See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/317369865

Four new species of terrestrial-breeding frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from Río....

Article in Zootaxa · June 2017 DOI: 10.11646/zootaxa.4273.3.4

CITATIONS READS 2 227

2 authors:

Lily Rodriguez Alessandro Catenazzi University of Bonn Florida International University

34 PUBLICATIONS 1,118 CITATIONS 115 PUBLICATIONS 1,101 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

An altitudinal transect along Manu Biosphere Reserve View project

Assessment of the conservation status and monitoring of Telmatobius intermedius and other amphibians in the province of Lucanas, Ayacucho, Peru View project

All content following this page was uploaded by Alessandro Catenazzi on 16 June 2017.

The user has requested enhancement of the downloaded file. Zootaxa 4273 (3): 381–406 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2017 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4273.3.4 http://zoobank.org/urn:lsid:zoobank.org:pub:ADC167F6-C3A0-43EC-8636-F65F5ABE85AF

Four new species of terrestrial-breeding frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from Río Abiseo National Park, Peru

LILY O. RODRIGUEZ1,3 & ALESSANDRO CATENAZZI2 1ILR, Uni-Bonn, Nussallee 21, 53115 Bonn, Germany 2Department of Zoology, Southern Illinois University, Carbondale, IL 62901, USA 3Corresponding author. E-mail: [email protected]

Abstract

We describe four new species of terrestrial-breeding frogs belonging to the genus Phrynopus from specimens collected on the eastern slopes of the Cordillera Oriental (2800–3850 m) near and within Río Abiseo National Park, Provincia Mariscal Cáceres, Departments of San Martín and La Libertad, northeastern Peru. All four species lack a visible tympanum and inhabit the upper ridges and slopes within or adjacent to the Park. Phrynopus anancites sp. nov. and P. capitalis sp. nov. inhabit the wet montane grasslands on the upper ridges and valleys from 3600 to 3850 m. Phrynopus anancites (SVL = 25.3 mm) has coarsely aerolated skin and olive green coloration and has small vomerine teeth, while P. c a pi t al i s (female SVL = 35.6 mm) is characterized by a large head, short limbs, and distinctive dorsal pattern. Phrynopus dumicola sp. nov. (female SVL = 25.3 mm) has a short head and dark colored body with granular skin on the flanks, and is known only from forest patches along the treeline from 3225 to 3550 m, whereas P. personatus sp. nov. (female SVL = 28.2 mm) has a dark facemask and bright yellow groin spots (possibly aposematic), and inhabits a narrow band of continuous tropical montane rain forest from 2890 to 3110 m. We report infection with Batrachochytrium dendrobatidis from one specimen of P. du m i - cola collected in July of 1988. With the addition of these four new species, Phrynopus now includes 32 nominal species.

Key words: amphibians, Andes, Batrachochytrium dendrobatidis, chytridiomycosis, direct development, montane trop- ical forest, puna, systematics, taxonomy

Resumen

Describimos cuatro especies nuevas de anuros de reproducción terrestre pertenecientes al género Phrynopus, a partir de especímenes colectados en el flanco Oriental de la Cordillera Oriental (2800–3850 m), Parque Nacional del Río Abiseo, Provincia Mariscal Cáceres, Departamentos de San Martín y La Libertad, noroeste del Perú. Las cuatro especies carecen de un tímpano visible y viven en las cimas y flancos más altos del parque. Phrynopus anancites sp. nov. y P. c a pi t al i s sp. nov. viven en los pajonales húmedos altoandinos, en las alturas del parque entre 3550 y 3850. Phrynopus anancites (LHC= 25.3 mm) se caracteriza por una piel gruesa y granulada, coloración verde oliva, y por poseer dientes vomerinos pequeños, mientras que P. capitalis (LHC= 35.6 mm en una hembra) se caracteriza por su cabeza grande, miembros cortos y un pa- trón dorsal distintivo. Phrynopus dumicola sp. nov. (LHC= 25.3 mm en hembras) se caracteriza por su talla pequeña y coloración oscura, es conocida sólo de parches de bosque a lo largo de la línea de árboles, entre 3225 y 3550 m; P. perso- natus sp. nov. (LHC= 28.2 mm en hembras) caracterizada por una máscara rostral, y manchas brillantes posiblemente aposemáticas en las ingles, vive en una banda angosta del bosque continuo, entre 2890 y 3110 m. Reportamos infección por Batrachochytrium dendrobatidis en un espécimen de P. dumicola colectado en julio de 1988. Con la adición de estas cuatro nuevas especies, Phrynopus incluye ahora 32 especies nominales.

Accepted by J. Padial: 10 Apr. 2017; published: 6 Jun. 2017 381 Introduction

The genus Phrynopus is endemic to Peru and currently contains 28 species distributed in the Cordillera Oriental from the Huancabamba depression in northern Peru to the Mantaro-Ene drainages in central Peru (Duellman & Lehr 2009; Frost 2016), with one species known to occur in the Cordillera Occidental (Duellman 2000). Similarly to other genera of high-elevation terrestrial-breeding frogs such as Bryophryne and Psychrophrynella (Catenazzi & Ttito 2016; Lehr & Catenazzi 2010), including species which had been assigned to Phrynopus prior to the splitting of this genus (Hedges et al. 2008; Padial et al. 2014), species of Phrynopus often have very small geographic ranges: more than half the species (16 of 28) are only known from the type locality (Duellman & Lehr 2009; Frost 2016). Species richness is high in central Peru (Figure 1), but habitats occupied by species of Phrynopus such as cloud forests and high elevation grasslands (puna and wet montane grasslands) are distributed continuously along the eastern slopes of the Andes as far north as the Huancabamba depression. One could thus expect to find similar levels of species richness of Phrynopus in northern Peru, where many regions have been poorly surveyed (Catenazzi & von May 2014). One such region was the Río Abiseo National Park (Río Abiseo NP), on the Amazonian slopes of the eastern slopes of the Cordillera Oriental, until teams of biologists started surveying vertebrate communities and discovered several new species (Gardner & Romo 1993; Leo & Gardner 1993). Río Abiseo NP is located in the Provincia Mariscal Cáceres, Department of San Martín, and protects the entire watershed of the río Abiseo (274,520 ha) from 600 to 4200 m (Figure 2). This watershed includes the Río Montecristo to the north, the Río Tumac in the middle, and the Río Abiseo to the south, flooding in a north-eastern direction into the Huallaga valley. The park lays south of the xeric Huancabamba depression, the most prominent physiographic feature of the so called cis-Andean region, often considered as a major geographical barrier for the distribution of Andean herpetofauna (Cadle 1991; Duellman 1979; Duellman & Wild 1993; Lynch 1986). A better knowledge of the herpetofauna of Río Abiseo NP improves our understanding of the biogeographic relevance of the Huancabamba depression (Lehr & Catenazzi 2011, 2013). We surveyed several localities within and adjacent to the upper part of Río Abiseo NP in July 1987, July 1988, July–August 1989, June–July 1999 and July 2000. This remote area was accessed after 1.5 days by mule and foot from Pataz (2600 m, Department of La Libertad), in the Marañon Valley. The survey area contains cloud and elfin forest, wet montane grasslands (grasslands covered by plant assemblages dominated by Loricaria sp., found from 3350 to 3850 m), and puna (general term for high-elevation grasslands) interspersed with glacial lakes which are at least 10,000 years old (Rodbell et al. 1992; Figure 3). Elfin forests occur within grasslands on slopes of small glacial valleys at lower elevations (3200–3550 m). Runoff from these valleys feed streams that descend sharply over steep slopes where continuous forest begins at approximately 3200 m. Along this altitudinal gradient ranging from 2200 to 3850 m, we collected 22 species of amphibians and reptiles. Among squamates, we collected an undescribed lizard of the genus Proctoporus sp., Sternocercus melanopygus Boulenger, and two snakes Erythrolamprus cf. taeniurus Tschudi and Chironius monticola Roze. We found more species of anurans: Telmatobius atahualpai Wiens, Gastrotheca phelloderma Lehr & Catenazzi, Hyloscirtus diabolus Rivera-Correa, García-Burneo & Grant, Pristimantis corrugatus (Duellman, Lehr & Venegas), P. deyi Lehr, Gregory & Catenazzi, P. wagteri (Venegas), and Phrynopus valquii, as well as undescribed species of Rhinella, Gastrotheca, Hypodactylus, and Pristimantis. Among the anuran specimens collected were four species of small, short-legged frogs inhabiting high- elevation montane forest and grasslands. All of these frogs are characterized by having tips of digits narrow, rounded or bulbous but always lacking circumferential grooves. Herein, we describe and name these four species and tentatively assign them to the Andean genus Phrynopus sensu Hedges et al. (2008), placed in the Terrarana taxon, and family Craugastoridae (Padial et al. 2014), based on an overall morphological similarity with other species of this genus.

Materials and methods

Specimens were collected during day and night while conducting visual transect surveys throughout the habitats. Mass of living frogs was measured to the nearest 0.5 g with spring scales (Pesola AG, Switzerland) prior to preservation. Then, specimens were euthanized with benzocaine 20%, preserved in 10% formalin, and stored in

382 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI FIGURE 1. Map of the Andes of central and northern Peru, with type localities of new species Phrynopus capitalis sp. nov., P. dumicola sp. nov., P. personatus sp. nov. (star) and P. anancites sp. nov. (asterisk) and of congeneric forms: P. valquii (asterisk), P. thompsoni (1), P. dae mon (2), P. lechriorhynchus and P. vestigiatus (3), P. horstpauli (4), P. kaune orum and P. kotosh (5), P. dagmarae and P. interstinctus (6), P. heimorum (7), P. barthlenae and P. tautzorum (8), P. miroslawae and P. nicoleae (9), P. badius and P. curator (10), P. auriculatus, P. bracki and P. tribulosus (11), P. pesantesi (12), P. bufoides and P. paucari (13), P. juninensis and P. montium (14), P. oblivious and P. peruanus (15), and P. chaparroi (16).

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 383 FIGURE 2. Study area within and around Río Abiseo National Park (bold continuous line) in the Departaments (Regiones) San Martín and La Libertad, eastern slopes of the Cordillera Oriental of the Andes, Peru, containing type localities of (1) Phrynopus personatus, sp. nov., El Mirador; (2) P. dumicola, sp. nov., Pampa del Cuy; (3) P. capitalis sp. nov.., Manachaqui lake; and (4) P. anancites, sp. nov., Puesto de Vigilancia Ventanas.

