Pristimantis pluvialis, Shepack, Alexander, von May, Rudolf, Ttito, Alex & Catenazzi, Alessandro, 2016

Shepack, Alexander, von May, Rudolf, Ttito, Alex & Catenazzi, Alessandro, 2016, A new species of Pristimantis (Amphibia, Anura, Craugastoridae) from the foothills of the Andes in Manu National Park, southeastern Peru, ZooKeys 594, pp. 143-164 : 146-155

Taxon classification Animalia Anura Craugastoridae

Pristimantis pluvialis sp. n.

Holotype

(Figs 1-3). CORBIDI 16510, an adult male from Quitacalzón, 13°01'31.80"S, 71°30'00.72"W (WGS84),, 1050 m a.s.l., Distrito Kosñipata, Provincia Paucartambo, Región Cusco, Peru, collected by A. Shepack, A. Ttito, and A. Catenazzi on 16 January 2015.

Paratopotypes

(Fig. 4). CORBIDI 16511, an adult female; CORBIDI 16512 and MHNC 15489-90, two adult males, collected by A. Shepack, A. Ttito, and A. Catenazzi on 16 January 2015.

Paratypes

(Fig. 5). Eight adult males, all from Distrito Kosñipata: MUSM 35217 and MHNG 2607.12-13 from Río Entoro, 13°00'45"S; 71°21'44"W (WGS84), 740 m a.s.l., collected on 2 September 1999 by A. Catenazzi and R. von May; CORBIDI 11862 from near Chontachaca, 13°01'33"S, 71°29'03"W (WGS84), 930 m a.s.l., collected by A. Catenazzi on 11 August 2012; CORBIDI 17014-15 from near Chontachaca, 13°01'33"S, 71°29'05"W (WGS84), 940 m a.s.l., collected by A. Catenazzi and A. Ttito on 3 March 2016; CORBIDI 16695 from between Chontachaca and Quitacalzón, 13°01'33"S, 71°29'07"W (WGS84), 950 m a.s.l., collected by A. Catenazzi and A. Ttito on 25 January 2014; MHNG 2607.11 from near Radiochayoc, 13°02'07"S, 71°30'46"W (WGS84), 1110 m a.s.l., collected on 25 February 1999 by A. Catenazzi, J. L. Martínez Ruiz and W. Qertehuari Dariquebe.

Generic placement.

We assign this species to Pristimantis on the basis of general morphological similarity to other members of the genus and molecular data. The genus Pristimantis lacks any diagnostic morphological synapomorphies ( Hedges et al. 2008), but molecular phylogenetic analyses support the placement of the new species within the genus (Fig. 6).

Diagnosis.

A new species of Pristimantis characterized by (1) skin on dorsum smooth, skin on belly areolate, discoidal and dorsolateral folds absent; (2) tympanic membrane differentiated, tympanic annulus distinct; (3) snout moderate in length, with small rostral tubercle, subacuminate in dorsal view and rounded in profile; (4) upper eyelid with minute conical tubercles, narrower than IOD; cranial crests absent; (5) dentigerous process of vomers barely noticeable; (6) vocal slits present; nuptial pads absent; (7) Finger I shorter than Finger II; discs broadly expanded and elliptical; (8) fingers with narrow lateral fringes; (9) single, minute ulnar tubercle present; (10) heel and tarsus lacking tubercles; (11) inner metatarsal tubercle ovoid, of higher relief and about 2.5 times the size of conical, rounded outer metatarsal tubercle; supernumerary plantar tubercles present; (12) toes with narrow lateral fringes; webbing absent; Toe V longer than Toe III; tips of digits expanded, truncate; (13) dorsum beige to reddish-brown with or without dark brown markings; interorbital bar present; venter cream; (14) SVL 21.8-26.9 mm in 12 males, 28.8 mm in one female (Table 1).

Comparisons.

