Pristimantis attenboroughi, Lehr, Edgar & May, Rudolf von, 2017

Lehr, Edgar & May, Rudolf von, 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, pp. 17-42 : 21-31

Pristimantis attenboroughi sp. n.

Common name.

English: Attenborough’s Rubber Frog. Spanish: Rana cutín Attenborough.

Holotype. MUSM 31196 (IWU 178, Figs 3, 4), adult male from the Pui Pui Protected Forest, Provincia Satipo, Región Junín, Peru, Upper part of Quebrada Tarhuish, "Laguna Udrecocha", Puna, open area on east side of Laguna Udrecocha, 11°23'24.1"S, 74°58'32.5"W, 3936 m a.s.l. (Fig. 8A), collected on 17 May 2012 by E. Lehr and R. von May.

Paratypes. A total of 33 (Figs 5-7, 8C), all from inside the PPPF (except for: MUSM 31199-31202, NMP6V 75526-29), Provincia Satipo, Región Junín: 10 adult females (MUSM 31977, 31980, 31987, 31201, NMP6V 75076, 75522 [GenBank accession numbers KY594753, KY594761], 75523, 75528 [GenBank accession numbers KY594756, KY594764], 75529 [GenBank accession number KY594757], 75534), 20 adult males (MUSM 31186 [GenBank accession number KY594752], 31195, 31199, 31202, 31975, 31979, 31988, 31989, 31992, 31993, NMP6V 75077-75079, 75524 [GenBank accession numbers KY594754, KY594762], 75525 [GenBank accession numbers KY594755, KY594763], 75526, 75527, 75533, UMMZ 244726, 244727), 3 juveniles (MUSM 31187, 31990, 31200).

MUSM 31186, MUSM 31187, NMP6V 75522, 75523: Quebrada Tarhuish, left bank of Antuyo River, “Shiusha”, upper montane forest, 11°22'3.9"S, 74°56'12.7"W, 3414 m a.s.l. collected on 12 May 2012 by E. Lehr and R. von May. MUSM 31195, NMP6V 75524, 75524: collected at the type locality along with the holotype. MUSM 31199, 31200, MUSM 31201, 31202, NMP6V 75526, 75527: Upper part of Quebrada Tasta, "Laguna Luichococha", Puna, 11°27'23.7"S, 74°55'10.6"W, 3708 m a.s.l. collected on 20 May 2012 by E. Lehr and R. von May. NMP6V 75528, 75529: near trail from Tasta to Tarhuish (first mountain peak), Polylepis forest patch, 11°26'8.6"S, 74°53'56.5"W, 3886 m a.s.l. collected on 20 May 2012 by E. Lehr and R. von May. MUSM 31975: Antuyo, 11°20'03.7"S, 74°59'49.1"W, 3700 m a.s.l. collected on 27 June 2013 by E. Lehr, J. Moravec, and J.C. Cusi. MUSM 31977, 31979, MUSM 31980, NMP6V 75076, UMMZ 244726: Hatunpata, 11°18'07.9"S, 75°01'35.0"W, 3710 m a.s.l. collected on 28 June 2013 by by E. Lehr, J. Moravec, and J.C. Cusi. MUSM 31987-31990, NMP6V 75077, 75078, 75533, UMMZ 244727: Trancapampa, 11°17'49.2"S, 75°00'46.3"W, 3550 m a.s.l. collected on 2 July 2013 by E. Lehr, J. Moravec, and J.C. Cusi. MUSM 31992, 31993, NMP6V 75079, 75534: Antuyo Bajo, 11°18'53.4"S, 74°59'34.8"W, 3400 m a.s.l. collected on 4 July 2013 by E. Lehr, J. Moravec, and J.C. Cusi.

Generic placement.

We assign this species to Pristimantis based on our molecular data (Fig. 2).

