South American Journal of Herpetology, 4(2), 2009, 125-138 © 2009 Brazilian Society of Herpetology

THREE NEW SPECIES OF BRYOPHRYNE (ANURA: STRABOMANTIDAE) FROM THE REGION OF CUSCO, PERU Edgar Lehr1,3 and Alessandro Catenazzi2 Senckenberg Naturhistorische Sammlungen Dresden, Museum für Tierkunde, Königsbrücker Landstrasse 159, D‑01109 Dresden, Germany. 2 Department of Integrative Biology, University of California at Berkeley. 3060 Valley Life Sciences Bldg #3140, Berkeley CA 94720, USA. Email: [email protected] 3 Corresponding Author: [email protected] 1

Abstract. We describe three new species of Bryophryne from the Region of Cusco in southern Peru, increasing the number of currently known Bryophryne to six. One of the new species differs from all species of Bryophryne in having a tympanic annulus and tympanic membrane. Males of this species have vocal slits, a vocal sac, and produce a call, which we analyze herein. This species is found at San Luis, a montane cloud forest along the road from Abra Málaga to Quillabamba at elevations between 3272 and 3354 m. The second new species has an orange throat and groin and is found along the Ericsson trail that connects Acjanaco to Pillahuata in Manu National Park and near Abra Acjanaco along the Paucartambo-Pilcopata road at elevations between 3266 and 3430 m. The third new species has the throat and chest mottled pale gray and tan, whereas the belly is black with white flecks. This species is only known from the upper Marcapata valley along the road from Abra Huallahualla to Quincemil at elevations between 3129 and 3285 m. Ecological observations for all new species are described and a map showing the type localities of all currently known species of Bryophryne is presented. Keywords. Anura, Bryophryne, new species, Strabomantidae, vocalization.

Introduction The genus Bryophryne was described by Hedges et  al. (2008). Based on DNA sequences, their phylogenetic analysis of strabomantid frogs recognized a distinct clade among Holodeninae that consisted of the single species B.  cophites (formerly Phryno‑ pus cophites Lynch, 1975). Phrynopus bustamantei Chaparro, De la Riva, Padial, Ochoa, and Lehr, 2007, was assigned to Bryophryne by Hedges et al. (2008) based on morphological similarities with B. cophites. Lehr and Catenazzi (2008) recently described B. nu‑ bilosus from the Region of Cusco in southern Peru. Both authors hypothesized that the deep valley of the Rio Apurimac is a biogeographic border separating Phrynopus from Bryophryne (Lehr and Catenazzi, 2008), and pointed out that new species will likely be discovered when fieldwork continues. Herein we describe three new species of Bryophryne recently discovered in the Region of Cusco southeast of the Rio Apurimac valley, thus doubling the number of species within the genus. Materials and Methods Taxonomy follows Hedges et  al. (2008) and the format for the description follows that of Lynch and Duellman (1997), except that we used the term dentigerous processes of vomers instead of vomerine

odontophores (Duellman et al., 2006). We follow the definition of conditions of the tympanum by Lynch and Duellman (1997). Specimens were preserved in 10% formalin and stored in 70% ethanol. Specimens were dissected to determine sex and maturity, and the otic region was dissected in order to determine condition of the tympanic annulus. We measured the following variables to the nearest 0.1 mm with digital calipers under a microscope: snout-vent length (SVL), tibia length (TL), foot length (FL, distance from proximal margin of inner metatarsal tubercle to tip of Toe IV), head length (HL, from angle of jaw to tip of snout), head width (HW, at level of angle of jaw), eye diameter (ED), tympanum diameter (TY), interorbital distance (IOD), upper eyelid width (EW), internarial distance (IND), eye-nostril distance (E‑N, straight line distance between anterior corner of orbit and posterior margin of external nares). We determined comparative lengths of Toes III and V by adpressing both toes against Toe IV; lengths of Fingers I and II were determined by adpressing the fingers against each other. Drawings were made by the senior author using a stereomicroscope with drawing tube attachment. Photographs taken by A. Catenazzi were used for descriptions of color in life and are available for all types at the Calphoto online database (http:// calphotos.berkeley.edu). We recorded advertisement calls for one of the new species with a Sony TCM‑150 audio tape-recorder equipped with a Azden SMX‑10 microphone.

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We used Cool Edit version 96 (Syntrillium Software Corporation) and Raven Lite, version 1.0 (Cornell Laboratory of Ornithology) to digitalize calls and analyze sonograms. We digitized and edited vocalizations at a sampling frequency of 44 KHz, FFT with 512 points, and 16‑bit resolution. Locality names follow the spelling of the US Board on Geographic Names (http://gnswww.nga. mil) and, for localities not listed in this database, according to Cartas Nacionales “Calca” (Hoja 27‑s), “Corani” (28‑u), “Ocongate” (28‑t) and “Urubamba” (27‑r), Instituto Geográfico Nacional, Lima (except for Acjanaco = Acanaco, Acanacu). We deposited specimens in the herpetological collections of the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos (MUSM) in Lima, Peru, Museum für Tierkunde Dresden (MTD), Germany, the Museum of Vertebrate Zoology, University of California Berkeley (MVZ), and the Musée d’Histoire Naturelle de la Ville de Genève, Geneva, Switzerland (MHNG). For specimens examined, see Appendix. Bryophryne gymnotis sp. nov. (Figs. 1 and 2)

pads absent; (7) Finger I shorter than Finger II; tips of digits rounded; (8)  fingers with lateral fringes; (9) ulnar and tarsal tubercles present; (10) heel with small tubercles; inner tarsal fold absent; (11)  inner metatarsal tubercle ovoid, about twice as large as rounded outer metatarsal tubercle; supernumerary plantar tubercles indistinct; (12) toes with lateral fringes; basal webbing present; Toe V shorter than Toe III; toe tips rounded, about as large as those on fingers; (13) in life, dorsum reddish brown, grayish brown, purplish brown, or dark gray, with narrow tan middorsal stripe, venter dark brown, tan, or reddish brown with pale gray flecks; (14)  SVL in adult females 16.0‑22.2 mm (n = 10), in males 16.7‑19.3 mm (n = 10). Bryophryne gymnotis is readily distinguished from the other currently known five species (including the ones described herein) in having a tympanic membrane and tympanic annulus, and a smooth (areolate in all others) venter. Furthermore, it differs from all its congeners in having the dorsal color uniform reddish brown, gray, dark brown, or purplish brown, with a narrow, tan middorsal stripe, and a ventral