70% ethanol. Preserved specimens were measured to the nearest 0.1 mm using dial calipers or a micrometer in a stereoscope when appropriate. We follow Lynch & Duellman (1997) for the format and Duellman & Lehr (2009) for diagnosing characters. Measurements were taken following Lynch and Duellman (1980) except that head length was measured from the tip of the snout to the angle of the jaw. Abbreviations for measurements are as follows: SVL = snout–vent length, HL = head length, HW = head width, TL = tibia length, THL= thigh length, FL = foot length, IOD = interorbital distance, EW = upper eyelid width, E-N = eye-nostril distance, ED = eye diameter; IND = internarial distance. Skeletons of Phrynopus dumicola sp. nov. (AMNH 134151 and 134167), P. valquii (MUSM 7467 and 9085), and Pristimantis simonsii (MUSM 1160) were cleared and stained following standard protocol (Dingerkus & Uhler 1977). When type series were too small to allow clearing and staining, X-ray plates (MUSM 3820, P. dum icol a sp. nov.; MUSM 8959, P. capitalis sp.nov.; MUSM 3813, P. personatus sp. nov.; MUSM 3827, P. val quii ) were made at the National Museum of Natural History of the Smithsonian Institution and at the American Museum of Natural History. At least one specimen of each new species (except for P. anancites sp. nov.) was dissected and checked for the existence of a tympanic annulus. We also examined and produced X-ray plates of P. valquii (MUSM 3824) collected near Río Abiseo NP to compare osteological characteristics with those of three of the new species. Photographs of the preserved types taken by A. Catenazzi and M. Flecks are available at the Calphoto online database (http://calphotos.berkeley.edu). Format of the description follows that of Duellman & Lehr (2009). In November 2015 we swabbed nine ethanol-preserved museum specimens of P. capitalis (n = 1), P. dumicola (n = 4), P. montium (n = 1), P. personatus (n = 1), and P. valquii (n = 2) collected from 1964 to 1989 to detect

384 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI infection by Batrachochytrium dendrobatidis (Bd) (Appendix 2). We swabbed specimens with a synthetic dry swab (Medical Wire & Equipment, #113) using a standardized swabbing protocol (Catenazzi et al. 2011; Catenazzi & Ttito 2016). Specifically, we stroked the swab across the skin a total of 30 times: 5 strokes on each side of the abdominal midline, 5 strokes on the inner thighs of each hind leg, and 5 strokes on the foot webbing of each hind leg (total of 30 strokes/frog). We used a real-time Polymerase Chain Reaction with a Life Technologies StepOne Plus qPCR instrument assay on material collected on swabs to quantify the level of infection (Boyle et al. 2004; Hyatt et al. 2007). We used PrepMan Ultra to extract DNA from swabs, and analyzed each sample once. We calculated ZE, the genomic equivalent for Bd zoospores by comparing the qPCR results to a set of standards, and considered any sample with ZE > 1 to be infected. We deposited specimens in the herpetological collection of the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos (MUSM) in Lima, Peru, the American Museum of Natural History of New York (AMNH), USA, and the Natural History Museum of The University of Kansas (KU) at Lawrence, USA. For specimens examined, see Appendix 1.

FIGURE 3. Habitats of species of Phrynopus in the Río Abiseo NP and surrounding area. (A, B) habitat of P. capitalis sp. nov. and P. valquii in the Manachaqui valley, 3500 m, Department of La Libertad, near the border of Río Abiseo NP. (C) Pampa del Cuy valley, showing forest patches on the slopes; habitat of P. dumicola sp. nov.. (D) View over the Montecristo Valley, from El Mirador, habitat of P. personatus sp. nov. Photographs by A. Catenazzi.

Generic assignment

We currently lack evidence of any synapomorphic phenotypic trait for Phrynopus that allows distinguishing species in this genus from Pristimantis and other Terrarana with similar body shape and anatomical structures. The overall body shape of Phrynopus and similar frogs presumably converged in response to the conditions of high- elevation environments. In absence of molecular data, we tentatively assign the four new species to Phrynopus on the basis of the structure of the digital discs, lack of circumferential groves, the absence of differentiated tympanic membrane and tympanic annulus, overall body morphology with narrow head, wide body and small size, and Finger I shorter or equal in length than Finger II (Hedges et al. 2008; Duellman & Lehr 2009). However, the affinities of these four species should be revisited using DNA sequences.

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 385 Results

Phrynopus anancites new species (Figures 4, 5, 6A)

Holotype. MUSM 33168, an adult male (Figures 4, 5, 6A) collected at Ventanas (8°01´53.54”S, 77°24´28.06” W, 3820 m), Distrito Parcoy, Provincia Pataz, Departamento (Región) La Libertad, Peru on 29 June 1999 by A. Catenazzi and L. O. Rodriguez (Figure 1). Diagnosis. A medium size species of Phrynopus characterized by (1) a coarsely aerolate thick dorsal and ventral skin; thoracic fold present, discoidal fold absent; (2) tympanic membrane and tympanic annulus absent, well defined supratympanic fold; (3) snout short, rounded in dorsal view, slightly blunt in profile; (4) upper eyelid without tubercles; width of upper eyelid narrower than IOD, cranial crests absent; (5) dentigerous processes of vomers minute; (6) male lacking nuptial pads, vocal sac and slits; (7) Finger I as long as Finger II; thenar tubercle ovoid, 1.5 times larger than outer palmar tubercle which is hart-shaped, tip of digits rounded, bulbous, (8) fingers without lateral fringes, (9) ulnar tubercle absent, minute tarsal tubercle; (10) heels lacking tubercles, inner tarsal fold absent; (11) inner metatarsal tubercle ovoid; outer metatarsal tubercle slightly smaller, round, protruding; (12) no fringes or webbing between toes, Toe V slightly longer than III; (13) in life, dorsum bluish-olive-green, venter gray, iris yellow with inner orange ring; in preservative, uniform dark brown, lighter brown on upper ventral surfaces; (14) SVL 25.3 mm in single male. No other species of Phrynopus has the combination of lack of tympanun, distinctive supratympanic fold, short snout, small vomerine teeth, and coarsely areolated skin with uniform dorsal and ventral coloration. Of the species lacking a visible tympanum and bearing dentigerous processes of vomers (character condition for P. anancites in parentheses), P. bracki, P. dagmarae, P. insterstinctus, P. nicoleae, and P. vestigiatus have bright spots or coloration in the groin (absent). Furthermore, P. dagmarae, P. insterstinctus, and P. nicoleae have either smooth or shagreened dorsal skin (coarsely areolate); P. bracki is smaller with male SVL 13.2–16.2 mm, has a smooth venter (coarsely areolate), ridges forming an “M” on the scapular region (no scapular ridges) and bears lateral fringes on fingers (absent); P. dagmarae bears dorsolateral folds, lateral fringes on all digits, and the first finger is much shorter than the second one; P. insterstinctus is a smaller frog with longer limbs than P. anancites, and a smooth venter with a distinctive spotted pattern (uniformly gray); P. vestigiatus has lateral fringes on digits, bears ridges and dorsolateral folds (absent). Among species of Phrynopus bearing dentigerous processes of vomers and sharing a supratympanic fold, P. kauneorum has a shorter head (HL/SVL= 28–33 % in kauneorum, 37% in anancites), with smooth dorsal and ventral skin (coarsely areolate) and dark blotches over a pale brown dorsum and a lighter ventral color with some spots (uniform gray in dorsum and venter); P. kotosh has widely separated dentigerous processes of vomers bearing two teeth (minute), dorsal skin shagreened with scattered tubercles, aerolate skin on venter (coarsely aerolate dorsally and ventrally); and P. lechriorhynchus, has a distinctly spatulate snout (rounded and short). Phrynopus capitalis has also a thick supratympanic fold, but lacks small vomerine teeth, bears fringes on digits and basal webbing (absent), and its dorsal coloration forms a pattern (absent). Phrynopus bufoides shares most characters with P. anancites, including the texture of the dorsal skin, but differs by bearing large elongated warts on dorsum and flanks over a darker ground color (rounded and continuous), by having first finger longer than second (shorter, or equal in size), and by lacking the dentigerous processes of vomers (present). Phrynopus daemon also lacks a tympanum and has uniform dorsum coloration, but lacks vomerine teeth, bears a prominent thoracic fold, has a shorter and less pronounced supratympanic fold, subacuminate snout in lateral view (blunt), and lateral fringes in toes (absent). Phrynopus thompsoni lacks a tympanum and has first and second fingers equal in length, but it bears lateral fringes on toes (absent), has pustular dorsal skin (coarsely areolate), and lacks the dentigerous processes of vomers (present). Phrynopus chaparroi shares most characters with P. anancites, but differs by having the skin of the tympanic area covered by elongate, round subconical tubercles instead of a supratympanic fold (fold present), by having a rounded snout in profile (blunt), by lacking the dentigerous processes of vomers (present), and by bearing a brownish-black dorsal coloration scattered with white to yellow spots (uniform olive), and a brown reticulated iris (yellow ring and bronze in P. anancites). Phrynopus auriculatus and P. peruanus have a visible tympanic annulus (absent), whereas P. montium has a dark dorsum and areolate dorsal and ventral skin, but differs by lacking dentigerous processes of vomers, by having a visible tympanic annulus and vocal slits and nuptial pads on swollen Finger I (absent). Most species of the Pristimantis orestes group superficially resemble

386 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI Phrynopus anancites; those are Pristimantis atrabracus, P. chimu, P. cordovae, P mariaelenae, P. melanogaster, P. pataikos, P. pinguis, P. seorsus, P. simonsii, P. stictoboubonus, P. stipa; all of which, except P. simonsii and P. attenboroughi, can easily be distinguished from Phrynopus anancites by having a visible tympanum (P. atrabracus, P. chimu, P. cordovae, P. mariaelenae, P. pinguis), or the tympanic annulus weakly defined and only visible beneath the skin (P. melanogaster, P. pataikos, P. stictoboubonus, P. seorsus, P. stipa). Pristimantis simonsii lacks the dentigerous processes of vomers (present), and bears lateral fringes and basal webbing on digits (absent), while P. attenbouroughi shares with anancites the lack of tympanic membrane and annulus, and lateral fringes on all digits, and the presence of dentigerous processes of vomers, but differs by bearing dorsal skin shagreened with low scattered tubercles (coarsely areolate with large rounded warts), by having a dark canthal and supratympanic stripe (well defined supratympanic fold, no color stripe), and by being smaller in size, males SVL 14.6–19.2 mm (Lehr and von May, 2017).

FIGURE 4. Holotype of Phrynopus anancites sp. nov., male MUSM 33168 (SVL = 25.3 mm), showing (A) head in lateral view and (B, C) body in dorsal and ventral views. Specimen collected at Ventanas, 3820 m, near the entrance of Río Abiseo National Park, San Martín, Peru. Photographs by Morris Flecks.

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 387 FIGURE 5. Holotype of Phrynopus anancites sp. nov., male MUSM 33168 (SVL= 25.3 mm), in life. Specimen from Ventanas, 3820 m, near the entrance of Río Abiseo National Park, San Martín, Peru. Photograph by A. Catenazzi.

FIGURE 6. Palmar and plantar surfaces of the new species of Phrynopus: (A) P. anancites sp. nov. (MUSM 33168), (B) P. capitalis sp. nov. (AMNH 134158), (C) P. dumicola sp. nov. (MUSM 33102), and (D) P. personatus sp. nov. (MUSM 33096). Photographs by M. Flecks (A, C and D) and A. Catenazzi (B).