Diagnosis. A new species of Pristimantis assigned to the danae species Group having the following combination of characters: (1) Skin on dorsum shagreen with low scattered tubercles, skin on flanks tuberculate, skin on venter areolate; discoidal fold absent, thoracic fold present; irregularly shaped, discontinuous dorsolateral folds present; (2) tympanic membrane and tympanic annulus absent; (3) snout short, rounded in dorsal and in lateral views; (4) upper eyelid without enlarged conical tubercles; EW shorter than IOD; cranial crests absent; (5) dentigerous processes of vomers present; (6) males without vocal slits, nuptial pads absent; (7) Finger I shorter than Finger II; tips of digits narrow, rounded, lacking circumferential grooves; (8) fingers without lateral fringes; (9) small conical ulnar and tarsal tubercles present; (10) heel with a small conical tubercle; inner tarsal fold usually absent; (11) inner metatarsal tubercle ovoid, 1.5 times as large as outer; outer metatarsal tubercle small, rounded; vie low supernumerary plantar tubercles; (12) toes without lateral fringes; basal toe webbing absent; Toe V longer than Toe III; tips of digits narrow, rounded, lacking circumferential grooves, toe tips slightly smaller than those on fingers; (13) in life, dorsal ground coloration pale or dark gray, reddish brown or brownish olive with dark gray scattered flecks, some with X-shaped mark on scapular and ill-defined diagonal bars on flanks; dark grayish-brown canthal and supratympanic stripes usually present; groin dark gray or pale reddish brown with a pale red to pink tint in some; venter dark gray, pale gray, grayish brown or pale grayish green and in some dark gray mottled; iris pale grayish green with fine black vermiculation and brownish-orange horizontal streak across pupil and lower half of iris; (14) SVL in adult males 14.6-19.2 mm (n = 21), in adult females 19.2-23.0 mm (n = 10).

Comparisons. Pristimantis attenboroughi is readily distinguished from its congeners in Ecuador (176 species, AmphibiaWeb 2016), Peru (128 species, AmphibiaWeb 2016), and Bolivia (17 species, AmphibiaWeb 2016) by having narrow digits without circumferential grooves, by lacking a tympanic annulus and tympanic membrane, and by having irregularly shaped, discontinuous dorsolateral folds. In Peru 18 species of Pristimantis lack a tympanum; these are Pristimantis academicus Lehr, Moravec, and Gagliardi Urrutia, 2010, Pristimantis altamazonicus (Barbour and Dunn, 1921), Pristimantis ashaninka Lehr and Moravec, 2017, Pristimantis colodactylus (Lynch, 1979), Pristimantis coronatus Lehr and Duellman, 2007a, Pristimantis croceoinguinis (Lynch, 1968), Pristimantis cruciocularis (Lehr, Lundberg, Aguilar, and von May, 2006), Pristimantis flavobracatus (Lehr, Lundberg, Aguilar, and von May, 2006), Pristimantis imitatrix (Duellman, 1978b), Pristimantis lirellus (Dwyer, 1995), Pristimantis leucorrhinus Boano, Mazzotti, and Sindaco, 2008, Pristimantis martiae (Lynch, 1974), Pristimantis minutulus Duellman and Hedges, 2007, Pristimantis rhabdocnemus (Duellman and Hedges, 2005), Pristimantis simonsii (Boulenger, 1900), Pristimantis tantanti (Lehr, Torres-Gastello, and Suárez-Segovia, 2007), Pristimantis ventrimarmoratus (Boulenger, 1912), and Pristimantis vilcabambae Lehr, 2007. Of these, only Pristimantis simonsii from northern Peru has narrow digits without circumferential grooves. Pristimantis attenboroughi and Pristimantis simonsii lack circumferential grooves and a tympanum, and both have dorsolateral folds, but Pristimantis attenboroughi is smaller than Pristimantis simonsii (female SVL 26.2-33.3 mm in Pristimantis simonsii ), and male Pristimantis attenboroughi lack nuptial pads which are present in Pristimantis simonsii .

Members of the Pristimantis orestes species Group are terrestrial and inhabit high elevations in southern Ecuador and in Peru (Duellman and Lehr, 2009) and have narrow digits, and only one of the 17 species ( Guayasamin and Artega 2013) lacks circumferential grooves ( Pristimantis simonsii ), and only two ( Pristimantis seorsus, Pristimantis simonsii ) lack a tympanum. Furthermore Pristimantis attenboroughi is phylogenetically distant from members of this group which is considered to be not monophyletic ( Duellman and Lehr 2009, Fig. 2).