Holotype – MUSM 24543. Adult male, collected 1 km east of San Luis (13°04’32.1”S, 72°22’55.3”W) at elevations of 3272‑3354 m, Distrito de Huayopata, Provincia de La Convención, Región Cusco, Peru, on 8 March 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. Paratypes – 29: 10 females (MHNG 2710.28, MTD 46860‑61, 47297, MUSM 24546‑50, MVZ 258407), 8 males (MTD 47288, 47291‑92, MUSM 24541‑42, 24544‑45, MVZ 258408‑09), 11 juveniles (MNNG 2710.29, MTD 46862‑64, MUSM 24551‑56, MVZ 258410), all collected with the holotype on 8 March 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. Diagnosis – A medium sized species of Bryophryne having the following combination of characters: (1) skin on dorsum shagreen, skin on venter smooth; discoidal fold absent, thoracic fold present; narrow, discontinuous dorsolateral fold; (2)  tympanic membrane and tympanic annulus present; (3)  snout rounded in dorsal and lateral views; (4)  upper eyelid without enlarged tubercles; width of upper eyelid narrower than IOD; cranial crests absent; (5) dentigerous processes of vomers present, minute, oblique; (6) males with vocal sac and vocal slits, but nuptial

Figure  1. Holotype of Bryophryne gymnotis in life (MUSM 24543, male) in lateral (A), and ventral (B) views. Photos by A. Catenazzi.

Lehr, E. and Catenazzi, A.



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color of tan, reddish brown, or dark brown with pale gray flecks. Table  1 compares selected characters among species of Bryophryne.

one half free; vocal slits straight, located at posterior half of mouth floor between tongue and margin of jaw; vocal sac distinct.

Description of holotype – Head narrower than body, slightly wider than long, HW 102.8% of HL; HW 40.2% of SVL; HL 39.1% of SVL; snout short, acutely rounded in dorsal view, rounded in lateral view (Figs. 2A, B), ED larger than E‑N distance; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis straight in dorsal view, rounded in profile; loreal region slightly concave; lips rounded; upper eyelid without enlarged tubercles; EW narrower than IOD (EW 58.3% of IOD); supratympanic fold narrow, slightly curved, extending from posterior corner of eye to insertion of arm; tympanic membrane and tympanic annulus present, weakly defined, upper and posterior margin concealed by supratympanic fold; two enlarged postrictal tubercles on each side of head. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers present, minute, embedded in buccal mucosa, oblique; tongue 3x as long as wide, not notched posteriorly, posterior

Skin on dorsum shagreen, short occipital fold merging into narrow dorsolateral fold extending to sacral region, anterior part continuous, posterior part discontinuous; skin on flanks slightly tuberculate with tubercles coalescing into long, narrow fold on upper part on both side of flanks; skin on throat, chest, and belly smooth; discoidal fold absent, thoracic fold present; cloacal sheath absent; large tubercles absent in cloacal region. Outer surface of forearm with four minute tubercles (= ulnar tubercles, only two are visible in Fig. 2C) arranged in a longitudinal row; outer and inner palmar tubercles low, ovoid, about equal in size; supernumerary tubercles distinct, low, ovoid, about one third size of subarticular tubercles; subarticular tubercles prominent, ovoid in dorsal view, rounded in lateral view, most prominent on base of fingers; fingers with lateral fringes; Finger I shorter than Finger II; tips of digits rounded lacking marginal grooves (Fig. 2C).

Figure 2. Dorsal (A) and lateral (B) views of head and ventral views of left hand (C) and right foot (D) of Bryophryne gymnotis (MUSM 24543). Drawings by E. Lehr.

Three new species of Bryophryne

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Table 1. Selected characters (+ = character present; — = character absent), character conditions, and elevational distribution among Bryophryne.

Characters and source Maximum SVL (mm) Female SVL Male SVL Tympanic annulus Tympanic membrane Dentigerous processes of vomers Dorsolateral folds Skin on venter Vocal sac Vocal slits Lateral fringes Nuptial pads Finger I < II Elevational distribution [m]

B. gymnotis this paper

B. hanssaueri this paper

B. zonalis this paper

B. bustamantei Chaparro et al., 2007, this paper

22.2 16.0‑22.2 (20.0 ± 2.2) n = 10 16.7‑19.3 (18.1 ± 0.9) n = 10 + +

24.6 18.1‑24.6 (21.7 ± 1.8) n = 12 12.3‑18.0 (15.5 ± 2.8) n = 4 — —

24.4 22.2‑24.4 (23.3 ± 1.1) n = 3 14.8‑17.6 (16.0 ± 1.4) n = 3 — —

23.4 21.0‑23.4 (22.0 ± 1.2) n = 3 19.0‑22.9 (21.0 ± 2.8) n = 2 — —

+

—

—

—

+, discontinuous +, discontinuous +, discontinuous smooth areolate areolate + — — + — — + + + — — — + + + 3272‑3354 3266‑3430 3129‑3285

Hind limbs short, robust, TL 37.0% of SVL; FL 41.3% of SVL; upper surface of hind limbs shagreen with small, scattered tubercles; posterior and ventral surfaces of thighs areolate; heel without small tubercles; outer surface of tarsus with few minute tubercles; metatarsal tubercles prominent, inner metatarsal tubercle ovoid, elevated, about twice the size of round, low outer metatarsal tubercle; few plantar supernumerary tubercles indistinct; subarticular tubercles low, ovoid in dorsal view; toes with lateral fringes, basal webbing present; toe tips rounded, lacking marginal grooves, about as large as those on fingers; relative lengths of toes: 1 < 2 < 5 < 3 < 4; Toe V shorter than Toe III (Fig. 2D). Measurements of holotype (in mm) – SVL 18.4; TL 6.8; FL 7.6; HL 7.2; HW 7.4; ED 1.9; TY 1.1; IOD 2.4; EW 1.4; IND 1.7; E‑N 1.5. Color of holotype in life (Fig. 1) – Dorsum purplish brown with pale gray spots and reddish brown flecks; narrow purplish gray middorsal stripe extending from snout to cloaca; narrow purplish gray stripe extending on both sides from upper margin of cloaca diagonally on posterior surface of thigh to inside of knee; dark brown canthal and supratympanic stripes; dark brown bar below eye; upper and lower lips dark brown with white spots; tips of postrical tubercles white; throat mottled dark brown and tan with white spots and