388 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI Description of the holotype. Head narrower than body, wider than long; HW 107% of HL, HW 41% of SVL; HL 37% of SVL; snout short, rounded in dorsal view and slightly blunt in lateral view, E-N distance around half the size of eye; nostrils slightly protruding laterally, canthus rostralis rounded; loreal region bearing a few large postrictal tubercles under the supratympanic fold; no tubercles on upper eyelid; choanae small, round, well separated and anterolaterally situated; dentigerous processes of vomers minute, posterior to choanae, slightly oblique, broadly separated; cranial crests absent; upper eyelid smaller than interorbital distance, EW 88% of IOD; tympanic membrane and tympanic annulus absent; supratympanic fold thick, extending from edge of eye to the end of postrictal area; tongue oval, not notched posteriorly, posterior two-third free. Vocal sac and vocal slits absent. Skin on dorsum coarsely areolate, with large rounded warts, without lateral folds; outside of arms bearing low rounded tubercles; discoidal fold absent, a thin thoracic fold present; skin on venter and throat coarsely areolated bearing distinctive rounded warts, extending onto the lower parts of arms and legs, and the femoral and perianal areas. Outer surface of arms lacking tubercles; first finger and second fingers equal in length; thenar tubercle ovoid, 1.5 times larger than palmar tubercle which is hart-shaped; fingers lacking lateral fringes, tip of digits rounded, bulbous (Figure 6A); TL 34% of SVL; tarsus bearing a small tubercle, no tarsal fold; two metatarsal tubercles, inner slightly elongated, outer slightly smaller, rounded, protruding; toes without lateral fringes, lacking basal webbing; toe tips bulbous, as large as those on fingers; Toe V slightly longer than III (Figure 6A). Measurements (in mm). SVL 25.3, HL 9.4, HW 10.1, TL 8.5, THL 9.7, FL 9.9, IOD 2.8, EW 2.5, E-N 2.7, IND 3.1, ED 3.2. Color in life. The dorsal and lateral surfaces are olive-green (Figure 5), whereas the ventral parts are pale gray with darker flecks. The iris is uniformly bronze with a yellow ring. Color in preservative. In alcohol (Figure 4), the dorsal surfaces are uniformly dark grayish-brown; chest and throat areas are light brown, the remaining areas are as dorsal surfaces. Etymology. The specific name anancites is a Latin noun for a type of diamond used to drive sadness away, given in reference to the frog’s rare dorsal coloration in life. Distribution and ecology. The species is known from a single specimen that was found near the Park rangers’ station and entrance to Rio Abiseo NP at Ventanas, in wet montane grassland covered with mosses at 3820 m of altitude. Nothing is known about its natural history.

Phrynopus capitalis new species (Figures 6B, 7, 8, 9A)

Holotype. AMNH 134158, an adult male (Figures 6B, 7) obtained at Lake Manachaqui (7°41’47” S, 77°30’56” W, 3600 m), ca. 14 km airline NE Pataz, Provincia Pataz, Departamento (Región) La Libertad, Peru (Figure 1), collected on 3 July 1989 by L.O. Rodríguez. Paratopotypes. MUSM 8959, a gravid female (Figure 8), and MUSM 8957, a juvenile, collected with the holotype. Diagnosis. A moderately-sized Phrynopus with the following characteristics: (1) skin on dorsum and flanks fleshy and tuberculated, densely covered with minute round tubercles, bearing low warts especially above the insertion of the forelimbs and dorsolaterally; skin on throat, chest and belly coarsely areolate, ventral surface of thighs coarsely areolate; discoidal fold absent, thoracic fold evident; dorsolateral folds absent; (2) tympanic membrane and tympanic annulus absent; supratympanic fold swollen (similar to a parotoid gland); (3) snout short, nearly rounded in dorsal view, sloping and rounded in profile; nasals large, frontoparietals in contact; (4) upper eyelid without tubercles; width of upper eyelid narrower than IOD; cranial crests absent; (5) dentigerous processes of vomers absent; (6) males with gray nuptial pad on thumb, lacking vocal slits and vocal sac; (7) Finger I slightly shorter than Finger II; tips of digits bulbous, terminal phalanges T-shaped (Figure 9A); (8) fingers bearing basal webbing and fleshy lateral fringes; (9) ulnar and tarsal tubercles absent; (10) heels lacking tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle rounded, about 1.5 times larger than rounded outer metatarsal tubercle; supernumerary plantar tubercles absent (12) toes bearing lateral fringes; basal webbing present; Toe V longer than Toe III; toe tips rounded, bulbous, about as large as those on fingers; terminal phalanges with lateral processes (as in Figure 9A) (13) in life, dorsal surfaces are brownish tan with small, dark brown reticulate spots having the

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 389 appearance of a labyrinth; areolation on ventral surfaces are grayish cream in a darker ground color; in preservative, flanks are blueish black or black; (14) SVL in single female 35.6 mm, in single male 23.2 mm. The new species cannot be confused with any other described species of Phrynopus because of its very robust and prominent head (HW/SVL = 40 %), swollen tympanic area, absence of tympanic annulus, thick lateral fringes on all digits, and its distinctive dorsal coloration pattern with small brown reticulated spots. Phrynopus capitalis differs from P. auriculatus, P. montium and P. peruanus by lacking a visible tympanic annulus. Phrynopus anancites, P. auriculatus, P. bracki, P. dagmarae, P. interstinctus, P. kauneorum, P. kotosh, P. lechriorhynchus, P. nicoleae, P. peruanus, P. vestigiatus all differ (character condition for P. capitalis in parentheses) by having the dentigerous processes of vomers (absent). Phrynopus badius, P. curator, P. horstpauli, and P. thompsoni have discontinuous or ridge-like dorsolateral folds (absent). Of the species lacking a tympanum, the dentigerous processes of vomers and dorsolateral folds or ridges, P. barthlenae has similar size, coarsely tuberculate dorsal skin, and lateral fringes on digits, but differs from P. capitalis by lacking warts (present), by bearing a dark canthal and postorbital stripe (absent), by having small nasals (large) and widely separated frontoparietals (large nasals, frontoparietals in contact), and distinctive black dorsal blotches (labyrinth-like short spots on dorsal surfaces). Phrynopus bufoides is most similar to P. capitalis, but differs by having a discoidal fold (absent), a broad supratympanic fold (swollen), by lacking lateral fringes on toes (present), and by bearing prominent dorsal isolated and elongated warts forming discontinuous ridges (coarsely areolate dorsal skin with warts and minute tubercles), and black mottling on venter (uniform ventral coloration). Phrynopus chaparroi lacks lateral fringes on digits (present), has a much darker coloration without dorsal pattern (tan with brown pattern); P. daemon is readily distinguished by having subacuminate snout in lateral view (rounded), short supratympanic fold (swollen), no dorsal pattern (short labyrinth-like lines) and males having prominent subgular vocal sac (absent), and by lacking nuptial pads (present). Phrynopus heimorum has a slightly tuberculate dorsum (fleshy and tuberculate) and light reticulations especially on flanks and venter (dorsum with labyrinth-like small spots, venter uniform), and lacks lateral fringes on all digits (present); P. juninensis has smooth dorsal and ventral skin (coarsely areolate). Phrynopus miroslawae differs by lacking lateral fringes on digits and basal webbing on toes (present), by bearing dorsolateral, occipital and supratympanic folds (absent, supratympanic fold swollen), by having a row of subconical tubercles on outer edge of tarsus (absent), and by being smaller with the single known female having SVL = 29.2 mm (SVL = 35.6 mm). Phrynopus pesantesi lacks lateral fringes on digits (present), has a blunt snout (sloping to rounded in lateral profile) and smaller head with HW/SVL = 36% (40% in P. capitalis), a tuberculate dorsum (tuberculated bearing low warts), and olive and gray mottled and yellow blotches on groin, ventral surfaces of throat, upper arms, forearms, thighs, shanks and venter. Phrynopus valquii differs from P. capitalis by lacking lateral fringes or basal webbing in toes and fingers, by bearing canthal and supratympanic stripes (absent), and by having dorsal skin shagreen with scattered tubercles (coarsely areolate). Phrynopus tautzorum has a smooth dorsum with scattered tubercles (fleshy and tuberculate), lacks lateral fringes on digits (present), and has Toe V slightly shorter than Toe III (Toe V longer than Toe III). The following species of the Pristimantis orestes group with reduced finger tips may externally resemble Phrynopus capitalis: Pristimantis atrabracus, P. chimu, P. cordovae, P mariaelenae, P. melanogaster, P. pataikos, P. pinguis, P. seorsus, P. simonsii, P. stictoboubonus, P. stipa. All of these except P. simonsii and P. attenbouroughi, have a visible tympanum (P. atrabracus, P. chimu, P. cordovae, P. mariaelenae, P. pinguis), or the tympanic annulus is weakly defined or concealed beneath the skin (P. melanogaster, P. pataikos, P. stictoboubonus, P. seorsus, P. stipa). The other two members of the group occurring in Peru, P. corrugatus and P. ventriguttatus have well developed pads on all digits and cannot be confused with Phrynopus capitalis. Pristimantis simonsii lacks a tympanum, dentigerous processes of vomers, and bears lateral fringes on digits, as does Phrynopus capitalis, but differs by having relatively larger nasal bones, by lacking the swollen supratympanic fold, by having smoother dorsal skin (coarsely tuberculate with warts) and by bearing some dorsal dark blotches (absent). Pristimantis attenbouroughi differs by bearing the dentigerous processes of vomers (absent), by having dorsal skin shagreened with low scattered tubercles (coarsely areolate with large rounded warts), a dark canthal and supratympanic stripe (absent, supratympanic fold swollen), and by being smaller with males SVL = 14.6–19.2 mm (single male SVL = 23.2 mm; Lehr and von May 2017). Description of holotype. Head distinct, narrower than body, wider than long, (HW 133% of HL; HW 40% of SVL; snout nearly rounded in dorsal view, sloping to rounded tip in lateral profile; snout moderately short; E-N 70% of eye diameter; nostrils small, weakly protuberant, dorsolateraly directed; canthus rostralis slightly curved in dorsal view, rounded in profile; loreal region slightly concave, lips weakly flared; interorbital area slightly convex,

390 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI no cranial crests; upper eyelid without enlarged tubercles; EW 90% of IOD in male specimen. Tympanic membrane and annulus absent; tympanic region with several irregular fused tubercles or warts, some of which are arranged in a swollen fold (similar to a parotoid gland), extending from the posterior margin of the eye to the shoulders. Oval to elongate, large tongue, weakly notched; choanae small, round, well separated and anterolaterally situated; dentigerous processes of vomers absent. Vocal sac and vocal slits absent.

FIGURE 7. Holotype of Phrynopus capitalis sp. nov., male AMNH 134158 (SVL= 23.2 mm), showing (A) head in lateral view and (B, C) body in dorsal and ventral views. Specimen collected near Lake Manachaqui, 3550 m, near the border of Río Abiseo National Park, San Martín, Peru. Photographs by A. Catenazzi.

Skin of dorsum irregularly granular bearing some warts and small ridges, especially in the scapular area and on the lower back, bearing scattered very small tubercles; skin of venter and throat coarsely areolate; two large postrictal tubercles under the swollen supratympanic fold; a low elongate tubercle on the interorbital area; metacarpal tubercles large, oval and low; outer areas of forelimbs bearing some elongate warts; inner palmar tubercle nearly rhomboidal, thenar round, small slightly shorter than palmar; fingers bearing thick lateral fringes, finger tips rounded and slightly bulbous; first finger slightly shorter than second; digital pads present; subarticular

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 391 tubercles round, conical in profile (Figures 6B, 9A); THL 38% of SVL; two metatarsal tubercles, round and large, inner one and a half the size of outer; some supernumerary plantar tubercles (Figure 6B). Toes bearing lateral fringes and basal webbing; toe tips bulbous, emarginated; Toe V longer than Toe III.

FIGURE 8. Female paratopotype of Phrynopus capitalis sp. nov. in life (MUSM 8959, SVL = 35.6 mm) from around Lake Manachaqui, 3600 m, near Rio Abiseo National Park, San Martín, Peru. Photograph by L. O. Rodriguez.