Among the three other new species of Pristimantis from the upper montane forests and Puna of the PPPF, only Pristimantis sp. n. E lacks circumferential grooves and a tympanum. However, Pristimantis attenboroughi and Pristimantis sp. n. E both differ regarding other morphological traits, coloration, and genetically.

Pristimantis attenboroughi shares with Pristimantis stipa Venegas and Duellman, 2012 from the Puna of northern Peru ( Venegas and Duellman 2012) narrow digits without circumferential grooves and dorsolateral folds. However, Pristimantis attenboroughi is smaller (female SVL 19.2-23.0 mm [n = 10] vs. 35.1 mm [n = 1]), lacks a tympanum (present in Pristimantis stipa ), and has ulnar tubercles not coalesced into fold (coalesced into low fold in Pristimantis stipa ), Venegas and Duellman (2012).

The new species shares narrow digits without circumferential grooves and the absence of a tympanic annulus and tympanic membrane with the Andean genera Phrynopus Peters, 1873 (except for Phrynopus auriculatus Duellman and Hedges, 2008, and Phrynopus peruanus Peters, 1873), 28 species from elevations between 2200 and 4400 m a.s.l. in central and northern Peru, Duellman and Lehr, 2009) and Bryophryne Hedges, Duellman, and Heinicke, 2008 (8 species from elevations between 2900 and 4120 m a.s.l. in southern Peru, Duellman and Lehr 2009), AmphibiaWeb (2016). Pristimantis attenboroughi is most similar with Phrynopus chaparroi Mamani and Malqui, 2014 which was described based on morphological characters and found at elevations between 4205 and 4490 m a.s.l. in southern Región Junín ( Mamani and Malqui 2014). Both Pristimantis attenboroughi and Phrynopus chaparroi lack a tympanum and have narrow digits without circumferential grooves. However, Pristimantis attenboroughi is smaller than Phrynopus chaparroi (female SVL 19.2-23.0 mm [n = 10] vs. 30.0-32.2 [n = 4]), lacks protuberant subconical postrictal tubercles (present in Phrynopus chaparroi ), has dorsolateral folds (absent in Phrynopus chaparroi ), dentigerous processes of vomers present (absent in Phrynopus chaparroi ), and males lack nuptial pads (present in Phrynopus chaparroi ). Phrynopus chaparroi might belong to Pristimantis , but molecular characters need to be applied to confirm our suspicion.

Description of the holotype.

Head about as long as wide; head length 39.7% of SVL; head width 38.6% of SVL; cranial crests absent; snout short, rounded in dorsal view, rounded in lateral view (Fig. 3A, B); eye-nostril distance 70% of eye diameter; nostrils slightly protuberant, directed dorsolaterally; canthus rostralis short, rounded in lateral view, weakly concave in dorsal view; loreal region concave; lips rounded; outer margin of upper eyelid each with few slightly enlarged conical tubercles; upper eyelid width 51.9% of IOD (see photo in life Fig. 3); supratympanic fold short and broad, extending from posterior margin of upper eyelid slightly curved to insertion of arm; tympanic membrane and annulus absent; distinct conical postrictal tubercles present bilaterally. Choanae small, ovoid, not concealed by palatal shelf of maxilla; dentigerous processes of vomers positioned posterior to level of choanae, oblique, narrowly separated; tongue long, oval, about three times as long as wide, not notched posteriorly, posterior half free.

Skin on dorsum shagreen with low scattered tubercles, skin on flanks tuberculate, irregularly shaped, discontinuous dorsolateral folds present extending from posterior level of tympanic area to level of hind limb insertion; skin on throat, chest, and belly areolate; discoidal fold absent, thoracic fold present; cloacal sheath short.

Outer ulnar surface each with a row of four minute low tubercles; palmar tubercle bifid; thenar tubercle ovoid; subarticular tubercles well defined, most prominent on base of fingers, round in ventral view, subconical in lateral view; supernumerary tubercles indistinct; fingers short and stout lacking lateral fringes, Finger I shorter than Finger II; tips of digits of fingers narrow, round, lacking circumferential grooves (Fig. 4A).