+, continuous areolate + + — — + 3555‑3950

— —

B. nubilosus Lehr and Catenazzi, 2008, this paper 21.9 19.2‑21.9 (20.5 ± 1.0) n = 5 12.7‑18.9 (14.9 ± 2.2) n = 5 — —

—

—

B. cophites Lynch, 1975 29.3 21.9‑29.3 18.0‑22.7

+, discontinuous +, discontinuous areolate areolate — — — — — — + — + + 3195‑3700 2350‑3215

midventral tan stripe extending to chest; chest, belly, and extremities mottled brown and tan with white and dark brown flecks; concealed surfaces of hind limbs with white flecks; Fingers I‑III, Toes I‑III, and metatarsal tubercles tan, remaining ventral surfaces of hands and feet gray; upper half of iris pale bronze, lower half dark brown, pupil encircled by pale orange ringlet. Color of holotype in preservative – Dorsum mottled dark gray and dark brown with narrow pale gray middorsal stripe extending from snout to cloaca; narrow pale gray stripe extending on both sides from upper margin of cloaca diagonally on posterior surface of thigh to inside of knee; dark brown canthal and supratympanic stripes, latter more distinct; dark brown bar below eye; upper and lower lips dark brown with pale gray spots; flanks as dorsum but slightly paler; tips of postrical tubercles white; throat mottled dark brown and tan with white spots and midventral tan stripe extending to chest; chest, belly, and extremities mottled brown and tan with white and dark brown flecks; concealed surfaces of hind limbs with white flecks; Fingers I‑III, Toes I‑III, and metatarsal tubercles pale gray, remaining ventral surfaces of hands and feet gray; iris gray. Variation – In life, all specimens have a tan middorsal stripe but differ in dorsal ground color, which varies

Lehr, E. and Catenazzi, A.

from reddish brown (MTD 47288), brown (MTD 47292), grayish brown (MUSM 24547), and purplish brown (MUSM 24545, 24548) to dark gray (MVZ 258408). Two females (MUSM 24549‑50) have a tan dorsal band and a paler tan middorsal stripe. One juvenile (MUSM 24554) has the dorsum nearly uniformly tan; two juveniles (MHNG 2710.29, MUSM 24553) have the dorsum pale purplish gray with dark brown blotches and dark brown bars on extremities. Ventral ground color varies from tan (MHNG 2710.28, MTD 47291) to brownish orange (MTD 47288, MUSM 24542) to dark brown (MUSM 24546, MVZ 258408). Two females (MUSM 24549‑50) and two juveniles (MTD 46862, MUSM 24551) have a midventral tan stripe crossed by a longitudinal tan stripe ventrally on arms and legs. Ventral surfaces of juveniles are nearly uniformly dark brown with pale gray spots. Males are smaller than females. The smallest juvenile is 10.3 mm SVL. Table 2 shows ranges and proportions of the type series. Advertisement call – Several males of Bryophryne gymnotis were calling during our visit to the type locality between 1000 h and 1300 h on 8 March 2008. The recorded male (MUSM 24544, SVL 18.9  mm; T = 18.0°C) was found under moss and leaf litter on the ground. The call is a short, single note repeated at irregular intervals and with a fundamental frequency of 3.01 KHz (dominant) and one harmonic at 4.45 KHz (Fig. 3). The call duration ranged from 86 to 136 ms (mean  =  121.0  ±  11.8  ms, n  =  4). Calls were composed of two weakly modulated parts, the first part having a generally ascendent amplitude modulation and a duration of 54 to 82 ms (mean = 69.0 ± 7.6 ms, n = 4), and the second part having a descendent amplitude modulation and a duration of 32 to 78  ms (mean = 52.0 ± 9.7 ms, n = 4). Calls were produced every 29 to 75 s (mean = 50.0 ± 13.3 s, n = 3; time from the end of one call to the beginning of the next



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Table 2. Measurements (in mm) and proportions of Bryophryne gymnotis; ranges followed by means and one standard deviation in parentheses. Characters SVL TL FL HL HW ED TY IOD EW IND E‑N TL/SVL FL/SVL HL/SVL HW/SVL HW/HL E‑N/ED EW/IOD TY/ED

B. gymnotis Females (n = 10) Males (n = 10) 16.0‑22.2 16.7‑19.3 (20.0 ± 2.2) (18.1 ± 0.9) 6.0‑7.5 (6.9 ± 0.4) 6.2‑6.8 (6.6 ± 0.2) 7.0‑9.2 (8.1 ± 0.7) 6.9‑7.9 (7.5 ± 0.3) 6.4‑8.3 (7.5 ± 0.6) 6.7‑7.4 (7.0 ± 0.2) 6.4‑8.5 (7.8 ± 0.7) 6.6‑7.9 (7.2 ± 0.4) 1.8‑2.5 (2.1 ± 0.2) 1.8‑2.1 (1.9 ± 0.1) 0.7‑1.5 (1.0 ± 0.3) 0.7‑1.1 (1.9 ± 0.1) 2.2‑2.9 (2.6 ± 0.2) 2.3‑2.6 (2.4 ± 0.1) 1.3‑1.7 (1.6 ± 0.1) 1.3‑1.7 (1.4 ± 0.1) 1.5‑2.0 (1.7 ± 0.1) 1.3‑1.9 (1.7 ± 0.2) 1.6‑1.9 (1.7 ± 0.1) 1.5‑1.8 (1.7 ± 0.1) 0.32‑0.39 0.34‑0.38 0.37‑0.46 0.40‑0.44 0.34‑0.41 0.35‑0.41 0.38‑0.41 0.38‑0.41 0.96‑1.13 0.97‑1.10 0.72‑1.00 0.79‑0.95 0.50‑0.73 0.54‑0.68 0.38‑0.71 0.37‑0.58

call). Frequency modulation was slight, with the first part of the call having a fundamental frequency of 3.01 KHz (range 2.97‑3.02 KHz) and a harmonic at 4.45 KHz, and the second part having a fundamental frequency of 3.05 KHz (range 2.97‑3.07 KHz). Distribution – The species is only known from the type locality of San Luis, a montane cloud forest along the road from Abra Málaga to Quillabamba at 3272‑3354  m. San Luis is 5.3  km from the closest locality of the congeneric B.  bustamantei (Fig.  4). Based on available information, the elevational range of these two species does not seem to overlap. All specimens were collected under moss, leaf litter, logs, and rocks on the ground during the day in the rainy

Figure 3. Waveform (above) and sonogram (below) of three advertisement calls (separated by intervals of 29‑75 s) of male Bryophryne gymnotis (MUSM 25444) recorded at the type locality (San Luis, Distrito de Huayopata, Provincia de La Convención, Región Cusco, Peru; elevation 3300 m) on 8 March 2008 at 1300 h (air temperature = 18.0°C).

