Pristimantis reichlei, Padial & Riva, 2009

Padial, José M. & Riva, Ignacio De La, 2009, Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura: Strabomantidae), Zoological Journal of the Linnean Society 155 (1), pp. 97-122 : 111-118

PRISTIMANTIS REICHLEI SP. NOV. ( Fig. 9A )

Holotype: MNK-A 6620 (field number JMP 286 ), an adult female from Los Guácharos 500 m asl, Carrasco National Park , Provincia Chapare, Departamento Cochabamba, Bolivia (17°03′51.5″S / 65°28′34.7″W) collected by J. M. Padial and D. Embert, 9.vii.2003.

Paratopotypes: MNCN 43012 (adult female, field number JMP 295 ), 43024 (adult female, field number JMP 303 ), 43028 (adult male, field number JMP 313 ), MNK-A 6621 (adult female, field number JMP 296 ), collected by J. M. Padial and D. Embert, 10–14.vii.2003, CBG 327 (adult male), 328 (adult female), 329 (adult male), collected by R. Aguayo.

Paratypes: BOLIVIA: Departamento Cochabamba: ZFMK 72587–9 , 72564–5 , 72537 a locality between Paractito and El Palmar , Carrasco National Park , collected by J. Köhler and S. Lötters, 16–18.xii.1998 ; ZFMK 66973–6 , 66988 , from a point between Parajti and El Palmar, Carrasco National Park , collected by J. Köhler and S. Lötters, 3–6.ii.1998 ; ZFMK 59574 , from Villa Tunari , collected by P. Ibisch, 22.viii.1991 ; Departamento La Paz: MNCN 43071–2 (adult males, field numbers 596–7), MNK-7193 (adult male, field number 595), from Arroyo Huactaya, Madidi National Park (14°20′12.1″S, 68°05′57.3″W) collected by D. Embert, 16.xii.2003 ; MNK-A 7273 (adult male, field number JMP 952 ) from Serranía de Bella Vista , road between Caranavi and Palos Blancos, collected by J. M. Padial and C. Ureña, 07.iii.2004 ; MNK-A 7178, from Chalalán, Area Natural de Manejo Integrado Madidi (14°25′28.4″S, 67°55′14.4″W), collected on 13.xii.2003 by J. M. Padial and D. Embert; Departamento Pando: NMP6 V 72578 /1–2, from Bioceanica (11°08′S, 69°22′W) (adult males, field number JM 65-66 ), collected by J. Moravec, 25.i.2005 ; MNCN 43151 , Florida, Reserva Nacional de Vida Silvestre Manuripi (immature female) collected by M. Guerrero ; PERU: Departamento Cusco: MNCN 43249 (juvenile), 5 km from San Lorenzo on the road to Quince Mil , collected by I. De la Riva, J. C. Chaparro, S. Castroviejo and J. M. Padial, 22.ii.2006 . Departamento Huánuco: NMW 28966 (ten specimens, two adult females and eight juveniles) from Río Llullapichis, Panguana, 220 m, collected by M. Aichinger; Mean ± standard deviation in parentheses follows range (in mm) .

Departamento Madre de Dios: KU 154856–57 from Cocha Cashu, Manu National Park, collected by C. A. Toft, 10 and 20.viii.1973, KU 205107 collected by T. A. Titus, 16.ii.1986, KU 205120 collected by P. A. Burrowes and R. de Sá, 2.ii.1986, KU 205132 collected by L. Trueb, n 09.i.1986, KU 205133 collected by T. Titus, 1.i.1986, KU 205134 collected 1986 by P. A. Burrowes and R. de Sá, 28.i, KU 205137 collected by R. de Sá, by R. McDiarmid, 14–22.ix.1988, USNM 342630–2 collected by R. McDiarmid and V. Morales, 24.i.1989, USNM 342854–55 , 345174–76 , collected by R. Reynolds and J. Icochea, 2.vii.1993, USNM 345177 collected by R. Reynolds and P. Sehgelmeble, 14.ii.1992, USNM 345278 collected by R. Reynolds, 21.ii.1992, USNM 345279 collected by P. Sehgelmeble, 29.ii.1996, USNM 345280–1 collected by R. Reynolds, 29.ii and 2.iii.1992, all from Pakitza , Reserve Zone , Manu National Park , c. 57 km (airline) NW of mouth of Río Manu , on Río Manu (11°52′S, 71°18′W) .