Color in life. Dorsal surfaces were brownish-gray on the scapular region on the holotype and brownish-tan bluish black on the flanks; the venter was yellowish gray. Iris cocoa brown. Nuptial pads black. Color in preservative. Dorsal surfaces are brownish-tan with small dark brown spots appearing like a labyrinth; flanks are black with some brown on the warts (Figure 7). Groin with black reticulations; posterior thigh black or brownish-tan, with the same dorsal pattern. Ventral surfaces grayish cream on the areoles with darker grayish ground color. Measurements in mm (data for male holotype followed by female paratopotype in parentheses). SVL 23.2 (35.9), HL 7.0 (13.6), HW 9.3 (14.3), TL (9.0 (12.0), THL 9.1 (13.0), FL 9.4 (13.9), IOD 2.9 (3.6), EW 2.6 (3.3), E-N 2.1 (2.8), IND 1.6 (2.7), ED 3.0 (3.7). Variation. Female MUSM 8959 is larger in size (35.6 mm), and EW is narrower than the IOD (wider in the holotype). The two postrictal tubercles are also present. Coloration is the same as in the holotype. In life (Figure 8), bluish black coloration under arms and above groin, more conspicuous than in male holotype. Etymology. The specific name capitalis is a Latin adjective meaning “pre-eminent” and is used in reference to the distinctive large head of the species Distribution and ecology. Phrynopus capitalis is known only from the type locality in the Manachaqui Valley, where it co-occurs with Phrynopus valquii and an undescribed species of Pristimantis. This valley is covered with wet montane grasslands and contains a glacial lake that feeds a tributary of the Marañon river (Figures 2, 3C). The three specimens were found within a 100 m2 area in the wettest flat area of this valley, among dense moss vegetation. This area lays outside of the Río Abiseo NP, but P. capitalis might be present in areas of the same habitat within the park.

Phrynopus dumicola new species (Figures 6C, 9B, 10, 11)

Holotype. MUSM 33102, a gravid female (Figures 6C, 10) obtained at Pampa del Cuy (7°39'49"S, 77°28'43"W; 3470–3550 m), ca. 18 km airline NE Pataz, Parque Nacional del Río Abiseo, Distrito Pataz, Provincia Mariscal Cáceres, Departamento (Región) San Martín, Peru, collected on 19 July 2000, by A. Catenazzi and R. von May.

392 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI FIGURE 9. Condition of terminal phalanges of Finger III, left hand: T-shaped in (A) Phrynopus capitalis sp. nov. (MUSM 8959), and knob-shaped in (B) P. dumicola sp. nov. (USNM 299788), (C) P. personatus sp. nov. (MUSM 3813), (D) P. valquii (MUSM 3823). Drawings by F. Chang.

Paratopotypes. Eleven adult males, one adult female and one juvenile female: males MUSM 33092 and 33118, collected on 18 and 19 July 2000 by A. Catenazzi and R. von May; female MUSM 3819, collected on 1 July 1987; males MUSM 3815, 3817, AMNH 134167 (cleared and stained), and juvenile female MUSM 3820, collected on 19 July 1987; males AMNH 134149–50 and 134151 (cleared & stained), collected on 29 July 1988; males MUSM 9078–79, collected on 3 August 1990, all collected by L. O. Rodríguez. Paratypes. Two adult males, one adult female and one juvenile male: adult male AMNH 134152 collected in elfin forest between Pampa del Cuy and Puerta del Monte (ca. 7°40'S,77° 27'W; 3350 m) on 19 July 1988; adult female MUSM 3818, adult male KU 220917, and juvenile male USNM 299788, collected at Puerta del Monte, ca. 20 Km airline NE Pataz, (7°39'29.64"S, 77°28'12.06"W; 3225 m) on 18 July 1987 by L. O. Rodríguez. Diagnosis. This species of Phrynopus has: (1) skin on dorsum shagreen or rugose with low scattered tubercles, skin on flanks areolate, skin on throat smooth, that of chest and venter areolate but not as coarsely as on flanks, ventral surface of thighs coarsely areolate; discoidal fold absent, thoracic fold present; dorsolateral ridges present ; (2) tympanic membrane and tympanic annulus absent, moderate supratympanic fold present; (3) snout short, rounded in dorsal and lateral views; (4) upper eyelid without conical or rounded tubercles; EW narrower than IOD; cranial crests absent; (5) dentigerous processes of vomers absent; (6) males lacking vocal slits and nuptial pads; (7) Finger I slightly shorter or equal in length than Finger II; tips of digits rounded, terminal phalanges knob-shaped; (8) fingers without lateral fringes; (9) ulnar and tarsal tubercles absent; (10) heels lacking tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, about 1.5 times larger than rounded outer metatarsal tubercle;

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 393 supernumerary plantar tubercles absent; (12) toes without lateral fringes; basal webbing absent; Toe III longer than Toe V; toe tips rounded, about as large as those on fingers; (13) in life, dorsum dark brown, reddish brown or olive green with irregular darker blotches, dark brown post orbital stripe present; throat varying from pearly white to pale salmon or creamy yellow, chest and belly dull brown to creamy white or bluish white with or without brown irregular blotches; ventral surfaces of forearms and thighs brown or salmon, ventral surface of hands and feet dark brown with irregular creamy white flecks or blotches; groin dark brown, or reddish brown with pearly white flecks; (14) SVL in females 22.3–25.3 mm (n = 5), in males 18.3–22.55 mm (n = 6).

FIGURE 10. Holotype of Phrynopus dumicola sp. nov., female MUSM 33102 (SVL = 23.34 mm), showing (A) head in lateral view and (B, C) body in dorsal and ventral views. Specimen collected at Pampa del Cuy, 3470 m, within Río Abiseo National Park, San Martín, Peru. Photographs by M. Flecks.

Seven other species of Phrynopus have aerolate skin ventrally, lack the tympanic annulus and dentigerous processes of vomers, but can be distinguished from P. dumicola by a combination of the following characters (character condition for P. dumi col a in parentheses). Phrynopus barthlenae bears lateral fringes on all digits (absent), has basal webbing on toes and nuptial pads in males (absent), and a dorsal pattern (absent). Phrynopus

394 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI bufoides is larger with females up to 33.6 mm SVL (25.2 mm) and wears large warts on dorsum (absent), whereas P. heimorum has a distinctive red coloration on ventral side of limbs (ventral coloration not red) and T-shaped terminal phalanges (not expanded). Phrynopus daemon has a weakly areolate skin (areolate), wears lateral fringes on toes (absent), and males have a subgular vocal sac (absent). Phrynopus horstpauli is larger with females up to 39.7 mm SVL, possesses a longer snout, toe V>III (toe III>V), and Finger I is much shorter than II. Phrynopus oblivius has a longer snout (E-N/ED 68-69% in P. oblivious, 60-61% in P. dumicola) smooth dorsal skin, bears ulnar tubercles (absent), has dark labial stripes (absent) and light small spots in venter (absent). Phrynopus valquii also lacks a tympanic annulus and the dentigerous processes of vomers, but differs by having a shorter and wider head, by lacking dorsolateral folds (discontinuous), by having shorter digits and bulbous digital tips (round tips), by bearing irregularly T-shaped terminal phalanges (knob-shaped; see Fig. 9B and 9D), and by having lighter dorsal coloration, and frontoparietals completely in contact (moderately separated). Phrynopus chaparroi, P. paucari and P. thompsoni also share most characters with P. dumicola, but P. chaparroi is larger, with females up to 32.2 mm in SVL, males wear nuptial pads (absent), bulbous toe tips (round), and a dark venter with irregular, diffuse white to gray blotches (ventral coloration light and lacking a pattern). Phrynopus paucari possesses a head that is longer than wide (HL < HW), has a discoidal fold (absent) and is bright greenish-yellow on the hands and the inner side of limbs and flanks, with fine reticulations on venter in live specimens (dull coloration ventrally, sometimes with salmon or dull pink on inner side of limbs). Phrynopus thompsoni has a longer snout, wears longitudinal dorsal rows of low tubercles with pustules (dorsum shagreen with low tubercles), lateral fringes on toes (absent), has Toe III = V (III > V) and many distinct brown spots on creamy tan venter (venter without any spots). Other species superficially resemble Phrynopus dumicola, but differ by having the dentigerous processes of vomers. Of these, P. kotosh further differs by bearing small tubercles on heels (absent) and by having transversal bars on thighs and lower frank (absent), whereas P. bracki differs by having a concealed tympanum (absent) and a very short first toe (longer than wide).

FIGURE 11. Live Phrynopus dumicola sp. nov. (MUSM 33127) from Pampa del Cuy, 3470 m, Rio Abiseo National Park, San Martín, Peru, in (A) dorsolateral and (B) ventral views. Note skin cysts caused by infestation with trombiculid mites. Photographs A. Catenazzi.

Species of the Pristimantis orestes group with reduced digital pads may externally resemble Phrynopus dumicola; those are P. atrabracus, P. chimu, P. cordovae, P mariaelenae, P. melanogaster, P. pataikos, P. pinguis, P. seorsus, P. simonsii, P. stictoboubonus, and P. stipa. All of those species, except P. si monsi i, have a visible tympanum (P. atrabracus, P. chimu, P. cordovae, P. mariaelenae, P. pinguis), or the tympanic annulus is weakly defined or concealed beneath the skin (P. melanogaster, P. pataikos, P. stictoboubonus, P. seorsus, P. stipa). The other two members of the orestes group occurring in Peru, P. corrugatus and P. ventriguttatus bear well developed pads on all digits and cannot be confused with Phrynopus dumicola. Pristimantis simonsii lacks a tympanum and dentigerous processes of vomers, as in Phrynopus dumicola, but differs by bearing lateral fringes and basal webbing (absent), by having relatively larger nasal bones, a shorter head and presenting black blotches on groins (no marks). Pristimantis attenbouroughi is slightly smaller than dumicola, males SVL to 19.2 mm, females SVL to 23.0 (males SVL to 22.6mm, females SVL to 25.3 mm), bears the dentigerous processes of vomers (absent), has a relatively longer snout with EN 70% of ED (EN 60% of ED), heel with a small conical ulnar and tarsal tubercles (absent), a short cloacal sheat (absent) and lighter dorsal coloration with stripes on low flanks (absent). Pristimantis