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season. A clutch of B.  gymnotis found at the type locality contained 19 eggs ranging between 4.0 and 4.8 mm in diameter. Etymology – The specific name gymnotis is composed of the Greek adjective gymnos meaning “bare, naked,” and the Greek noun “otos” meaning ear. The specific name refers to the character condition of the new species, which currently is the only member of the genus having a tympanum. Bryophryne hanssaueri sp. nov. (Figs. 5 and 6) Holotype – MUSM 27567. Adult female, collected at Acjanaco, Manu National Park (13°10’58.4”S, 71°37’11.7”W) at 3266  m elevation, Distrito de Cosñipata, Provincia de Paucartambo, Región Cusco, Peru, on 24 February 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. Paratypes – 17: 11 females (MHNG 2698.25, MTD 46865, 46887‑89, MUSM 24557, 27608‑11, MVZ 258411), 4 males (MTD 46866, MUSM 27568, 27607, MVZ 258413), and two juveniles (MUSM 27569, MVZ 258412), all from near Acjanaco (= Acanaco, Acanacu), Manu National Park, Distrito de Cosñipata, Provincia de Paucartambo, Región Cusco,

Figure 4. Map illustrating the type localities of Bryophryne in Peru.

Peru. MUSM 24557, MVZ 258411 (13°11’29.4”S, 71°37’18.3”W) collected at 3381  m elevation on 23 February 2008; MTD 46865 (13°11’14.9”S, 71°37’18.6”W) at 3313 m elevation on 24 February 2008; MTD 46866, MUSM 27568‑69, MVZ 258412 (13°10’10.3”S, 71°37’51.2”W) at 3417  m elevation on 28 February 2008. Collected by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. MTD 46888, MUSM 27610 (13°11’28.3”S, 71°37’19.0”W) collected at 3360  m elevation on 23 October 2008. MHNG 2698.25, MUSM 27607, 27609, MVZ 258413 (13°11’15.5”S, 71°37’18.9”W) collected at 3320 m elevation on 23 October 2008. MTD 46889, MUSM 27608, 27611 (13°11’07.7”S, 71°37’16.9”W) at 3280 m elevation on 24 October 2008. MTD 46887 (13°11’57.8”S, 71°36’27.3”W) at 3430 m on 25 October 2008. Collected by A. Catenazzi, D. Cruz, J. C. Jahuanchi, and E. Luna. Diagnosis – A medium-sized species of Bryophryne having the following combination of characters: (1) skin on dorsum shagreen with small scattered tubercles, skin on venter areolate; discoidal fold absent, thoracic fold present; short, irregularly shaped, discontinuous dorsolateral fold; (2) tympanic membrane and tympanic annulus absent; (3)  snout rounded in dorsal and lateral views; (4) upper eyelid without enlarged tubercles; width of upper eyelid narrower than

Lehr, E. and Catenazzi, A.

IOD; cranial crests absent; (5) dentigerous processes of vomers absent; (6) males without vocal sac, vocal slits, and nuptial pads; (7) Finger I shorter than Finger II; tips of digits rounded; (8) fingers with lateral fringes; (9) ulnar tubercles coalesced to narrow fold; tarsal tubercles present; (10) heel with small tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, twice as large as rounded outer metatarsal tubercle; supernumerary plantar tubercles indistinct; (12) toes with lateral fringes; basal webbing present; Toe V usually longer than Toe III; toe tips slightly pointed, about as large as those on fingers; (13)  in



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life, dorsum pale grayish brown with a dark brown X‑shaped or triangular blotch on head, with or without narrow middorsal tan stripe, in females throat orange, chest and belly pale grayish white; in males venter brownish orange with grayish white flecks on chest and belly; (14) SVL in adult females 18.1‑24.6 mm (n = 12), in males 12.3‑18.0 mm (n = 4). Bryophryne hanssaueri differs from the other currently known five species (including the ones described herein) in that females have an orange (brownish or reddish orange in males) throat and orange (brownish or reddish orange in males) groin. Furthermore it differs from B.  cophites in being smaller (maximum SVL 24.6 mm in B. hanssaueri vs. 29.3 mm: Lynch, 1975). Bryophryne hanssaueri differs from B. gymnotis in lacking a tympanum. Male B. hanssaueri lack vocal slits and a vocal sac, both of which are present in B. gymnotis and B. bustamantei. Furthermore B. bustamantei has a continuous dorsolateral fold (discontinuous, short in B.  hanssaueri) and the flanks have prominent warts (small tubercles). Bryophryne hanssaueri and B. nubilosus both have flanks with tubercles and discontinuous dorsolateral folds, but the folds are more prominent in B. nu‑ bilosus, and B.  nubilosus has two slightly enlarged tubercles on the upper eyelid (absent in B. hanssau‑ eri). Bryophryne zonalis is larger than B. hanssaueri (max SVL 26.8  mm vs. 24.6  mm in B.  hanssaueri) and female Bryophryne zonalis have a black belly with white flecks (belly pale grayish white in female B. hanssaueri). Table 1 compares selected characters among species of Bryophryne. Description of holotype – Head narrower than body, wider than long, HW 115.4% of HL; HW 39.6% of SVL; HL 34.4% of SVL; snout short, rounded in dorsal and lateral views (Figs.  6A,  B), ED larger than E‑N; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis straight in dorsal view, rounded in profile; loreal region slightly concave; lips rounded; EW without enlarged tubercles; EW narrower than IOD (EW 73.1% of IOD); supratympanic fold low, narrow; tympanic membrane and tympanic annulus absent; two enlarged postrictal tubercles on each side of head. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers absent; tongue 2x as long as wide, not notched posteriorly, posterior one third free.

Figure  5. Holotype of Bryophryne hanssaueri in life (MUSM 27567, female) in lateral (A), dorsal (B), and lateroventral (C) views. Photos by A. Catenazzi.

