp. Pui Pui is much larger (SVL up to 31.3 mm vs 13.4–14.5 mm [n = 3]), and has a gray groin (greenish yellow with black blotches).

Description of the holotype

Head broader than body, as long as wide; head length 41.1% of SVL; head width 41.1% of SVL; cranial crests absent; snout short, rounded in dorsal view, rounded in lateral view ( Figs 3 , 5 A–B); eye-nostril distance 50% of eye diameter; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis short, broadly rounded in lateral view, weakly concave in dorsal view; loreal region slightly concave; lips rounded; upper eyelid each with an enlarged conical tubercle at its center and one enlarged conical tubercle at its posterior end; upper eyelid width 57.1% of IOD; few small tubercles on scapular region (see photos in life Fig. 3 A–B); supratympanic fold short and broad, extending from posterior margin of upper eyelid slightly curved to insertion of arm; tympanic membrane and annulus absent; small low postrictal tubercles present bilaterally. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers absent; tongue oval, tongue width is about three-fourths of the tongue length, posterior half free.

Skin on dorsum and flanks smooth, with low scattered tubercles (denser on flanks than on dorsum), dorsolateral folds absent; occipital and scapular region with sinusoidal ridge; skin on throat, chest, and belly areolate, with scattered low tubercles; discoidal and thoracic folds absent; cloacal sheath short.

Outer ulnar surface with minute low tubercles; palmar tubercle partially divided distally; thenar tubercle ovoid; subarticular tubercles well defined, most prominent on base of fingers, round in ventral view, subconical in lateral view; supernumerary tubercles distinct, ovoid, approximately half the size of subarticular tubercles; fingers with lateral fringes; Finger I shorter than Finger II; discs on digits of fingers expanded, round ( Fig. 5C ).

Hind limbs moderately long, slender, tibia length 54.6% of SVL; foot length 48.9% of SVL; upper surfaces of hind limbs smooth, with low scattered tubercles; inner surface of thighs smooth, posterior and ventral surfaces of thighs weakly areolate; heels each with a prominent conical tubercle; outer surface of tarsus with scattered minute low tubercles; inner tarsal fold absent; inner metatarsal tubercle ovoid, two and a half times the size of round outer metatarsal tubercle; subarticular tubercles well defined, round in ventral view, subconical in lateral view; plantar supernumerary tubercles distinct, about half the size of subarticular tubercles; toes with lateral fringes; basal webbing present; discs expanded, round, less expanded than those on fingers; relative length of toes: 1<2<3<5<4; disc on Toe III not reaching distal subarticular tubercle on Toe IV, disc on Toe V reaching distal subarticular tubercle on Toe IV; Fig. 5D .

Measurements (in mm) of the holotype

SVL 14.1; HL 5.8; HW 5.8; ED 2.4; IOD 2.1; EW 1.2; IND 1.4; E-N 1.2; TL 7.7; FL 6.9.

Coloration of the holotype in life ( Fig. 3 )

The dorsal ground coloration is greenish gray with reddish-brown and scattered brown flecks surrounded by black; a reddish-brown blotch mid-dorsally behind the eyes; sinusoidal ridge on occipital and scapular region dark brown; upper lip with two irregularly shaped grayish-brown bars bordered by black on each side of head below eye, bars separated by an irregular pale tan blotch; narrow brown bar laterally in area of canthus rostralis, but not forming a canthal stripe, supratympanic stripe grayish brown, bordered by black; flanks pale greenish and pale reddish brown with scattered dark brown flecks; groin and anterior surfaces of thighs greenish yellow with black blotches and black stripes that extend dorsally to posterior surfaces of thighs; throat, chest, belly and thighs gray with pale reddish and greenish brown mottling and scattered dark gray flecks; palmar and plantar surfaces gray, fingers I and II cream, fingers III and IV gray except for cream discs, toes I and II cream, toes III–V gray with reddish-brown lateral fringes; iris reddish copper with fine black vermiculation and narrow black vertical streak from pupil across lower half of iris.

Coloration of the holotype in preservative ( Fig. 4 )

Dorsal coloration grayish tan with scattered brown flecks; brown blotch middorsally behind eyes; sinusoidal ridge on occipital and scapular region dark brown; upper lip with two irregularly shaped grayish-brown bars on each side of head below eye, bars separated by an irregular pale gray blotch; narrow brown bar laterally in area of canthus rostralis, but not forming a canthal stripe, supratympanic stripe grayish brown; flanks tan with scattered brown flecks; groin and anterior surfaces of thighs tan with black blotches and black stripes that extend dorsally to posterior surfaces of thighs; throat, chest, belly and thighs grayish tan with dark gray flecks; palmar and plantar surfaces pale gray, fingers I and II tan, fingers III and IV gray except for tan discs, toes I and II tan, toes III–V gray; iris gray with fine black vermiculation and black narrow vertical streak from pupil across lower half of iris.

Variation

All paratypes are similar to the holotype regarding morphology ( Tables 3–4 ) and coloration pattern ( Fig. 6 ). They can easily be assigned to the species by having a small size with a disproportionally large head with short snout. The juvenile specimen (MUSM 24474) has two prominent tarsal and two prominent ulnar tubercles on each hind limb. One male specimen (MUSM 24477) has black bars dorsally, laterally and ventrally on the tibia and a brown blotch midventrally on the throat. One specimen (MUSM 24479) is considered a subadult female because of its small size, presence of ovaries, but absence of ovarian eggs.

Distribution, natural history, and threat status

Pristimantis boucephalus sp. nov. is currently only known from the YCNP. The type locality ( Figs 1 , 7 ) is located on a mountain crest at 2950 m a.s.l. covered with primary cloud forest. The holotype was found at night, sitting on a leaf at 1 m above the ground. Syntopic anurans included Pristimantis cf. aniptopalmatus (MUSM 31103–05), P. cf. mendax (MUSM 31101, 31107), and Phrynopus curator (MUSM 31106). We classify Pristimantis boucephalus sp. nov. as “Data Deficient” according to the IUCN red list criteria and categories ( IUCN Standards and Petitions Subcommittee 2016) based on the limited information on its geographic range. Given that Pristimantis boucephalus sp. nov. occurs inside the YCNP, a long-term protection of this species should be granted.

Figures

Fig. 3. Live holotype (MUSM 31102, SVL 14.1 mm) of Pristimantis boucephalus sp. nov. A. Dorsal view. B. Dorsolateral view. C. Ventral view. Photos by E. Lehr.

Fig. 4. Preserved holotype (MUSM 31102, SVL 14.1 mm) of Pristimantis boucephalus sp. nov. A. Dorsal view. B. Ventral view. Photos by E. Lehr.

Fig. 5. Pristimantis boucephalus sp. nov., holotype (MUSM 31102). A. Dorsal view of head. B. Lateral view of head. C. Ventral view of hand. D. Ventral view of foot. Drawings by J. Moravec.

Fig. 6. Paratypes of Pristimantis boucephalus sp. nov. in dorsal (upper row) and ventral (lower row) views. From left to right: ♀ (MUSM 24479), ♂ (MUSM 24477), ♂ (MUSM 24478), juvenile (MUSM 24474). Photos by E. Lehr.

Fig. 7. Type locality of Pristimantis boucephalus sp. nov. in the Yanachaga-Chemillén National Park. Photo by E. Lehr.

Fig. 1. Map of Peru with the Yanachaga-Chemillén National Park indicated in red.