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 395 stipa externally resembles Phrynopus dumicola, but differs by bearing a supratympanic fold and tympanic annulus (absent in P. dumicola), by bearing the dentigerous processes of vomers, bulbous digital tips (round), prominent subarticular tubercles (weakly defined), and by having white mottling on venter, and white nuptial pads in dorsal and medial surfaces of thumbs in males (absent). Description of holotype. Head narrower than body, wider than long; HW 103% of HL; HW 37% of SVL; snout nearly rounded in dorsal view, rounded in lateral profile; canthus rostralis rounded to moderately sharp in lateral view; nostrils small, slightly protuberant, laterally directed; loreal region concave, sloping; snout short, E-N 86% of eye length; interorbital region flat, no cranial crests; EW 83% of IOD; tympanic membrane and annulus absent; supratympanic fold short, not prominent bordered by a dark stripe; tongue oval, not notched and one-third free posteriorly; choanae small, round, not hidden by palatal shelf of maxillae; dentigerous processes of vomers absent; skin of dorsum shagreen with low scattered tubercles, low postocular folds, discontinuous dorsolateral folds; some low small supraorbital tubercles; skin of venter coarsely areolate extending to the flanks and postrictal area; skin of throat areolate; moderate thoracic fold present, no discoidal fold; no ulnar tubercles; weakly defined palmar tubercle, palmar slightly smaller than thenar tubercle; fingers lacking lateral fringes; Finger I equal to Finger II. Hind limbs slender, short, TL 35% of SVL; upper surfaces of hind limbs smooth; posterior and ventral surfaces of thighs coarsely areolate; heel and outer surface of tarsus lacking tubercles; two metatarsal tubercles, inner oval; outer rounded, half size of inner; no supernumerary plantar tubercles; slightly areolate plantar surface; toes lacking lateral fringes and basal webbing; toe tips rounded, lacking marginal grooves, about as large as those on fingers; Toe III longer than Toe V (Fig. 4C). Color in life. Overall dark brown dorsally and ventrally, with some light reddish areas on throat, chest and upper venter. Iris bronze, turning darker towards the rounded pupil. Color in preservative. Dark brown to brown dorsally and laterally, with a visible supratympanic stripe. Venter brown to light brown with some darker spots. Measurements of the holotype (in mm). SVL 23.3, HL 8.3, HW 8.6, TL 8.5, THL 9.2, FL 10.8, IOD 2.7, EW 2.3, IND 2.5, ED 3.2, E-N 2.7. Variation. Coloration pattern in some specimens (MUSM 3819 and 33116) includes a middorsal line that extends onto back of thigh. Some specimens (e.g., MUSM 3815) have lighter areas on throat and venter. In darker specimens, the supratympanic fold bordered by a dark stripe is barely visible (MUSM 9078 and 9079). The skin of dorsum is usually shagreened, forming discontinuous dorsolateral ridges and occipital low folds. Etymology. The specific name dumicola is a Latin adjective meaning "a dweller in thickets" in reference to the habitat of forest patches bordering the tree line, inhabited by the species. Distribution and ecology. This species is only known from Pampa del Cuy, Río Abiseo NP. Most specimens were found in mosses on the ground of patches of elfin forest patches ranging from 0.01 to 5 ha in size. These elfin forests grow on rocky substrates surrounded by wet montane grassland along a linear distance shorter than 3 km in the Pampa del Cuy Valley (Figure 3B), from 3350 to 3550 m. The holotype was found in the grassland adjacent to forest patches, during a rainy night. Phrynopus dumicola was the only species of frogs encountered in leaf-litter plots in these elfin forest, while the surrounding grasslands contained other species of Pristimantis and Gastrotheca. We found at least one P. dum icol a specimen in every forest patch. We found some eggs (4.5 mm in diameter) with adult specimens on 19 July 1987, suggesting parental clutch attendance. Most P. dumicola had trombiculid mites under the skin, especially in the ventral area and limbs.

Phrynopus personatus new species (Figures 6D, 9C, 12, 13)

Holotype. MUSM 33096, a gravid female (Figures 6D, 12) obtained near El Mirador (7°39'50"S, 77°26'55"W; 2890 m), ca. 20 km airline NE Pataz, Distrito Huicungo, Provincia Mariscal Cáceres, Departament (Región) of San Martín, Peru, collected on 26 July 2000 by A. Catenazzi and R. von May. Paratopotypes. MUSM 33166, an adult male collected with the holotype. Paratypes. Five adult males and six adult females, all collected near the type locality, but at different elevations: males MUSM 33121 (7°39'33"S, 77°28'07"W, 3260 m), MUSM 33109 (7°39'36"S, 77°27'46"W, 3180 m); females

396 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI MUSM 33116 (7°39'36"S, 77°27'46"W, 3160 m), MUSM 33091 and 33099 (7°39'48"S, 77°28'26"W, 3110 m), MUSM 33100 (7°39'43"S, 77°27'36"W, 3150 m), collected on 21–22 July 2000 by A. Catenazzi and R. von May; female MUSM 3813 (7°39'45.92"S, 77°27'11.04"W, 3000 m), male AMNH 134153 and female MUSM 3811 (2930 m) collected on 23 July 1988 by L.O. Rodríguez; and males MUSM 3810 and 3812 (7°39´48” S, 77° 28´26” W, 3100 m) collected on 26 July 1988 by L. O. Rodríguez.

FIGURE 12. Holotype of Phrynopus personatus sp. nov., female MUSM 33096 (SVL = 24.47mm), showing (A) head in lateral view and (B, C) body in dorsal and ventral views. Specimen from El Mirador, 2890 m, Río Abiseo National Park, San Martín, Peru. Photographs by M. Fleks.

Diagnosis. This species of Phrynopus has: (1) skin on dorsum shagreen with low scattered round tubercles on dorsum and flanks, skin on flanks areolate; skin on throat, chest and belly finely areolate, ventral surface of thighs coarsely areolate; discoidal fold absent, fine subgular and thoracic folds present; dorsolateral folds and an X shaped medial ridge usually present; (2) tympanic membrane and tympanic annulus absent; (3) snout rounded in dorsal and lateral views; (4) upper eyelid bordered by a dermal ridge and bearing some low rounded tubercles; width of

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 397 upper eyelid narrower than IOD; cranial crests absent; (5) dentigerous processes of vomers of vomers absent; (6) males lacking vocal slits and nuptial pads; (7) Finger I slightly shorter than Finger II; tips of digits rounded, terminal phalange knob-shaped (Fig. 9c); (8) fingers without lateral fringes; (9) ulnar and tarsal tubercles absent; (10) heels lacking tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, about 1.5 times larger than rounded outer metatarsal tubercle; supernumerary plantar tubercles absent; (12) toes without lateral fringes; Toe V slightly longer than Toe III; toe tips rounded, about as large as those on fingers; (13) in life, dorsum dark brown, reddish brown or olive green with irregular darker blotches, dark brown canthal and post orbital stripe marking always a face mask; throat and ventral surfaces of forearms and thighs reddish brown to red-wine, ventral surface of hands and feet lighter or dark brown with scattered creamy white flecks or blotches topping tubercles; low venter and groin region dark brown, or black with sharp defined round white blotches, yellow in life, sometimes extending onto the shank and also present behind the thigh; (14) SVL in females 23.4–28.2 mm (n = 7), in males 17.5–21.1 mm (n = 7).

FIGURE 13. Live specimens of Phrynopus personatus sp. nov. (A, B) MUSM 33121, (C, D) MUSM 33100 and (E, F) MUSM 33091 from near El Mirador, 2890 m, Río Abiseo National Park, San Martín, Peru. Photographs by A. Catenazzi.

398 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI No other species of Phrynopus has such a combination of dorsal folds and masked dark face. Among Phrynopus species lacking a tympanic annulus (present in P. auriculatus, P. montium, and P. peruanus) and the dentigerous processes of vomers (character status for P. personatus in parentheses), P. capitalis is much larger, lacks dorsolateral folds and has a different dorsal coloration pattern, possesses bulbous digital tips (rounded) and wears lateral fringes in toes and fingers (absent). Phrynopus dumicola does not have a distinctive face mask, has smaller nasal bones, a uniform dorsal coloration, and no light spots on groin whereas P. val quii has a weakly defined canthus rostralis (sharp), much lighter coloration and bulbous digits (rounded in personatus). Among species that exhibit bright coloration on groin (P. badius, P. bracki, P. dagmarae, P. heimorum, P. interstinctus, P. nicoleae, P. paucari, P. peruanus, and P. vestigiatus), P. peruanus has a tympanic annulus (absent); P. bracki has dentigerous processes of vomers (absent), and P. badius has smooth uniform brown ventral skin, scattered with minute white dots and labial bar and very prominent subarticular at the base of fingers (absent in P. personatus); P. paucari has a bright yellow venter. Phrynopus vestigiatus shares with P. personatus the presence of X ridges on the scapular region, but has smooth dorsal skin, is smaller with single known female having SVL=18.8 mm (28.2 mm), has minute dentigerous processes of vomers (absent), and a dark venter with small white flecks (light flecks absent). Phrynopus dagmarae possesses light groin marks sharply bordered by black, but differs from P. personatus by having the dentigerous processes of vomers and labial bars (both absent), different dorsal and ventral coloration, and bulbous tip of fingers (rounded, not expanded). Phrynopus horstpauli has dorsal markings and large nasal bones like P. personatus, but differs by its larger size, by lacking bright coloration on groin, and by having T- shaped terminal phalanges (knobbed) and yellow-copper iris (upper iris golden with brown reticulations). Phrynopus miroslawae is similar to P. personatus in having a supratympanic fold and broad dark canthal and postorbital stripes delineating a face mask, and by bearing dorsolateral and occipital folds, but differs by lacking bright coloration on groin, and by having bulbous digital tips (round), areolated ventral skin, and dorsal gray coloration with dark blotches. Phrynopus nicoleae is similar to P. personatus in having first finger shorter than second, and in bearing X-shaped dorsal marks and occipital and dorsolateral folds, but differs by its longer snout, and by having labial bars and vomerine teeth. Among species of Phrynopus lacking tympanum and dentigerous processes of vomers, P. curator also has dorsal Y shaped ridges, and tubercles, but has a weakly areolate ventral skin (aerolate), three tubercles on upper eyelid (dermal ridge with low tubercles), a conical tubercle on heel (absent), longer limbs (TL/SVL= 49% in P. curator, 33-35 % in P. personatus) and lacks bright coloration in the groin (present in P. personatus). Species of the Pristimantis orestes group bearing reduced digital pads may externally resemble Phrynopus personatus; those are P. atrabracus, P. chimu, P. cordovae, P mariaelenae, P. melanogaster, P. pataikos, P. pinguis, P. seorsus, P. simonsii, P. stictoboubonus, P. stipa; all of which, except P. simonsii, have either a visible tympanum, or the tympanic annulus is weakly defined or concealed beneath the skin (in P. melanogaster, P. pataikos, P. stictoboubonus, P. seorsus and P. stipa). Furthermore, P. stipa, has a dark dorsal skin, but differs from Phrynopus personatus by lacking medial dorsal ridges and dorsolateral folds, and bearing prominent dentigerous processes of vomers (absent in P. personatus). Pristimantis simonsii also lacks the dentigerous processes of vomers, but lacks dorsal folds and a distinctive face (both present in P. personatus), and bright yellow or white spots on groin, on black ground (present). Pristimantis attenbouroughi differs by bearing dentigerous processes of vomers (absent), by having the upper eyelid without dermal ridge (dermal ridge present, bearing some low rounded tubercles), areolate ventral skin (finely areolate), heel with a small conical ulnar and tarsal tubercles (absent), and a short cloacal sheath (absent). Description of holotype. Head narrower than body, longer than width; HW 95% of HL; HW 37.8% of SVL; interorbital area flat, no cranial crests; upper eyelid bearing several round supraorbital tubercles, EW 57% of IOD,; snout semicircular in dorsal view, slightly truncate in profile; snout short, E-N 69% of eye length; canthus rostralis sharp in lateral view, loreal region strongly sloping outward to lip, slightly concave; nostrils weakly protuberant, directed dorsolaterally; lips not flared; tongue large, oval, posterior one-fourth free; choanae small, round, situated well anterolaterally on palate, fairly separated; dentigerous processes of vomers absent; tympanic annulus and tympanic membrane absent, supratympanic fold thick and prominent; several postrictal tubercles present, extending onto the loreal area. Skin of dorsum shagreened; prominent but incomplete dorsolateral ridges; flanks and upper surfaces of limbs bearing scattered conical warts, lateral surfaces of limbs and paravertebral area bearing low small tubercles; an X- shaped middorsal ridge formed by a series of closely packed warts starting postorbitally and joining the middorsal line at the middle of the back, shorter and less prominent on posterior half; skin on throat shagreened, that of venter

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 399 finely areolate; an outer row of tubercles present on forearms; palmar tubercle ovoid, thenar rounded barely defined; subarticular tubercles low, simple; finger tips not bulbous; first finger shorter than second. Tibia length 33% of SVL; showing an external row of tubercles on the heel and tarsal area, as an extension of the warts on lateral surfaces of limbs; outer metatarsal tubercle flat, oval, barely defined, inner slightly smaller than outer, rounded; supernumerary and subarticular tubercles not evident. Toes lacking lateral fringes and basal webbing. Color in life. The dorsal ground color was brown to reddish brown; venter, throat and inner forelimbs were brown-red to red; bright to light rounded yellow spots on groin sharply bordered with black. Face and dorsal surfaces as in preservative. Iris golden with fine dark reticulations on upper half, lower half dark brown.