Hind limbs short, slender, tibia length 40.2% of SVL; foot length 41.3% of SVL; dorsal surfaces of hind limbs tuberculate; inner surface of thighs smooth, posterior surfaces of thighs tuberculate, ventral surfaces of thighs areolate; heels each with a small conical tubercle; outer surface of tarsus with few scattered minute low tubercles; inner tarsal fold absent, but small tubercle proximal to metatarsal tubercle; inner metatarsal tubercle ovoid, one and a half times the size of round outer metatarsal tubercle; subarticular tubercles well defined, round in ventral view, subconical in lateral view; few plantar supernumerary tubercles, about one third the size of subarticular tubercles; toes without lateral fringes; basal webbing absent; tips of digits narrow, round, less expanded than those on fingers, lacking circumferential grooves; relative length of toes: 1<2<5<3<4; Toe V slightly longer than Toe III (tip of digit of Toe III and Toe V not reaching distal subarticular tubercle on Toe IV; Fig. 4B).

Measurements (in mm) of the holotype.

SVL 18.9; tibia length 7.6; foot length 7.8; head length 7.5; head width 7.3; eye diameter 2.0; inter orbital distance 2.7; upper eyelid width 1.4; internarial distance 1.9; eye–nostril distance 1.4.

Coloration of the holotype in life

(Fig. 3). The dorsal ground coloration is pale reddish brown with few dark brown flecks; narrow dark brown canthal and supratympanic stripes; flanks pale reddish brown with dark brown flecks forming irregularly shaped diagonal bars; groin and anterior surfaces of thighs reddish brown with dark brown flecks and pale reddish tint; chest, belly, and ventral surfaces of thighs dark grayish brown, throat pale reddish brown and pale gray mottled; palmar and plantar surfaces, and fingers and toes dark grayish brown; iris pale grayish green with fine black vermiculation and brownish-orange horizontal streak across pupil and lower half of iris.

Coloration of the holotype in preservative.

The dorsal ground coloration is pale brown with few dark brown flecks; narrow dark brown canthal and supratympanic stripes; flanks pale brown with many dark brown flecks forming irregularly shaped diagonal bars; groin and anterior surfaces of thighs brown with dark brown flecks; chest, belly, and ventral surfaces of thighs dark brown, throat pale brown and pale gray mottled; palmar and plantar surfaces, and fingers and toes dark brown; iris pale gray.

Variation. All paratypes (Figs 5-7) are similar to the holotype regarding morphology and proportions (Tables 3, 4). Besides differences in SVL, notable morphological variation includes prominence of dorsolateral folds (e.g., prominent dorsolateral folds in MUSM 31192, 31195, Fig. 5 D–F, G–I; weak dorsolateral folds in MUSM 31186, 31975, 31977, NMP6V 75522, 75528, 75529, Fig. 6 G–I), and coarseness of tuberculate skin texture on flanks and hind limbs (skin coarsely tuberculate in MUSM 31186, 31192, 31195, NMP6V 75525, Fig. 5; skin weakly tubercular MUSM 31987, 31997, NMP6V 75528, 75529). Two specimens (NMP6V 75529, 75534) have a tubercle-like inner tarsal fold present. Pristimantis attenboroughi demonstrates a remarkable polymorphism in coloration (Figs 5-7).