Skin on dorsum shagreen with small scattered tubercles; dorsolateral fold from posterior margin of eye

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to sacral region, low, discontinuous; skin on flanks slightly tuberculate; skin on throat smooth, skin on chest and belly areolate; discoidal fold absent, thoracic fold present; cloacal sheath absent; large tubercles absent in cloacal region. Outer surface of forearm (= ulnar) with a narrow fold extending from outer margin of hand three-fourths distance to elbow; outer and inner palmar tubercles low, outer ovoid, about twice size of inner elongate palmar tubercle; supernumerary tubercles indistinct; subarticular tubercles prominent, ovoid in dorsal view, rounded in lateral view, most prominent on base of fingers; fingers with lateral fringes; Finger I shorter than Finger II; tips of digits slightly pointed, lacking marginal grooves (Fig. 6C). Hind limbs short, robust, TL 34.8% of SVL; FL 40.5% of SVL; upper surface of hind limbs shagreen with small, scattered tubercles; posterior and ventral surfaces of thighs areolate; heel with small tubercles; outer surface of tarsus with few, minute tubercles; metatarsal tubercles low, inner metatarsal tubercle elongate, about twice size of ovoid outer metatarsal

tubercle; plantar supernumerary tubercles indistinct; subarticular tubercles low, ovoid in dorsal view, most prominent on base of toes; toes with lateral fringes, basal webbing present; toe tips slightly pointed, lacking marginal grooves, slightly smaller than those on fingers; relative lengths of toes: 1 < 2 < 3 < 5 < 4; Toe V longer than Toe III (Fig. 6D). Measurements of holotype (in mm) – SVL 22.7; TL 7.9; FL 9.2; HL 7.8; HW 9.0; ED 2.4; IOD 2.6; EW 1.9; IND 2.2; E‑N 1.8. Color of holotype in life (Fig. 5) – Dorsum pale grayish brown with an irregularly shaped dark brown blotch on head; flanks slightly paler, axilla mottled pale gray and white; groin bright orange; dark brown canthal and supratympanic stripes, the latter less distinct; throat bright orange; chest, belly, and extremities (except hands and feet) pale grayish white with grayish brown flecks; hands and feet ventrally brownish orange; iris greenish gold with fine black reticulations.

Figure 6. Dorsal (A) and lateral (B) views of head and ventral views of left hand (C) and left foot (D) of Bryophryne hanssaueri (MUSM 27567). Drawings by E. Lehr.

Lehr, E. and Catenazzi, A.

Color of holotype in preservative – Dorsum grayish brown with an irregularly shaped brown blotch on head; dark brown canthal stripe; supratympanic stripe indistinct; groin and throat pale orange; chest, belly, and extremities cream with grayish brown flecks; hands and feet ventrally pale gray; iris gray. Variation – Adult females have a bright orange throat and groin, whereas adult males have a brownish or reddish orange throat and groin. In juveniles, throat and groin are tan, distinct dark brown canthal and supratympanic stripes, a dark brown X‑shaped blotch on head, and dark brown blotches on extremities on a tan dorsum are present. One juvenile (MUSM 27569) has a dark brown diagonal stripe on both sides of the flanks. Five adult females (MTD 46888, MUSM 24557, 27608‑09, MVZ 258411) and one male (MUSM 27607) have a narrow tan middorsal stripe, and a narrow tan diagonal stripe on posterior surfaces of the thighs and on concealed surfaces of the shanks. Two females (MTD 46865, MUSM 24557) have a X‑shaped blotch on the head. Four females (MTD 46888, MUSM 27608‑09, MVZ 258411) and three males (MTD 46866, MUSM 27568, 27607) have a triangular-shaped blotch on the head. Two females (MUSM 24557, MVZ 258411) and two males (MTD 46866, MUSM 27568) have a dark brown blotch on upper lip below the eye. Males are smaller than females and lack vocal slits, nuptial pads, and a vocal sac. The smallest juvenile is 9.3 mm SVL (MVZ 258412). Table 3 shows ranges and proportions of the type series. Distribution – Bryophryne hanssaueri has only been collected from the type locality (Fig. 4) at elevations between 3266 and 3430  m along the Ericsson trail that connects Acjanaco to Pillahuata in Manu National Park and near Abra Acjanaco along the Paucartambo-Pilcopata road. Etymology – The species is dedicated to Hans Sauer, Germany, for supporting the BIOPAT initiative. Bryophryne zonalis sp. nov. (Figs. 7 and 8) Holotype – MUSM 27570. Adult female, collected at Kusillochayoc (13°34’38.7”S, 71°00’08.6”W) at 3129  m elevation, Distrito de Marcapata, Provincia de Quispicanchis, Región Cusco, Peru, on 4 March 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca.



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Paratypes – Nine: three females (MTD 46867, MUSM 27572, MVZ 258414), three males (MTD 46870, MUSM 27574, MVZ 258415), and three juveniles (MTD 46869, MUSM 27575, 27861). All were collected with the holotype (except MVZ 258415) on 4 March 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. MVZ 258415 was collected at Puente Coline (13°34’37.7”S, 71°00’23.8”W), 3285  m elevation, Distrito de Marcapata, Provincia de Quipicanchis, Región Cusco, Peru, on 5 March 2008 by A. Catenazzi, I. Chinipa, J. C. Jahuanchi, and A. Machaca. Diagnosis – A medium-sized species of Bryophryne having the following combination of characters: (1) skin on dorsum shagreen, skin on venter areolate; discoidal fold absent, thoracic fold present, weakly defined; dorsolateral fold usually discontinuous; (2)  tympanic membrane and tympanic annulus absent; (3)  snout rounded in dorsal and lateral views; (4)  upper eyelid without enlarged tubercles; width of upper eyelid narrower than IOD; cranial crests absent; (5)  dentigerous processes of vomers absent; (6) males without vocal sac, vocal slits, and nuptial pads; (7) Finger I shorter than Finger II; tips of digits rounded; (8) fingers with lateral fringes; (9) ulnar and tarsal tubercles present; (10) heel without tubercles; inner tarsal fold absent; (11) inner metatarsal tubercle ovoid, one and a half the size of outer metatarsal tubercle; outer metatarsal tubercle rounded; supernumerary plantar tubercles indistinct; (12) toes with lateral fringes; basal webbing present; Toe V slightly longer or equal to Toe III; toe tips rounded, about as large as those on fingers; (13)  in life, dorsum pale gray, grayish brown or tan, throat and chest pale gray and tan mottled, belly black with white flecks; (14) SVL in adult females 12.2‑24.4 (n = 3), in males 14.8‑17.6 mm (n = 3). Bryophryne zonalis differs from the other currently known five species (including the ones described herein) in having females that have a black belly with white flecks, a mottled pale gray and tan throat and chest, and partly reddish fingers and toes. Bryophryne zonalis (maximum SVL 24.4  mm) is much smaller than B.  cophites (maximum SVL 29.3  mm, Lynch, 1975), larger than B.  bustamantei (maximum SVL 23.4 mm, Chaparro et al., 2007), B. gymnotis (maximum SVL 22.2  mm), B.  nubilosus (maximum SVL 21.9 mm), and about equal in SVL to B. hanssaueri (maximum SVL 24.6 mm). Table 1 compares selected characters among species of Bryophryne.