We tentatively assign Pristimantis pluvialis to the putative Pristimantis lacrimosus group sensu Arteaga et al. (2013) because of its smooth dorsal skin, presence of rostral tubercle, subacuminate snout profile, moderately long limbs, Finger I shorter than Finger II, expanded digital disks, and distinct tympanic membrane. Furthermore, our phylogenetic analysis (Fig. 6, Tables 2-3) supports the distinctiveness of Pristimantis pluvialis from other closely related taxa, including Pristimantis bromeliaceus , Pristimantis galdi , Pristimantis cf. mendax , Pristimantis omeviridis , and two undescribed species (Fig. 6). We found substantial genetic distances (uncorrected p-distances of 0.06-0.15 for 16S and 0.23-0.27 for COI; Tables 2-3) between Pristimantis pluvialis and the most closely related species for which mitochondrial sequence data were available. Given our taxon sampling, we emphasize distances for 16S. Pristimantis pluvialis is most closely related to two undescribed Pristimantis , one from near the type locality (CORBIDI 17473, 16S uncorrected p-distance: 0.06), and another from Guyana (ROM 43978, 16S uncorrected p-distance: 0.07). This species was previously identified as Pristimantis zeuctotylus by Hedges et al. (2008), but was treated as Pristimantis sp. by Padial et al. (2014). Other closely related species are Pristimantis moro (16S uncorrected p-distance: 0.08-0.11), Pristimantis schultei (0.10), Pristimantis bromeliaceus (0.11), and Pristimantis mendax (0.11).

The new species differs from most known Peruvian species of Pristimantis by having a rostral tubercle. Fewer than 20 species of Peruvian Pristimantis possess a rostral papilla or tubercle ( Duellman and Lehr 2009): Pristimantis acuminatus , Pristimantis aquilonaris , Pristimantis bromeliaceus , Pristimantis caeruleonotus , Pristimantis cordovae , Pristimantis coronatus , Pristimantis lacrimosus (variable), Pristimantis olivaceus , Pristimantis omeviridis , Pristimantis pardalinus , and Pristimantis proserpens , Pristimantis rhodostichus , and Pristimantis schultei . Pristimantis pluvialis differs from all these species by having smooth dorsal skin and by its larger snout-vent length reaching 24.9 mm in males (except for Pristimantis cordovae , the largest Pristimantis bearing a rostral tubercle, and whose males reach 27.1 mm in SVL).

The two species that superficially most resemble Pristimantis pluvialis are Pristimantis lacrimosus and Pristimantis waoranii . However, Pristimantis pluvialis differs from both species by having a rostral tubercle (absent in Pristimantis waoranii and variable in Pristimantis lacrimosus ), and by its larger size. Furthermore, it differs from Pristimantis lacrimosus by its call with lower dominant frequency (~2500 Hz). Calls of Pristimantis lacrimosus available at AmphibiaWeb Ecuador ( Read 2012; Ron et al. 2016) have higher dominant frequency ranging from 3100-3273 Hz (n = 6). Furthermore, the new species differs from Pristimantis waoranii by having dark bands or markings on the dorsum (absent in Pristimantis waoranii ). Another morphologically similar species, Pristimantis schultei , has an acuminate snout in dorsal view (subacuminate in Pristimantis pluvialis ), skin on dorsum shagreen (generally smooth), and heel and outer edge of tarsus bearing many low tubercles (tubercles absent). Furthermore, Pristimantis schultei occurs in northern Peru at elevations above 2400 m (below 1110 m for Pristimantis pluvialis ), and its advertisement call consists of a double note, “ping-ping” ( Duellman 1990), in contrast with the single, low frequency note produced by Pristimantis pluvialis .

Two species related to Pristimantis lacrimosus , Pristimantis mendax and Pristimantis olivaceus , occur near the type locality of Pristimantis pluvialis in Manu NP and surrounding areas in southern Peru ( Catenazzi et al. 2013; Duellman 1978b; Duellman and Lehr 2009; Köhler et al. 1998). In addition to the characters listed in the previous paragraph, Pristimantis olivaceus further differs from Pristimantis pluvialis by being smaller (17.7-22.1 mm in males, and up to 25.5 mm in females; Duellman and Lehr 2009) and by having dorsal skin shagreen with scattered tubercles and dorsal coloration brownish green or olive green. Both species produce advertisement calls with higher dominant frequencies (4000-5320 Hz; see FonoZoo recording #875 for Pristimantis mendax , and Köhler et al. 1998 and Márquez et al. 2002 for Pristimantis olivaceus ) than the advertisement call of the new species (~2500 Hz). Pristimantis mendax further differs from Pristimantis pluvialis by lacking a rostral tubercle, by possessing a sigmoid inner tarsal fold and by having dorsal skin shagreen with scattered spicules. Furthermore, Pristimantis mendax occurs in montane cloud forests above 1400 m ( Duellman and Lehr 2009), an elevational distribution range that does not appear to overlap with that of Pristimantis pluvialis .