The dorsal coloration ranges from pale gray (MUSM 31987, NMP6V 75533, Fig. 6 D–F), dark gray (MSUM 31186, 3199, NMP6V 75522, 75523, 75528, 75529, Fig. 6 A–C), reddish brown (MUSM 31195, 31975, NMP6V 75525, Figs 5 D–F) to brownish olive (MUSM 31992, 31997, Figs 5 G–I, 6 G–I) with dark gray scattered flecks. Some have an X-shaped mark on scapular (MUSM 31200, 31975, 31990), some ill-defined diagonal bars on the flanks (MUSM 31195). Dark grayish-brown canthal and supratympanic stripes are usually present except for dark gray specimens (MSUM 31186, 3199, NMP6V 75522, 75523, 75528, 75529). The groin is dark gray (MSUM 31186, 3199, NMP6V 75522, 75523, 75528, 75529) or pale reddish brown with a pale red to pink tint in some specimens (MUSM 31195, 31196). The venter is dark gray (NMP6V 75522, 75523, 75528, 75529, Fig. 6C), pale gray (MUSM 31987, Fig. 6F), grayish brown (MUSM 31186, 31195, NMP6V 75525, Fig. 5C, F) or pale grayish green and gray mottled (MUSM 31197, Fig. 6I) or dark gray and pale gray mottled (MUSM 31199, 31975, 31992, NMP6V 75533, Fig. 5I).

Juveniles (MUSM 31187, 31990, 31200, Fig. 7) have a paler coloration (yellowish to reddish brown) with contrasting dark brown flecks and distinct canthal and supratympanic stripes. All have the iris pale grayish green with fine black vermiculation and brownish-orange horizontal streak across pupil and lower half of iris, and usually a narrow vertical dark gray streak from pupil through middle of lower iris.

Etymology.

We dedicate this species to Sir David Frederick Attenborough in honor for his educational documentaries on wildlife, especially on amphibians (e.g., Life in Cold Blood, Fabulous Frogs), and for raising awareness about the importance of wildlife conservation. The specific epithet is used as noun in apposition.

Distribution, natural history, and conservation status.

Pristimantis attenboroughi is known from six localities inside the PPPF (Puna of Quebrada Tarhuish at Laguna Udrecocha, Fig. 8A; upper montane forest of Quebrada Tarhuish on the left bank “Shiusha” of Antuyo River; Antuyo; Antuyo Bajo; Hatunpata, and Trancapampa, Figs 8B, 9) and from two outside the PPPF (upper part of Quebrada Tasta close to Laguna Luichococha; in Polylepis forest of first mountain peak next to trail from Tasta to Tarhuish), and is distributed at elevations between 3400 and 3936 m a.s.l., Fig. 9. The type locality (Figs 8A, 9), upper part of Quebrada Tarhuish, on the east side of Laguna Udrecocha at 3936 m a.s.l., belongs to the Puna ecoregion ( Brack 1986). The vegetation consists of Peruvian feather grass ( Stipa ichu ), mosses, and small bushes. The holotype was found inside moss in the afternoon on 17 May 2012. No sympatric anurans were found at the type locality. At the upper montane forest of Quebrada Tarhuish on the left bank “Shiusha” of Antuyo River, Pristimantis attenboroughi was found deep inside large moss layers. Sympatric anurans are Gastrotheca griswoldi (MUSM 31193), Pristimantis sp. n. C (MUSM 31190-92), Pristimantis sp. n. D (MUSM 31197-98), and Phrynopus sp. n. A (MUSM 31203).

A female Pristimantis attenboroughi (MUSM 31980, Fig. 8C) guarding 20 eggs was found at Hatunpata inside moss, 3710 m a.s.l., on 28 June 2013. The eggs were pale cream colored and had an average diameter of 3.5 ± 0.1 mm (3.3-3.6 mm, n = 20).

The IUCN Red List criteria ( IUCN 2001) consider that if a species occurs in fewer than 10 threat-defined locations and the extent of occurrence (EOO) is <20,000 km2, it should be classified as Vulnerable or Endangered. Pristimantis attenboroughi is known from seven localities distributed in the PPPF and its buffer zone (Fig. 9), with an estimated EOO of 66.54 km2. As such, this new species might be classified as Vulnerable if we take into account these criteria. However, given that the PPPF may host a greater number of locations and most of them are inside the protected area, we propose that Pristimantis attenboroughi should likely be categorized as Near Threatened (NT).

Given that the known distribution of Pristimantis attenboroughi overlaps with the PPPF, a substantial portion of the habitat of this species is formally protected. However, other factors such as fungal infections, climate change, pollution, and man-made fires (used to expand grazing areas for livestock) continue to be threats for many Andean amphibians even inside protected areas ( Catenazzi and von May 2014).