18.ii.1986, KU 205138 collected by P. A. Burrowes, 27.ii.1986, KU 205142 collected by P. A. Burrowes, 01.ii.1986, KU 207708 collected by A. Channing, 22.xi.1986, KU 207715, collected by W. E. Duellman, 16.xi.1986, KU 207716 collected by B. Quibell, 17.xi.1986, KU 207717 collected by B. Quibell, 24.xi.1986, KU 215481 collected by V. R. Morales, 15.i.1989, KU 215482 collected by E. R. Wild, 24.i.1989, KU 215483 collected by D. A. Kizirian, 26.i.1989, KU 215484 collected by W. R. Wild, 02.vii.1989, KU 215485 collected by D. A. Kizirian, 11.vii.1989, KU 215486 collected by H. R. Sisniegos, 12.vii.1989, KU 215487 collected by A. W. Salas, 25.i.1990, KU 215488 collected by L. A. Coloma, 16.ii.1990, all from Cuzco Amazónico, 15 km E of Puerto Maldonado; KU 154853–4 colected by C. A. Toft, 03.viii.1973, KU 154855 colected by C. A. Toft, 04.viii.1974, all from Manu river, Manu National Park, 365 m; MCZ 136394 (adult female), Puesto Euahuipa, Río Palma Real Grande, Santuario Nacional Pampas del Heath, collected by J. Cadle; USNM 298900 (adult male) and 298901 (subadult female) collected by J. Cadle, 4–5.ii.1984; 342623–29 collected Referred specimens: BOLIVIA: Departamento Beni: MNK-A 4178, 4203–7, 4181, Serranía del Pilón, Antena de Entel; Departamento Cochabamba: CBG 437, Altamachi 1000 m; CBG 373–7, Arepucho 1000 m, Carrasco National Park; CBG 200–202, Chaquisacha 1500 m, Carrasco National Park; CBG 1021, Bia Recuate 210 m, Isiboro-Sécure National Park; CBG 544, road from Villa Tunari to El Palmar, 1000 m, Carrasco National Park; CBG 333, 524–526, Río Ichilo, brazo muerto; CBG 957–62, road from Villa Tunari to El Palmar 1300 masl; CBG 746, Santa Anita, Isiboro- Sécure National Park; CBG 604–11, Santo Domingo, Isoboro Sécure National Park; CBG 560, Villa Fátima; Departamento La Paz: CBG 378, CBG 845–49, CBG 851–3, Boquerón, 1000 m; CBF 5223–5, Candelaria, Madidi National Park; MNK-A 4128, Lima; MNK-A 4112–3, Quebrada Boquerón 1140 m; MNK-A 4081–2, San Ignacio 1100 m; MNK-A 3692, 3703, 3705, 3710, 3714, 3717, Serranía Beu; MNK-A 4743, Serranía de Chepite; CBF 2485–6, Serranía Pilón Lajas; MNK-A 4119–22, 4126–32, 4139–43, Serranía San Ignacio; Departamento Pando: MNK-A 5178, Arroyo Tulapa, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 6034–5, 6044, 6069–70, Campamento Malecom, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 6083–5, 6095–8, 6090, Campamento Nueva América, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 4401, Campamento Serna-Humaita, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 6896, Curichón, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 4597, El Porvenir road; MNK-A 5085, 5095–110, Florida, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 4596, Mukden; MNK-A 6174, Nueva España, Reserva Nacional de Vida Silvestre Manuripi; MNK-A 4592–5, 4598–9, Reserva Nacional de Vida Silvestre Tahuamanu; MNK-A 6891, San Antonio, Reserva Nacional de Vida Silvestre Manuripi; USNM 336178, San Juan de Nuevo Mundo, 18 km N; CBF 2538, 2543–4, San Sebastián; PERU: Departamento Cusco: USNM 537903–34, San Martín-3, c. 5 km N of the Camisea River; Departamento Huánuco: MHNSM 12444–6, Dantas, Río Pachitea; MNHNSM 603–612, Río Llullapichis, Panguana, 220 m; Departamento Madre de Dios: MHNSM 17347–52, Pakitza, c. 57 km (airline) NW of mouth of Río Manu, on Río Manu; USNM 222269–73, 247305–21, 247632–3, 343241, 268946–53, Puerto Maldonado, 30 km (airline) SSW, Tambopata Reserve, Explorer’s Inn; USNM 346142, Atalaya, c. 3 km NW, on west bank of Río Alto Madre de Dios, Hacienda Amazonia; MHNSM 751–755, 1194, 9302–3, 9259–68; MHNSM 10070, 15508, 15585, Cocha Cashu, Manu National Park; MHNSM 620–626, 14673, 14676, 14678, Cuzco Amazónico, 15 km E of Puerto Maldonado; USNM 298839–44, Lago Valencia, extreme W bank, Río Madre de Dios; MCZ 136395–6, Puesto Euahuipa, Río Palma Real Grande, Santuario Nacional Pampas del Heath; MHNSM 14011, USNM 332444–46, Río Tambopata, W bank, Zona Reservada Tambopata–Candamo, Colpa de Guacamayos; MHNSM 613–16, 628, 1032–7, Río Tambopata; BM 1987.610–2, Tambopata Wildlife Reserve, junction río La Torre and río Tambopata; Departamento Puno: BM 1907.5.7.22, Río Huacamayo, Carabaya, 2000 ft.