TABLE 1. Measurements and proportions of two new species of Phrynopus. For measurements abbreviations see Material and Methods. Mean and standard deviation are followed by range. P. dumicola sp. nov. P. personatus sp. nov. ♂ (n=6) ♀ (n=5) ♂ (n=7) ♀ (n=7) SVL 20.1 + 0.5 24.1 + 0.6 19.2 + 0.5 25.3 + 0.6 (18.7–22.6) (22.3–25.3) (17.5–21.1) (23.4–28.2) HL 6.9 + 0.2 8.0 + 0.4 6.8 + 0.2 8.9 + 0.3 (6.2–7.7) (7.2–9.4) (6.0–7.4) (7.7–10.0) HW 7.5 + 0.2 8.6 + 0.4 7.0 + 0.2 9.3 + 0.3 (6.6–8.0) (7.9–10.1) (6.5–7.6) (8.1–10.4) THL 7.2 + 0.1 8.8 + 0.4 7.8 + 0.2 9.3 + 0.2 (6.9–7.5) (8.1–9.5) (7.2–8.5) (8.7–10.2) TL 6.9 + 0.1 8.2 + 0.2 6.7 + 0.2 8.4 + 0.1 (6.5–7.1) (7.6–8.9) (6.1–7.7) (8.2–9.2) FL 8.5 + 0.2 10.0 + 0.2 8.5 + 0.3 10.0 + 0.3 (7.9–9.5) (9.5–10.8) (7.0–9.4) (8.3–11.3) IOD 2.3 + 0.1 2.6 + 0.1 2.2 + 0.1 2.8 + 0.1 (2.1–2.7) (2.2–2.9) (1.9–2.5) (2.4–3.3) EW 1.8 + 0.1 2.2 + 0.1 1.5 + 0.1 1.9 + 0.2 (1.6–2.1) (1.9–2.5) (1.3–1.9) (1.4–2.8) E-N 1.5 + 0.1 1.9 + 0.2 1.6 + 0.2 1.8 + 0.1 (1.4–1.6) (1.3–2.7) (1.3–2.4) (1.4–2.4) IND 2.0 + 0.1 2.6 + 0.2 2.0 + 0.2 2.6 + 0.1 (1.8–2.2) (2.2–3.1) (1.4–2.7) (2.2–3.1) ED 2.5 + 0.2 3.1 + 0.2 2.4 + 0.2 3.0 + 0.3 (2.0–2.9) (2.6–3.8) (2.0–3.2) (2.3–3.9) TL/SVL 34.9% 33.4% HW/SVL 36.7% 36.6%

Color in preservative. The face is uniformly dark brown, with a faint line bordering the canthal stripe and the tympanic fold. The tympanic and loreal regions underneath the faint line are dark brown, and form a pattern resembling a mask. The upper lip is bordered by small cream blotches. A thin, pale cream middorsal stripe extends from the internasal area to the vent. Above the cloacal opening, the stripe divides and extends across the thighs to the lower edge of the knee, continuing on the posterior side of shanks to reach the heel, and forming an irregular broad cream stripe (yellow in life) on the inner surface of the shank. Dorsal coloration is gray-brown above, with dorsal folds, warts and ridges bordered with faint and dark brown, as on the face. Venter and concealed surfaces of limbs, brown with dirty cream blotches. Rear surfaces of thigh and knees are dark brown.

400 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI Measurements (in mm) of the holotype. SVL 24.5, TL 8.1, FL 9.7, HW 9.3, HL 9.7, IOD 2.7, EW 1.6, IND 2.3, ED 2.3, E-N 1.6. Variation. Tibia length is 33% of SVL in females (n=7) and 35% in males (n=7). In some specimens, the postympanic ridge does not continue over the eye. Some specimens bear small oblique ridges, formed by a row of round tubercles (MUSM 3811 and MUSM 381, AMNH 134153), in the interorbital area. The dorsolateral folds are not continuous in MUSM 33100 and completely absent in MUSM 33091. This last specimen has an additional white spot (yellow in life) in the inner thigh, and two in the inner shank, as does MUSM 3811. In life, MUSM 9073, 90–74 and 9076, had very dark dorsal coloration and some ventral irregular spots. The thin pale cream mid- dorsal line is persistent in all specimens but MUSM 33100, where the line is ill defined. Etymology. The specific name personatus is a Latin adjective meaning masked and is used in reference to the distinctive face mask of this species. Distribution and ecology. Phrynopus personatus is known only from a narrow elevational range around the type locality in the upper reaches of the continuous mountain forests of the Abiseo National Park. Fourteen specimens were found in wet leaf litter of flat areas, all in the narrow elevational range from 2890 to 3110 m near El Mirador (3000 m). The area is a continuous tropical montane rain forest about 15 m tall. Arboreal ferns are common and tree trunks and ground surfaces are covered with moss, liverworts and lichens. Individuals of P. personatus were notably inactive before and after capture. The reproductive stage of the holotype indicates that the species may reproduce in the dry season. Males weighed 0.65– 0.95 g, females 1.90–3.05 g. Although no eggs were found with the specimens, the large size of the well-developed eggs in the holotype strongly suggests direct development. Some specimens had trombiculid mites under the skin (see cysts in Figures 13B, F).

Infection with Batrachochytrium dendrobatidis

All swabbed specimens were negative (Appendix 2), except for a specimen of P. dumicola (AMNH 134152) collected on 19 July 1988 that had a low ZE = 9.56 zoospore equivalents.

Discussion

With the four species described herein, the genus Phrynopus now comprises 32 species, all endemic to Peru, supporting the idea that many species await discovery in the eastern slopes of the Peruvian Andes, and that this genus contains high regional diversity and endemism (Figure 1, Table 2). Our findings highlight this striking diversity specifically for the region of Río Abiseo National Park, similarly to what has been reported for this genus at Cordillera Carpish, Yanachaga-Chemillen NP, and other localities in central Peru (Hedges 1990; Lehr & Aguilar 2002, 2003; Chaparro et al. 2008; Trueb & Lehr 2008; Lehr et al. 2000, 2005, 2012, Lehr & Oróz 2012; Mamani & Malqui 2014; Chávez et. al. 2015). The phylogenetic relationships and generic assignment of species of Phrynopus of these two regions, and more broadly the biogeography of the genus in the Peruvian Andes, will not be fully understood until molecular analyses can be conducted with a larger sample of species; the more recent analysis included only eleven of twenty-eight nominal species (Padial et al. 2014). The genus Phrynopus Peters, 1874, was first defined “by the lack of digital pads, simple digital tips, plantar surfaces lacking conical or subconical supernumerary tubercles, having alary processes on the hyoid plate, and having a “normal” skull architecture (i.e. not helmeted)” (Lynch 1975; Cannatella 1984). More recently, Phrynopus sensu Lynch (1975) was found to be composed of several non-sister clades on the basis of molecular analyses, and was split into different genera (Hedges et al. 2008). Although no synapomorphies are known for the genus, Phrynopus was redefined as the clade containing most species of short-legged, terrestrial-breeding frogs having head narrower than the body, digits lacking circumferential groves, terminal phalanges knob-shaped, and lacking differentiated tympanic membrane and tympanic annulus in the high Andes of central and northern Peru. Most species of Phrynopus lack cranial crests, and in most species the dentigerous processes of vomers are absent (but present in P. anancites, P. auriculatus, P. bracki, P. dagmarae, P. interstinctus, P. kauneorum, P. kotosh, P. lechriorhynchus, P. nicoleae, P. peruanus and P. vestigiatus). Finger I is usually smaller than Finger II (equal in length in some species), Toe V slightly longer than Toe III, and digits can be narrow, rounded, or bulbous, with

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 401 subarticular tubercles not projecting. Skin texture range from smooth to postulate dorsally, and smooth to areolate ventrally, while SVL range from 14.5 mm in P. auriculatus to 54 mm in P. kauneorum. The four species described herein are short-legged frogs lacking tympanum, columella and cavum tympanicum, and only P. anancites wears dentigerous processes of vomers. We include in our comparisons a fifth species, P. valquii, which we collected during our surveys and which occurs almost syntopically with P. anancites. Examination of cleared and stained specimens and X-ray plates demonstrated relatively large nasal bones in P. personatus, P. capitalis, and P. valquii, and small nasal bones in P. dum icol a. The terminal phalanges show reduced lateral processes in P. personatus, P. dum icola and P. valqui i, while P. capitalis possesses moderate lateral processes (Figure 9). In addition to having moderate lateral processes, P. capitalis also shares with species of the Pristimantis orestes group the partial emargination of some digital tips. These similarities suggest that P. capitalis could be related to species in the Pristimantis orestes group, but the absence of molecular data and morphological synapomorphies for these genera prevents us from further exploring this hypothesis. Phrynopus dumicola differs from P. valquii and P. capitalis by having reduced nasal bones and frontoparietals separated medially. Although the characters presented here readily separate the new species from congeners, molecular information is currently missing, preventing us from assessing the monophyletic relationships with other species of Phrynopus (Padial et al. 2014). Species of Phrynopus occur in wet grasslands, elfin forests and rain forests from 2600 to 4490 m, between latitudes 9°54´S (south of the Huancabamba depression) and 7°41´S (north of the Ene-Mantaro drainage; Figure 1, Table 2). On the basis of available information, all species have small distribution ranges and, when co-occurring in the same region, they segregate by elevation or by microhabitat type. A preliminary phylogeny including 11 species (Padial et al. 2014) suggests divergence between species inhabiting montane forests in the northern portion of the distribution range, and species inhabiting the puna in central Peru. We lack sufficient sampling to examine possible scenarios of diversification in the genus. Furthermore, several species inhabit fragmented elfin forests (e.g., P. curator, P. dumicola, P. kotosh, P. lechriorhynchus, and P. oblivius). The five species of Phrynopus of Río Abiseo NP occur along a linear distance shorter than 25 km, but are separated spatially by microhabitat and elevation. Of these five species, only P. anancites and P. valqui i are found in proximity, share similar microhabitats in wet montane grasslands, and might occur sympatrically. Data from our leaf-litter plots (which will be reported in detail in a different publication) indicate clumped distributions of most species, which may be related to narrow microhabitat requirements and limited dispersal abilities. Phrynopus capitalis inhabited a wet montane grassland at 3550 m, while P. valquii occurred in puna from 3550 to 3750 m and wet montane grassland at 3850 m (similarly to P. anancites), P. dumi col a was found in elfin forest between 3300 and 3550 m, and P. personatus in a narrow band (2930–3100 m) of continuous montane cloud forest well inside the Park. These data suggest a fine altitudinal and habitat segregation within species of Phrynopus in the study area. Small distribution ranges make species intrinsically more vulnerable to extinction, but at least two of the four new species, P. dumicola and P. personatus, and P. valqui i appear to have healthy populations within Río Abiseo NP. According to the IUCN Red List criteria and categories (IUCN 2013), and considering that no anthropogenic disturbance is currently threatening frog populations within the park, we propose to consider these two species for the “Least Concern” (LC) category. A short survey within the park and surrounding areas (down to Pampa del Cuy) in 2010 revealed the presence of Atelopus patazensis, Phrynopus valquii, P. dumicola and undescribed Pristimantis. Furthermore, P. valquii has been described from specimens collected in 2014, after our last visit. The other two species, P. anancites and P. capitalis, have not been collected within the park (although P. anancites was found at the park’s boundary) and are known from few specimens; in absence of more detailed data regarding their extent of occurrence, these species can provisionally be considered for the “Data Deficient” category of the Red List. The pathogenic fungus Batrachochytrium dendrobatidis has been reported from dying Atelopus patazensis near Río Abiseo NP on 21 June 1999 (Venegas et al. 2008), which is the oldest case of chytridiomycosis causing amphibian die-offs in Peru (Catenazzi & von May 2014). Of nine preserved specimens, all were negative, except for P. dumicola (AMNH 134152) that had a low ZE = 9.56 zoospore equivalents. This specimen had been collected on 19 July 1988, earlier than infected and dying Atelopus patazensis from nearby Pataz (Venegas et al. 2008). Although this fungus can cause dramatic declines in species richness and abundance of stream-breeding frogs (Catenazzi et al. 2011, 2014), it generally does not threaten terrestrial-breeding frogs in the Peruvian Andes (Catenazzi & Ttito 2016, Catenazzi & von May 2014), and we did not observe dead specimens of Phrynopus and other terrestrial-breeding frogs during our surveys in Río Abiseo NP.