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Table 3. Measurements (in mm) and proportions of Bryophryne hanssaueri and B. zonalis; ranges followed by means and one standard deviation in parentheses. Characters SVL TL FL HL HW ED IOD EW IND E‑N TL/SVL FL/SVL HL/SVL HW/SVL HW/HL E‑N/ED EW/IOD

B. hanssaueri Females (n = 12) Males (n = 4) 18.1‑24.6 (21.7 ± 1.8) 12.3‑18.0 (15.5 ± 2.8) 6.5‑8.1 (7.5 ± 0.5) 4.7‑5.8 (5.4 ± 0.5) 7.2‑9.5 (8.7 ± 0.8) 5.2‑6.4 (5.9 ± 0.5) 6.9‑8.4 (7.7 ± 0.5) 5.2‑6.5 (5.9 ± 0.6) 6.9‑9.0 (8.0 ± 0.7) 4.5‑5.9 (5.3 ± 0.7) 1.8‑2.6 (2.3 ± 0.2) 1.5‑1.9 (1.8 ± 0.2) 2.2‑3.1 (2.6 ± 0.2) 1.9‑2.1 (2.0 ± 0.1) 1.7‑2.0 (1.8 ± 0.1) 1.1‑1.6 (1.3 ± 0.3) 1.6‑2.2 (1.9 ± 0.2) 1.4‑1.6 (1.5 ± 0.1) 1.5‑2.2 (1.9 ± 0.2) 1.3‑1.8 (1.5 ± 0.2) 0.31‑0.39 0.32‑0.39 0.38‑0.44 0.33‑0.46 0.32‑0.40 0.35‑0.42 0.34‑0.40 0.32‑0.37 0.96‑1.15 0.87‑0.97 0.73‑0.95 0.74‑0.95 0.58‑0.77 0.52‑0.84

Description of holotype – Head narrower than body, about as long as wide; HW32.8% of SVL; HL 32.4% of SVL; snout short, acutely rounded in dorsal and lateral views (Figs. 8A, B), ED larger than E‑N; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis slightly curved in dorsal view, rounded in profile; loreal region slightly concave; lips rounded; EW without enlarged tubercles; EW narrower than IOD (EW 75.0% of IOD); supratympanic fold short, narrow; tympanic membrane and tympanic annulus absent, postrictal tubercles coalescing in two short, prominent ridges on each side of head. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers absent; tongue 2.5x as long as wide, not notched posteriorly, posterior one third free. Skin on dorsum shagreen, narrow, slightly elevated dorsolateral fold extending from posterior margin of upper eyelid to sacral region, posteriorly discontinuous; skin on flanks slightly tuberculate; venter areolate; discoidal fold absent, thoracic fold present; cloacal sheath short; large tubercles absent in cloacal region. Outer surface of forearm with minute tubercles; palmar tubercles low, outer palmar ovoid, approximately 2x the size of elongate, inner palmar tubercle; few supernumerary tubercles, about one third size of subarticular tubercles; subarticular tubercles prominent, ovoid in dorsal view, rounded in lateral view, most prominent on base of fingers; fingers with lateral fringes; Finger I shorter than Finger II; tips of digits rounded (Fig. 8C).

B. zonalis Females (n = 3) Males (n = 3) 22.2‑24.4 (23.3 ± 1.1) 14.8‑17.6 (16.0 ± 1.4) 8.7‑9.5 (9.0 ± 0.4) 6.5‑7.6 (7.1 ± 0.6) 9.6‑9.9 (9.7 ± 0.2) 6.9‑8.9 (7.8 ± 1.0) 7.9‑8.3 (8.0 ± 0.2) 5.5‑6.8 (6.2 ± 0.7) 7.5‑8.0 (7.8 ± 0.3) 5.2‑6.7 (5.9 ± 0.8) 2.2‑2.3 (2.3 ± 0.1) 1.6‑1.8 (1.7 ± 0.1) 2.7‑2.8 (2.8 ± 0.1) 2.3‑2.4 (2.3 ± 0.1) 2.1 1.2‑1.4 (1.3 ± 0.1) 1.7‑2.2 (1.9 ± 0.3) 1.3‑1.7 (1.5 ± 0.2) 1.8‑2.0 (1.9 ± 0.1) 1.4‑1.8 (1.7 ± 0.2) 0.38‑0.40 0.43‑0.45 0.39‑0.45 0.47‑0.51 0.32‑0.37 0.37‑0.39 0.32‑0.35 0.35‑0.38 0.94‑1.01 0.94‑0.99 0.82‑0.87 0.88‑1.06 0.75‑0.78 0.52‑0.61

Hind limbs short, slender, TL 38.9% of SVL; FL 39.3% of SVL; upper surface of hind limbs shagreen with small, scattered tubercles; posterior and ventral surfaces of thighs areolate; heel without enlarged tubercles; outer surface of tarsus with minute tubercles; metatarsal tubercles elevated, slightly conical in lateral view, inner metatarsal tubercle elongate, about twice the size of rounded outer metatarsal tubercle; plantar supernumerary tubercles indistinct; subarticular tubercles most prominent on base of toes, low, ovoid in dorsal view, rounded in lateral view; toes with lateral fringes; basal webbing present; toe tips rounded, slightly pointed due to preservation, lacking marginal grooves, about as large as those on fingers; relative lengths of toes: 1 < 2 < 3 < 5 < 4; Toe V longer than Toe III (Fig. 8D). Measurements of holotype (in mm) – SVL 24.4; TL 9.5; FL 9.6; HL 7.9; HW 8.0; ED 2.3; IOD 2.8; EW 2.1; IND 2.2; E‑N 2.0. Color of holotype in life (Fig. 7) – Dorsum pale cinnamon with small dark brown flecks; canthal and supratympanic stripes ill defined, gray; margin of upper and lower lips dark gray; throat mottled cream and pale gray; chest, ventral surfaces of arms and thighs pale gray with purpleish gray mottling; belly, groin, concealed surfaces of shanks, and dorsal surface of tarsus dark gray with white flecks; fingers and toes partly reddish brown, otherwise dark gray; iris gold

Lehr, E. and Catenazzi, A.

with fine black reticulations and a horizontal reddish brown streak through pupil. Color of holotype in preservative – Dorsum gray with small dark gray flecks; throat and chest mottled cream and gray; ventral surfaces of hands and feet mottled cream and dark gray; iris mottled dark and pale gray; otherwise as described below. Variation – The dorsal color in females is more uniform than in males, varying from pale cinnamon to pale grayish tan to pale gray. One male (MUSM