Diagnosis: A member of the Pristimantis unistrigatus Group, as defined by Lynch & Duellman (1997), characterized by: (1) skin on dorsum homogeneously shagreen; flanks shagreen; venter coarsely granular; posterior surfaces of limbs smooth; discoidal fold not evident; dorsolateral folds absent; postrictal glands present; (2) tympanic membrane and annulus round, large, their length about half eye length; supratympanic fold short, very prominent; (3) head slightly longer than wide; snout round in dorsal and lateral views; canthus rostralis straight in dorsal view, sharp in profile; (4) cranial crests absent; upper eyelid without conspicuous granules; (5) vomerine odontophores large, situated posteromedial to choanae; (6) males with vocal slits and a single white nuptial pad on thumb; (7) fingers short, first finger shorter than second; subarticular tubercles subconical, prominent; supernumerary tubercles round, prominent, smaller than subarticular tubercles; terminal discs of inner two fingers moderately expanded, those external fingers very enlarged, ovate to truncate; circumferential grooves conspicuous, ungual flap not indented; lateral fringes and keels on fingers present; (8) single ulnar tubercles present; (9) tubercles on heel and tarsus absent; tarsal fold prominent, longer than inner metatarsal tubercle; (10) inner metatarsal tubercle ovate, prominent, outer subconical, prominent; a single supernumerary tubercle, round to conical; (11) toes long and slender (foot length 50% SVL); lateral fringes or keels conspicuous, basal toe webbing absent; fifth toe reaching the tip of penultimate subarticular tubercle of Toe IV, third toe reaching the base; tips of toes rounded to ovate, expanded; ungual flap not indented, circumferential grooves conspicuous; (12) dorsal coloration variable, mostly tan with dark brown flecks and chevrons; ventral coloration white with fine mottling; posterior surface of thighs brown with conspicuous orange (white in preservative) spots; (13) mandibular ramus of the trigeminal nerve passing lateral to the m. adductor mandibulae externus (S condition sensu Lynch, 1986).