Description of holotype.

Adult male (24.6 mm SVL); head narrower than body, its length 36.3% of SVL; head slightly longer than wide; head width 33.6% of SVL; snout short, squared in dorsal view, subtruncate in lateral view (Fig. 2); eye large, 33.9% of head length, its diameter 0.97 times its distance from the nostril; nostrils slightly protuberant, situated close to snout; canthus rostralis weakly concave in dorsal view, rounded in profile; loreal area flat; lips rounded; dorsal surface of head smooth and upper eyelids with minute tubercles; upper eyelid width 65.7% of interorbital distance; supratympanic fold absent; tympanic membrane not differentiated, tympanic annulus visible; postrictal ridges or tubercles absent. Choanae round, very small, positioned far anterior and laterally, widely separated from each other, not concealed by palatal shelf of maxilla; dentigerous processes of vomer and vomerine teeth barely noticeable.

Skin on dorsum smooth; no dorsolateral folds; skin on flanks smooth; skin on ventral surfaces and gular regions areolate; pectoral and discoidal folds absent; cloacal sheath absent, cloaca not protuberant; cloacal region lacking tubercles. Ulnar tubercle present, minute; palmar tubercle flat and bifurcate, its inner lobe much larger than outer lobe; palmar tubercle approximately twice the size of elongate, thenar tubercle; supernumerary palmar tubercles present; subarticular tubercles prominent, ovoid in ventral view, rounded in lateral view; fingers with narrow lateral fringes; fingers length when adpressed, 3> 4> 2> 1 (Fig. 3); tips of digits broadly expanded and elliptical, pads with well-defined circumferential grooves (Fig. 3); forearm without tubercles.

Tibia length 52.5% of SVL; foot length 40.3% of SVL; upper and posterior surfaces of hindlimbs smooth; heel without tubercles; outer surface of tarsus without tubercles; inner metatarsal tubercle ovoid, of higher relief and about 2.5 times the size of conical, rounded outer metatarsal tubercle; supernumerary plantar tubercles present; subarticular tubercles rounded, ovoid in dorsal view; toes with narrow lateral fringes, basal webbing absent; discs of toes expanded, rounded; toes with ventral pads well-defined by circumferential grooves; toe lengths, when adpressed, 4> 5> 3> 2> 1 (Fig. 3).

Measurements of holotype and paratopotypes are provided in Table 1. The SVL of paratypes (all males) are (in mm): MUSM 35217 = 22.5, MHNG 2607.11= 24.2, MHNG 2607.12 = 21.8, MHNG 2607.13 = 24.2, CORBIDI 11862 = 22.9, and CORBIDI 16695 = 24.9.

Coloration of holotype in life.

Dorsum orange-brown with faint brown markings (Fig. 2). Interorbital bar dark brown, forming a triangular shape posteriorly; canthus rostralis dark brown; light green on upper eyelids. Triangular brown patterning on back, not extending to venter. Hind legs with broad brown barring. Forelimbs with faint brown barring. Throat yellowish-cream; venter cream.

Coloration of holotype in alcohol.

Dorsal surfaces of head, body, and limbs grayish-tan, with dark brown regions around scapulae (see Fig. 2). Interorbital as a dark blotch that extends posteriorly; canthus rostralis dark brown. Dorsal surfaces of hind limbs with dark flecking. Iris dark gray. Throat pale white; chest and belly pale white to cream; ventral surfaces of thighs the same color as chest and belly; plantar and palmar surfaces and tips of digits pale, tubercles darker gray.

Variation.

Coloration in life is based on field notes and photographs taken by A. Shepack and A. Catenazzi of 13 type specimens. The dorsum is beige to reddish-brown with or without faint dark-brown markings (Figs 3-4). A dark brown interorbital bar is present in most specimens (barely visible in some individuals). The iris is bronze with dark-brown to red reticulations. Some individuals possess faint brown barring on hind legs. The throat is cream to yellowish-white while the belly is predominantly cream to white. Dorsal skin is generally smooth, but CORBIDI 16695, 17014 (Fig. 5), and MHNG 2607.13, have minute, scattered tubercles, indicating that skin texture might be a variable trait. Some individuals have small tubercles on the outer edge of tarsus.

Vocalization and reproduction.