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27574) has the dorsum mottled dark grayish brown and reddish brown, postrictal ridges cream, and venter mottled dark grayish brown, pale gray, and reddish brown. Another male (MTD 46870) has the dorsum mottled pale gray and reddish brown, the flanks pale gray, and the venter mottled blueish gray and reddish brown. One juvenile (MUSM 27575) has a tan dorsal band, dark gray dorsolateral folds, grayish tan flanks, and the venter mottled blueish gray and reddish brown. Another juvenile (MUSM 27861) has the dorsum and flanks mottled pale reddish brown and pale gray with dark brown blotches; dark brown bars on extremities; dark brown canthal and supratympanic stripes, a dark brown labial bar below eye, and tan postrictal ridges. Only females have a dark gray to black belly with white flecks. Females are larger than males and have more continuous, narrower, and less elevated dorsolateral folds. Males have more tuberculate flanks than females. The smallest juvenile is 11.5 mm SVL (MUSM 27861). Table 3 shows ranges and proportions of the type series. Distribution – Bryophryne zonalis is only known from the upper Marcapata valley, at elevations between 3129 and 3285  m along the road from Abra Huallahualla to Quincemil (Fig. 4). Etymology – The specific name zonalis is derived from the Latin noun “zona” meaning girdle or belt. The name refers to the contrasting pattern consisting of black with white flecks on the belly in females. Ecological Results

Figure 7. Holotype of Bryophryne zonalis in life (MUSM 27570, female) in lateral (A), dorsal (B), and ventral (C) views. Photos by A. Catenazzi.

All specimens of Bryophryne gymnotis occurred along a transect of ~400 x 2 m. Four people actively searched this transect for ground-dwelling anurans for 3  h. Frogs were found in damp soil under logs, moss, and rocks and in leaf litter. In some cases, up to three frogs were found under the same log. This species seems to have a patchy distribution, because no frogs were found in the first km of walking along a trail from San Luis to the type locality, followed by a high density of frogs for 400 m, and a subsequent drop in density above 3350 m. We found no sympatric anurans during our visit and during a nocturnal survey in San Luis, but Chaparro et al. (2007) reported Nannophryne corynetes, Gastrotheca excubitor, Pleurodema marmoratum, and Pristimantis rhabdol‑ aemus sympatric with B. bustamantei. In our survey at the nearby locality of Alfamayo (2490  m), we

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observed P.  rhabdolaemus and Gastrotheca ochoai, whereas at Abra de Málaga we found B. bustamantei and G. excubitor. Bryophryne hanssaueri inhabits leaf litter at the transition of montane forest with the high-Andean grassland or puna. Cano et  al. (1995) discuss vegetation of the area and Lehr and Catenazzi (2008) list the most common plant species. The elevational range of this species and relative density based on 10 x 10 m² leaf litter quadrats has been illustrated by Lehr and Catenazzi (2009, Bryophryne sp. in Fig. 4). Bryophryne hanssaueri seems to be a rare species and was not discovered until the rainy season of 2008, despite intensive sampling between 1996 and 1998 and in the dry season of 2007. However, we found 12 individuals and a clutch in a single 10 x10 m2 quadrat plot at 3415 m in the rainy season of 2009, suggesting that this species can be locally abundant. The clutch contained 19 eggs ranging between 4.2 and 4.8 mm in diameter and that were close to hatching. We found the clutch unattended under mosses, and moved it to the field station until hatching occurred. Hatchlings measured 4.9‑5.2 mm in snout-vent length (n = 8). The elevational range overlaps with that of

B. cophites, B. nubilosus, Psychrophrynella usurpa‑ tor, Gastrotheca excubitor, Gastrotheca marsupiata, Telmatobius timens and an undescribed species of Telmatobius. Specimens of Bryophryne zonalis were found under rocks and moss in fragments of elfin and montane cloud forests. Much of the landscape of the upper Marcapata valley has been modified through deforestation, cattle grazing, and cultivation; remnants of the original forest habitats can be found along streams and in areas of difficult access. In addition to severe habitat disturbance, the pathogenic fungus Batra‑ chochytrium dendrobatidis occurs this area (Seimon et al., 2006) and has been detected (pers. comm. A. Catenazzi) in one of the types of B. zonalis (MUSM 27861). Discussion The genus Bryophryne contains six species restricted to the Cusco Region in southern Peru. Previously, one of the defining characters for Bryophryne was the absence of a tympanum, which was

Figure 8. Dorsal (A) and lateral (B) views of head and ventral views of right hand (C) and left foot (D) of Bryophryne zonalis (MUSM 27570). Drawings by E. Lehr.

Lehr, E. and Catenazzi, A.

considered a synapomorphy. Bryophryne gymnotis is the first species of the genus with a tympanic ������������� membrane and a tympanic annulus, thus altering the ��������� definition of the genus provided by Hedges et al. (2008), as follows: …(2) ������������������������������� tympanic membrane, tympanic annulus, columella, and cavum tympanicum are present or absent. Even though the phylogenetic relationships among species of Bryophryne are unknown, we are confident of the generic assignment for B. gymnotis because of the overall similarity with other members of the genus. We recognize a convergence in the state of the tympanum in Bryophryne and Phrynopus. Both genera have high local species diversity and occur at high elevations, and the majority of the species lack a tympanum. Bryophryne hanssaueri is sympatric with both B. nubilosus and B. cophites in the upper Cosñipata valley, Manu National Park. This locality has been intensively sampled over the past 12 years (Lehr and Catenazzi, 2008, 2009; Catenazzi and Rodriguez, 2001). In the upper Umasbamba valley (near Abra de Málaga), 80 km west of the upper Cosñipata valley, we found B. gymnotis approx. 5 km from the closest collecting site of B. bustamantei. These two species might be sympatric, but further field research is needed to establish the elevational ranges of both species. In the case of B.  zonalis collected from the Marcapata valley (80 km southeast of the upper Cosñipata valley), a currently undescribed species (identified as B. cophites in the KU catalogue, KU196596‑7, herein referred to as Bryophryne sp. A) might be sympatric with B.  zonalis. Our own collections of this undescribed species are limited to high elevations in the high-Andean grassland, whereas B. zonalis was collected in fragments of montane cloud forest and elfin forest. In the three valleys (Umasbamba, Cosñipata, and Marcapata), only one species of Bryophryne seems to inhabit the high-Andean grassland: B. bustamantei in Umasbamba, B. cophites in Cosñipata, and B. sp. A in Marcapata. One to two additional species live in the elfin and montane forests immediately adjacent to the grasslands, usually around 3000‑3400 m but down to 2300  m in the case of B.  nubilosus in Cosñipata: B. gymnotis in Umasbamba, B. hanssau‑ eri and B. nubilosus in Cosñipata, and B. zonalis in Marcapata. Interestingly, both species (B. bustaman‑ tei, B.  gymnotis) from Umasbamba produce vocalizations and males have vocal slits and vocal sacs, whereas none of the Bryophryne species in the other watersheds is known to produce any call. Chaparro et al. (2007) described the call of B. bustamantei as