402 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI TABLE 2. Geographic and elevational ranges of species of Phrynopus.

Species Known distribution Elevation Habitat

P. anancites sp. nov. La Libertad: Ventanas 3820 m puna P. auriculatus1,2 Pasco: Oxapampa 2600 m montane forest P. badius3 Pasco: PN Yanachaga-Chemillén 2900 m montane forest P. barthlenae1 Huánuco: Maraypata 3425–3770 m puna P. bracki1 Pasco: Oxapampa 2600 m montane forest P. bufoides1,4 Pasco: Paucartambo 3850–4100 m puna P. capitalis sp. nov. La Libertad: Pataz 3600 m puna P. chaparroi5 Junín: Comas 4205–4490 m puna P. curator2 Pasco: PN Yanachaga-Chemillén 3000 m montane forest/puna P. daemon6 Huánuco: Carpish 3140–3340 m montane forest P. dagmarae1,7 Huánuco: Chaglla (Carpish) 3020–3380 m montane forest P. dumicola sp. nov. San Martín: PN Río Abiseo 3225–3550 m elfin forest/puna P. heimorum1 Huánuco: Conchamarca 3420 montane forest P. horstpauli1 Huánuco: Conchamarca 3010–3770 m montane forest P. interstinctus9 Huánuco: Umari (Carpish) 3100–3180 m montane forest P. juninensis1 Junín, Pasco (Cordillera Oriental)3420–3850 m puna P. kauneorum1,7 Huánuco: Chaglla (Carpish) 3020–3380 m montane forest P. kotosh1,10 Huánuco: Huancapallac 2950 m montane forest P. lechriorhynchus1 Huánuco: Acomayo 2740–2800 m montane forest P. miroslawae1 Pasco: Oxapampa 3363 m elfin forest P. montium1 Junín (several localities) 3000–4012 m puna P. nicoleae1 Pasco: Oxapampa 3589 m puna P. oblivius1,10 Junín: Maraynioc 3210–3220 m montane forest P. paucari1,4 Pasco: Paucartambo 3600 puna P. personatus sp. nov. San Martín: PN Río Abiseo 2930–3100 m montane forest P. peruanus1 Junín: Maraynioc 3825 mpuna P. pesantesi1,4 Pasco: Huachón 4280–4390 m puna P. tautzorum1 Huánuco: Maraypata 3770 m puna P. thompsoni1 La Libertad: Yamobamba 3290 m puna P. tribulosus1,2 Pasco: Oxapampa 2600 m montane forest P. valquii6 La Libertad: Parcoy 4025 – 4125 m puna P. vestigiatus9 Huánuco: Chinchao (Carpish) 3100 m montane forest

1Duellman, W. E. and E. Lehr. 2009. Terrestrial-breeding frogs (Strabomantidae) in Peru. Nature und Tier Verlag, Münster, Germany, 382 pp. 2Duellman, W. E., and S. B. Hedges. 2008. Two minute species of Phrynopus (Lissamphibia: Anura) from the Cordillera Oriental in Peru. Zootaxa 1675: 59–66. 3Lehr, E., J. Moravec, and J. C. Cusi. 2012. Two new species of Phrynopus (Anura, Strabomantidae) from high elevations in the Yanachaga-Chemillén National park in Peru (Departamento de Pasco). ZooKeys 235: 51–71. 4Lehr, E., M. Lundberg, and C. Aguilar. 2005. Three new species of Phrynopus from central Peru (Amphibia: Anura: Leptodactylidae). Copeia 2005: 479–491. 5Mamani, L., and S. Malqui. 2014. A new species of Phrynopus (Anura: Craugastoridae) from the central Peruvian Andes . Zootaxa 3838: 207–214. 6Chávez, G., R. Santa Cruz, D. Rodríguez, and E. Lehr. 2015. Two new species of frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from the Peruvian Andes. Amphibian & Reptile Conservation 9(1, e105): 15–25. 7Lehr, E., C. Aguilar, and G. Köhler. 2002. Two sympatric new species of Phrynopus (Anura: Leptodactylidae) from a cloud forest in the Peruvian Andres. Journal of Herpetology 36: 208–216. 8Lehr, E. 2001. A new species of Phrynopus (Anura: Leptodactylidae) from the eastern Andean slopes of central Peru. Salamandra 37: 11–20. 9Lehr, E., and A. Oróz. 2012. Two new species of Phrynopus (Anura: Strabomantidae) from the Cordillera de Carpish in central Peru (Departamento de Huánuco). Zootaxa 3512: 53–63. 10Lehr, E. 2007. New eleutherodactyline frogs (Leptodactylidae: Pristimantis, Phrynopus) from Peru. Bulletin of the Museum of Comparative Zoology 159: 145–178.

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 403 Chávez et al. (2015) suggested Phrynopus valquii to be Data Deficient, in absence of known localites within the park. Here we confirm that P. valquii does indeed occur within Río Abiseo NP, because we found MUSM 9085 brooding a clutch of 20 eggs at the puna of Laplap (3850m), MUSM 3827 and AMNH 134155 at Paredones (3635 m), and MUSM 3824 near Lake Manchaqui (Figure 2). Therefore, similarly to P. dum icol a and P. capitalis, we propose the LC category for P. valquii. We recommend continuous monitoring of frog populations inside the park to provide stronger support for future assessments of the conservation status of these species (Catenazzi & von May 2014).

Acknowledgments

We thank M. Leo, M. Romo, E. Ortiz, R. von May, M. Fernandez, D. Aguilar and M. Silva for support during field expeditions. Logistic support was provided by T. and I. Hurtado, P. Moore, the friendly people from Pataz, E. Alayo, the park administration and rangers. LOR is especially grateful to D.W. Davidson for providing all necessary support, working space and constructive comments on early version of the manuscript, C.W. Myers (AMNH) , G.R. Zug (USNM), W.E. Duellman (KU), B. Clarke and C. McCarthy (BMNH) and G. Köhler (SMF) kindly provided working space and facilities for specimen examination of collections at their care. We thank S.B. Hedges for help with species comparisons; K. Tige for X-ray plates and G. Zug (USNM) and J. Icochea for clearing and staining. We thank W.E. Duellman and L. Trueb for their hospitality during our visits to KU. LOR thanks C.W. Myers for help with the initial descriptions and for extending many courtesies during her visits to the AMNH, L.S. Ford for her help with defining localities, F. Chang (+) for drawing Figure 9 and M. T. Fuentes (CIMA-Cordillera Azul), for Figure 2; D. Rödder for providing working space at the König Zoological Museum of Bonn, and M. Flecks for assisting with holotype photographs. The inventories conducted by the Asociación Peruana para la Conservación de la Naturaleza (APECO) in Río Abiseo NP were funded by grants from the David and Lucille Packard Foundation and the PEW Charitable Fund, through the University of Colorado at Boulder. Visits to AMNH were supported through a Collection Study Grant and to KU with support from the University of Kansas. A visit to the National Museum of Natural History, Smithsonian Institution was supported by the Biological Diversity Program in Latin America (BIOLAT). The Dirección General Forestal y de Fauna of the Ministerio de Agricultura, Lima, provided the necessary permits for scientific collections within Río Abiseo National Park.

References

Boyle, D.G., Boyle, D.B., Olsen,V., Morgan, J.A.T. & Hyatt, A.D. (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60, 141–148. https://doi.org/10.3354/dao060141 Cadle, J.E. (1991) Systematics of lizards of the genus Stenocercus (Iguania: Tropiduridae) from northern Perú: new species and comments on relationships and distribution patterns. Proceedings of the Academy of Natural Sciences of Philadelphia, 143, 1–96. Cannatella, D.C. (1984). Two new species of the leptodactylid frog genus Phrynopus, with comments on the phylogeny of the genus. Occasional Papers, Museum of Natural History, University of Kansas, 113, 1–16. Catenazzi, A., Lehr, E., Rodriguez, L.O. & Vredenburg, V.T. (2011) Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the upper Manu National Park, southeastern Peru. Conservation Biology, 25, 382–391. Catenazzi, A., Lehr, E. & Vredenburg, V.T. (2014) Thermal physiology, disease and amphibian declines in the eastern slopes of the Andes. Conservation Biology, 28, 509–517. https://doi.org/10.1111/cobi.12194 Catenazzi, A. & Ttito, A. (2016) A new species of Psychrophrynella (Amphibia, Anura, Craugastoridae) from the humid montane forests of Cusco, eastern slopes of the Peruvian Andes. PeerJ, 4, e1807. https://doi.org/10.7717/peerj.1807 Catenazzi, A. & von May, R. (2014) Conservation status of amphibians in Peru. Herpetological Monographs, 28, 1–23. https://doi.org/10.1655/HERPMONOGRAPHS-D-13-00003 Chaparro, J.C., Padial, J.M. & De la Riva, I. (2008) Two sympatric new species of Phrynopus (Anura: Strabomantidae) from Yanachaga Chemillén National Park (central Peruvian Andes). Zootaxa, 1761, 49–58. Chávez, G., Santa-Cruz, R., Rodríguez, D. & Lehr, E. (2015) Two new species of frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from the Peruvian Andes. Amphibian and Reptile Conservation, 9, 15–25. (e105)