Males call from grasses, shrubs, and trees in the understory of the submontane forest, during crepuscular hours and at night, conspicuously after heavy rains. Holotype CORBIDI 16510 was calling from a broad fern leaf at 150 cm above the ground, along a trail at ~30 m from a stream (Tair = 21.4°C). The advertisement call consisted of a note 28.7 ± 0.7 ms (range 23.0-35.0 ms, n = 20) in duration (Fig. 7). Pulses emitted at the highest amplitude had dominant frequencies of 2412-2584 Hz (average 2489 ± 20 Hz, n = 20) and were located in the first half of the note (Fig. 7). The calling rate was 0.70 calls/second at a temperature of 21.4°C. Male MUSM 35217 was perched on a shrub at 2 m, near a stream (Tair = 20.2°C), and produced single note calls 36.0 ± 0.5 ms (range 24.0-58.0 ms, n = 102) in duration, with dominant frequencies of 2067-2756 Hz (average 2407 ± 19 Hz, n = 102), at a calling rate of 0.64 calls/s. At least three unvouchered males were recorded at the type locality near the holotype (Tair = 21.4°C). Their calls were 40.7 ± 0.2 ms (range 26.0-47.0 ms, n = 220) in duration, with dominant frequencies of 2067-2756 Hz (average 2586 ± 20 Hz, n = 220); call rate could not be determined. Similarly, several unvouchered males recorded near MUSM 35217 (Tair = 20.2°C) produced calls with dominant frequencies of 2067-2584 Hz (average 2312 ± 13 Hz, n = 104), but their note durations and call rates could not be determined. Overall, the call of the new species can be described as a single “tock” note, 23-58 ms in duration, emitted at a rate of 0.64-0.70 calls/s, and with peak frequency ranging from 2312-2756 Hz. The call has amplitude and frequency modulation (Fig. 7): a short, high energy pulse with frequency decreasing from dominant frequency (~2500 Hz, see above) to ~2000 Hz is followed by a low energy pulse with frequency increasing from ~2000 Hz to ~2500 Hz.

Etymology.

The name of the new species is a Latin word and refers to the high rainfall recorded at the type locality, which averages ~6 m annually, and represents the peak rainfall amount along the elevational transition from the Amazon lowlands to the Andean peaks. Furthermore, males of Pristimantis pluvialis typically call during or immediately after heavy rains.

Distribution, natural history, and threats.

The new species was found during surveys in the humid sub-montane forests of the Kosñipata and Entoro valleys (Fig. 8). Observers made intensive visual searches of vegetation and leaf litter during evenings (18h30-0h00). Individuals were found after rains, calling on vegetation up to 2 m above the ground. Male CORBIDI 16511 and female CORBIDI 16512 were captured while in amplexus, during one such choruses on 16 January 2015. Average individual mass was 0.97 g ± 0.06 for males (n = 12) and 2.1 g for one female. The oviducts of this female contained 22 unpigmented eggs, about 2.5 mm in diameter. Additionally, four out of ten individuals (MHNC 15490 and CORBIDI 11862, 16512 and 16695) tested positive for the amphibian chytrid fungus Batrachochytrium dendrobatidis . This fungus has been implicated in population declines of numerous other species in this region, although it is unknown what effect it has had on this species, and there is no evidence for declines in the populations of Pristimantis pluvialis ( Catenazzi et al. 2011; Catenazzi et al. 2014). In addition to being found near, and likely within, Manu NP, Pristimantis pluvialis has been found within the Huachiperi Haramba Queros Conservation Concession, a protected area consisting of state-owned lands given in concession to private organizations with the goal of preserving biodiversity. The Huachiperi Haramba Queros concession, legally recognized in 2006 was the first concession to be granted to an indigenous community in Peru. Sympatric frog species at the type locality include Cochranella nola , Hypsiboas gladiator , Osteocephalus mimeticus , Pristimantis platydactylus , Pristimantis reichlei , and Rulyrana spiculata . Other species found around the type locality are Allobates alessandroi , Ameerega simulans , Dendropsophus parviceps , Hyalinobatrachium bergeri , Hyloscirtus phyllognathus , Hypsiboas lanciformis , Noblella sp., Oreobates granulosus , Pristimantis danae , Pristimantis fenestratus , Pristimantis mendax , Pristimantis toftae , Ranitomeya sirensis , Rhinella leptoscelis , Rhinella margaritifera , Rhinella tacana , Rulyrana spiculata and Scinax ruber .