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a ‘short whistle’ produced during the day in April, but they did not provide the spectrogram and oscillogram of the call. The description of three new species of Bryophryne and the high endemism of Andean frogs (Duellman, 1999) suggest that many more Bryophryne species remain to be discovered from other watersheds in southern Peru. Resúmen Describimos tres nuevas especies de Bryophryne de la Región de Cusco en el sur de Perú, incrementando a seis el numero de especies conocidas en el género. Una de las nuevas especies se diferencia de todos los demás Bryophryne por la presencia de annulus y membrana timpánicos. Los machos de esta especie tienen un saco y aberturas vocales y producen vocalizaciones que describimos en este artículo. Esta especie ocurre en San Luis, un bosque nublado a elevaciones entre 3272 y 3354  m en la carretera entre el Abra Málaga y Quillabamba. La segunda especie se caracteriza por tener garganta e ingles anaranjadas y ha sido encontrada en la parte alta del Parque Nacional del Manu (elevación 3266‑3430 m), en la trocha Ericsson entre Acjanaco y Pillahuata y a lo largo de la carretera Paucartambo-Pilcopata cerca de Abra Acjanaco. La tercera especie tiene garganta y pecho gris claros y gris oscuro moteado, mientras que el vientre es negro con manchas blancas. Este Bryophryne se conoce únicamente de la parte alta del Valle de Marcapata a lo largo de la carretera entre Abra Huallahualla y Quincemil a elevaciones entre 3129 y 3285  m. Incluimos observaciones sobre la ecología de cada especie y un mapa con las localidades tipo de todas las especies conocidas de Bryophryne. Acknowledgments We thank an anonymous reviewer for his helpful comments and suggestions. Specimens were loaned by J. Córdova (MUSM). AC was assisted in the field by J. Carrillo, D. Cruz, I. Chinipa, J. C. Jahuanchi, E. Luna, A. Machaca, and W. Qertehuari. AC thanks the staff of the Amazon Conservation Association in Cusco and Wayqecha for field and logistic support; the National Institute for Natural Resources in Lima for research, collecting and export permits; the administration of Manu National Park in Cusco for research permit and logistic support. Fieldwork was funded by grants from the Amazon Conservation Association, the Chicago Board of Trade Endangered Species Fund, the Rufford Small Grants Foundation and the Fondation Matthey-Dupraz to AC and by an Amphibian Specialist Group Award to AC and EL. AC was supported by a Post-doctoral fellowship from the

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Swiss National Science Foundation (116305). EL thanks the Humboldt-Foundation for an alumni grant to conduct research at the Natural History Museum and Biodiversity Research Center, The University of Kansas, USA.

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Duellman, W. E., E. Lehr, and P. Venegas. 2006. Two new species of Eleutherodactylus (Anura: Leptodactylidae) from northern Peru. Zootaxa, 1285:51‑64. Hedges, S. B., W. E. Duellman, and M. P. Heinicke. 2008. New World direct developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737:1‑182. Lehr, E. and A. Catenazzi. 2008. A new species of Bryophryne (Amphibia: Strabomantidae) from southern Peru. Zootaxa, 1784:1‑10. Lehr, E. and A. Catenazzi. 2009. A new species of minute Noblella (Anura: Strabomantidae) from southern Peru: the smallest frog of the Andes. Copeia, 2009:148‑156. Lynch, J. D. 1975. A review of the Andean leptodactylid frog genus Phrynopus. Occasional Papers of the Museum of Natural History, The University Kansas, 35:1‑51. Lynch, J. D. and W. E. Duellman. 1997. Frogs of the genus Eleutherodactylus in western Ecuador. Systematics, ecology, and biogeography. The University of Kansas Special Publication, 23:1‑236. Seimon, T. A., A. Seimon, P. Daszak, S. R. P. Halloy, L. M. Schloegel, C. A. Aguilar, P. Sowell, A. D. Hyatt, B. Konecky, and J. E. Simmons. 2006. Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology, 12:1‑12. Submitted 13 January 2009 Accepted 09 April 2009

Appendix I Bryophryne bustamantei – PERU: Cusco: Provincia La Convención: Abra de Málaga: MUSM 24537‑38. Bryophryne cophites – PERU: Cusco: Provincia de Paucartambo: Distrito Cosñipata: S slope Abra Acanaco, 14 km NNE Paucartambo, 3400 m: KU 138884 (holotype); N slope Abra Acanaco, 27 km NNE Paucartambo, 3450  m: KU 138885‑908, 138911‑5 (all paratypes); 2  km NE of Abra Acanaco, 13°11.367’S, 71°36.223’W, 3280 m: MHNG 2698.24, Tres Cruces, 8.5 km N of Abra Acanaco, 13°07’18.3”S, 71°36’37.8”, 3590 m: MUSM 26283, 26267. Bryophryne hanssaueri – PERU: Cusco: Provincia de Paucartambo: Distrito Cosñipata: Acjanaco, Manu National Park: 1 km south of the type locality, 13°11’30.0”S, 71°37’16.1”W, 3355 m: MUSM 27940; 900 m south of the type locality, 13°11’27.4”S, 71°37’15.2”W, 3390 m: MUSM 27941‑2; 1.9 km NW of the type locality, 13°10’07.9”S, 71°37’49.2”W, 3414 m: MUSM 27943‑54. Bryophryne nubilosus – PERU: Cusco: Provincia de Paucartambo: Distrito de Cosñipata, 500 m NE of Esperanza, 2712 m: MUSM 26310 (holotype), MUSM 26311; near the type locality, 13°11’33.21”S, 71°35’25.17”W, 3065 m: MTD 47294; near Hito Pillahuata, 2600 m: MUSM 20970; Quebrada Toqoruyoc, 3097 m: MUSM 26312, MTD 47293; Esperanza, 2800 m: MHNSM 26316‑17; 13°11’20.2”S, 71°35’07.3”W, 2900 m: MUSM 24539‑40. Bryophryne sp. A – PERU: Cusco: Provincia de Quispicanchis: Distrito de Marcapata: Coline, 3672 m: MUSM 27571, 27573.