404 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI Dingerkus, G. & Uhler, L.D. (1977) Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technology, 52, 229–232. https://doi.org/10.3109/10520297709116780 Duellman, W.E. (1979) The herpetofauna of the Andes: patterns of distribution, origin, differentiation, and present communities. In: Duellman, W.E. (Ed.), The South American Herpetofauna: Its Origin, Evolution and Dispersal. University of Kansas, Museum of Natural History Monographs, 7, pp. 371–459. Duellman, W.E. (2000) Leptodactylid frogs of the Genus Phrynopus in northern Peru with descriptions of three new species. Herpetologica, 56, 273–285. Duellman, W.E. & Wild, E.R. (1993) Anuran amphibian from the Cordillera de Huancabamba, northern Peru: Systematics, ecology, and biogeography. Occasional Papers, Museum of Natural History, University of Kansas, 1557, 1–53. Duellman, W.E. & Lehr, E. (2009) Terrestrial breeding frogs (Strabomantidae) in Peru. Natur und Tier Verlag, Naturwissenschaft, 382 pp. Frost, D.R. (2016) Amphibian species of the world: an online reference. Version 6.0 Electronic Database accessible. American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 2 January 2017). Gardner, A. & Romo, M. (1993) A new Thomasomys (Mammalia: Muridae: Sigmodontinae) from the Peruvian Andes. Proceedings of the Biological Society of Washington, 106, 762–774. Hedges, S.B. (1990) A new species of Phrynopus (Anura: Leptodactylidae) from Peru. Copeia, 1990, 108–112. https://doi.org/10.2307/1445826 Hedges, S.B, Duellman, W.E. & Heinicke, M.P. (2008) New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737, 1–182. Heinicke, M.P., Duellman, W.E. & Hedges, S.B. (2007) Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences, 104, 10092–10097. https://doi.org/10.1073/pnas.0611051104 Hyatt, A.D., Boyle, D.G., Olsen, V., Boyle, D.B., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. & Colling, A. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 73, 175–192. https://doi.org/10.3354/dao073175 IUCN Standards and Petitions Subcommittee (2017) Guidelines for using the IUCN Red List categories and criteria. Version 13. Prepared by the Standards and Petitions Subcommittee. Available from: http://www.iucnredlist.org/documents/ RedListGuidelines.pdf (accessed 22 May 2017) Lehr, E. & Aguilar, C. (2002) A new species of Phrynopus (Amphibia, Anura, Leptodactylidae) from the puna of Maraypata (Departamento de Huanuco, Peru). Zoologische Abhandlungen (Dresden), 52, 57–64. Lehr, E. & Aguilar, C. (2003) A new species of Phrynopus (Amphibia, Anura, Leptodactylidae) from the puna of Maraypata (Departamento de Huánuco, Peru). Zoologische Abhandlungen (Dresden), 53, 87–92. Lehr, E. & Catenazzi, A. (2010) Two new species of Bryophryne (Anura: Strabomantidae) from high elevations in southern Peru (Region of Cusco). Herpetologica, 66, 308–319. https://doi.org/10.1655/09-038.1 Lehr, E. & Catenazzi, A. (2011) A new species of marsupial frog (Anura: Hemiphractidae: Gastrotheca) from the Río Abiseo National Park in Perú. Herpetologica, 67, 449–459. https://doi.org/10.1655/HERPETOLOGICA-D-11-00002.1 Lehr, E., Gregory, C. & Catenazzi, A. (2013) A new species of Pristimantis (Anura: Strabomantidae) from the Rio Abiseo National Park, Peru. Zootaxa, 3731 (2), 201–211. https://doi.org/10.11646/zootaxa.3731.2.1 Lehr, E., Köhler, G. & Ponce, E. (2000) A new species of Phrynopus from Peru (Amphibia, Anura, Leptodactylidae). Senckenbergiana Biologica, 80, 205–212. Lehr, E., Lundberg, M. & Aguilar, C. (2005) Three new species of Phrynopus from central Peru (Amphibia: Anura: Leptodactylidae). Copeia, 2005, 479–491. https://doi.org/10.1643/CH-04-278R2 Lehr E., Moravec, J. & Cusi, J.C. (2012) Two new species of Phrynopus (Anura, Strabomantidae) from high elevations in the Yanachaga-Chemillén National park in Peru (Departamento de Pasco). ZooKeys, 235, 51–71. https://doi.org/10.3897/zookeys.235.3885 Lehr, E. & Oróz, A. (2012) Two new species of Phrynopus (Anura: Strabomantidae) from the Cordillera de Carpish in central Peru (Departamento de Huánuco). Zootaxa, 3512, 53–63. Lehr, E. & von May, R. (2017) A new species of terrestrial-breeding frog (Amphibia, Craugastoridae, Pristimantis) from high elevations of the Pui Pui Protected Forest in central Peru. ZooKeys, 660, 17–42. https://doi.org/10.3897/zookeys.660.11394 Leo, M. & Gardner, A. (1993) A new species of a giant Thomasomys (Mammalia: Muridae: Sigmodontinae) from the Andes of northcentral Peru. Proceedings of the Biological Society of Washington, 106, 417–428. Lynch, J.D. (1975) A review of the andean leptodactylid frog genus Phrynopus. Occasional PapErs, Museum Of Natural History, University of Kansas, 35, 1–51. Lynch, J.D. (1986) Chapter 19. Origins of the high Andean herpetological fauna. In: Vuilleumier, F. & Monasterio, M. (Eds.),

FOUR NEW SPECIES OF PHRYNOPUS Zootaxa 4273 (3) © 2017 Magnolia Press · 405 High altitude tropical biogeography. Oxford University Press, Oxford & New York, pp. 479–499. Lynch, J. D. & Duellman, W.E. (1980) The Eleutherodactylus of the Amazonian slopes of the Ecuadorian Andes (Anura: Leptodactylidae). University of Kansas, Museum of Natural History Miscellaneous Publications, 69, 1–86. Lynch, J. D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador: systematics, ecology, and biogeography. Special Publication Natural History Museum University of Kansas, 23, 1–236. Mamani, L. & Malqui, S. (2014) A new species of Phrynopus (Anura: Craugastoridae) from the central Peruvian Andes. Zootaxa, 3838 (2), 207–214. https://doi.org/10.11646/zootaxa.3838.2.5 Padial J., Grant, T. & Frost, D.R. (2014) Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria. Zootaxa, 3825 (1), 1–132. https://doi.org/10.11646/zootaxa.3825.1.1 Rodbell, D.T., Birkeland, P.W., Miller, D.C. & Hansen, B.C.S. (1992) Resultados del estudio geológico y palinológico en el Parque Nacional Río Abiseo y zona adyacente. In: Aguilar, P. (Ed.), Resúmenes del Symposio Biodiversidad, historia cultural y futuro del Parque Nacional Río Abiseo. APECO, Lima, pp. 11. Trueb, L. & Lehr, E. (2008) A new species of Phrynopus (Anura, Strabomantidae) from Peru, with comments on the osteology of the genus. Phyllomedusa, 7, 11–24. https://doi.org/10.11606/issn.2316-9079.v7i1p11-24 Venegas, P.J., Catenazzi, A., Siu-Ting, K. & Carrillo, J. (2008) Two new species of harlequin frogs (Anura: Bufonidae: Atelopus) from the Andes of northern Peru. Salamandra, 44, 163–176.

APPENDIX I. Specimens examined

Phrynopus bracki: PERU: PASCO: 2.9 km N, 5.5 km E (airline) Oxapampa, Cordillera Yanachaga (2600 m), USNM 286918 (holotype), 286919, MUSM 4400 (paratype). Phrynopus chaparroi: PERU: JUNÍN: Canchapalca, Distrito de Comas, Provincia Concepción, (11°44'45" S, 74°58'47"W): MHNC 10983 (holotype, 4490 m.), MHNC 10980–10982 (4490 m.), MHNC 10984 and MHNC 10985 (4205 m.). Phrynopus dagmarae: PERU: HUÁNUCO: Distrito Chaglla, Provincia Pachitea, Chaglla-Palteanan (09°51´27"S, 75°53´12"W): SMF 80480–83; Maraypata (10°09´35"S, 7´6°06´05"W, 3370 m), SMF 80475 (paratype); Palma Pampa (09°53´12"S, 75°53´22"W): SMF 80476–79 and 80629–33 (paratypes); E slope Cordillera Carpish, Carretera Central, 2400 m: KU 196592. Phrynopus heimorum: PERU: HUÁNUCO: Provincia Ambo, Conchamarca: SMF 80470, 80474 (09°59´44”S, 76°09´40”W, 3420m); 500 m east of Conchamarca (09°59´44”S, 76°09´40”W, 3420m): SMF 80471–80472. Phrynopus horstpauli: PERU: HUÁNUCO: Provincia Ambo, 7 km east of Conchamarca, Huacamonte forest (09°5955”S, 76°09´43”W, 3070 m): SMF 80447–52, 80459–60; Huacamonte forest (09°59´41”S, 76°09´44”W, 3420 m): SMF 80466– 67; Ichocan, Jatunloma, 3100 m: KU 291399–291400, 311452: 10 km E of Conchamarca, 3420 m: KU 311453. Phrynopus kauneorum: PERU: HUÁNUCO: Chaggla, SMF 80626–28, SMF 80484–85, AMNH 311451. Phrynopus montium: PERU: JUNÍN: Tarma, 45 min. of Maranyioc (12000 ft = 3658 m), USNM 217416–17; JUNÍN: Prov. Yauli, 9.5 min. from La Oroya (13000 ft = 3962 m), AMNH 84795. Phrynopus valquii: PERU: SAN MARTÍN: Río Abiseo NP: MUSM 3824, MUSM 3821, 3823, KU 220918 and AMNH 134154– 55. Pristimantis simonsii: PERU: CAJAMARCA: 23 km S Celendín, 3050, KU 181357- -181360; 33 km S Celendín, 3200 m, KU 181361--181391, 181830--181833, MUSM 1526--1527, 1546-1548; NE Encanada-, 23,5 km from Cajamarca, 3510 m, MUSM 1160 (cleared and stained), 1161--1179; CAJAMARCA, 3500 M, BM 1900.3.30.22-23, Lectotype "Paramo, Cajamarca, 9000 feet".

APPENDIX 2. Museum specimens analyzed for the presence of Batrachochytrium dendrobatidis through skin swabbing (November 2015) and quantitative PCR (see methods). ZE = zoospore equivalents

Specimen # Species Collection date Status ZE

AMNH 134158 P. capitalis 3 July 1989 Negative – AMNH 134149 P. dumicola 29 July 1988 Negative – AMNH 134150 P. dumicola 29 July 1988 Negative – AMNH 134152 P. dumicola 19 July 1988 Positive 9.57 KU 220917 P. dumicola 18 July 1987 Negative – AMNH 84795 P. montium 13 June 1964 Negative – AMNH 134153 P. personatus 23 July 1989 Negative – AMNH 134154 P. valquii 23 July 1987 Negative – AMNH 134155 P. valquii 28 July 1987 Negative –

406 · Zootaxa 4273 (3) © 2017 Magnolia Press RODRÍGUEZ & CATENAZZI

View publication stats