The presence of orange spots (white in alcohol) in the posterior surface of thighs has led this species to be frequently mistaken for P. peruvianus . However, it differs from P. peruvianus by having first finger shorter than second, coarsely granular belly and lacking dorsolateral folds. For differences with other members of the P. conspicillatus Group see Table 3. Pristimantis reichlei is most similar to P. danae , from which it cannot be distinguished by qualitative characters ( Table 3, Fig. 9B ). Nevertheless, differences in morphometrics, advertisement call and 16S rDNA allow a clear separation (see above). This species is readily distinguished from other members of the group by the combination of: canthus rostralis and loreal region bold, dorsum finely shagreen, and presence of orange spots on posterior part of thighs. Other species of the P. unistrigatus Group (sharing Finger I < II, granular or aerolate belly and any kind of orange spots) inhabiting the Andean foothills and/or adjacent lowlands are distinguished as follows: P. altamazonicus , P. carvalhoi and P. croceoinguinis all present one or two large red, orange or yellow blotches on the anterior surface of thighs and adjacent flanks, are smaller and have warty skin; P. diadematus , P. eurydactylus and P. ventrimarmoratus present bold black reticulation and spots on belly and limbs and have warty skin; P. rhabdolaemus , P. toftae and P. sagittulus have conspicuous dorsolateral folds; P. salaputium , P. martiae and P. platydactylus all have warty dorsal skin, poorly evident tympanic membrane and lack orange or yellow spots on posterior surfaces of thighs; finally, P. ockendeni presents a conspicuous dark subocular vertical bar, has light brown canthal and loreal regions, and lacks pale spots on posterior surfaces of thighs.

Description of the holotype: Head as long as wide (head length/head width = 1.0); snout round in dorsal and lateral profile; nostrils slightly protuberant, orientated laterally; canthus rostralis straight in dorsal view, sharp in frontal profile; loreal region flat; lips not flared; upper eyelid without tubercles or granules; no cranial crests. Supratympanic fold prominent, short; tympanic membrane and tympanic annulus large, distinct; tympanic membrane nearly round, its length about half of eye length; 2–3 postrictal glands, conical, conspicuous. Choanae not concealed by palatal shelf of the maxillary arch when roof of mouth is viewed from below; choanae large, ovate; vomerine odontophores large, prominent, drop-shaped, situated posteromedial to choanae but with the anterior margin at the level of choanae, separated by a distance of one half the length of a vomerine odontophore, bearing a row of around ten vomerine teeth. Skin of dorsal surfaces and posterior parts of hind limbs homogeneously shagreen; throat smooth, belly and groin coarsely areolate; occipital folds absent; dorsolateral folds absent; discoidal fold not evident.

Arm with a single low, round ulnar tubercle; palmar tubercle bifid, flat, conspicuous, equal in length to elongate, prominent, thenar tubercle; a single supernumerary tubercle on the basis of each finger, round, prominent, smaller than subarticular tubercles; subarticular tubercles prominent, subconical; finger tips round, moderately expanded on fingers I and II, and large, ovate to truncate on fingers III and IV; Finger III bearing lateral fringes; relative length of fingers: III > IV > II <I.

Toes long and slender (foot length 50% of SVL); heel and tarsus lacking tubercles; tarsal fold prominent, twice length of inner metatarsal tubercle, not in contact with it; inner metatarsal tubercle ovate, prominent, larger than outer; outer metatarsal tubercle prominent, subconical; one supernumerary tubercle on toes II, III and IV; subarticular tubercles conical, prominent, much larger than supernumerary tubercles; conspicuous lateral fringes on toes I, II and III; basal toe webbing absent; toe tips round, moderately developed; ungual flap not indented, circumferential grooves evident; relative length of toes IV > III > V > II > I; Toe III reaching the base and Toe V reaching midpoint of penultimate subarticular tubercle of Toe IV.

Measurements (in mm) of the holotype: SVL 32.3, HL 12.6, HW 11.8, EL 3.8, EN 4.0, IND 3.0, EE 6.1, TYH 1.7, TYL 1.7, FIII 1.6, FIV 1.6, FA 6.6, TL 20.51, TH 18.7, FL 17.0, TIV 1.6.

Colour: In preservative, dorsal surfaces tan with dark brown chevrons, flanks lighter. Bold black colour on canthus rostralis, supratympanic fold, pair of occipital spots, around vent, knees and elbow, that of canthus and supratympanic fold outlined by a thin white stripe; loreal region dark brown to black; interocular dark brown bar; grey diffuse subocular and labial bars; tympanic membrane brown, annulus cream; arms with transverse dark stripes, oblique on hind limbs; plantar surfaces dark brown; ventral surfaces cream with inconspicuous fine greyish-brown mottling, some enlarged spots on belly; thighs intensely mottled, shanks completely brown ventrally; posterior and anterior surfaces of hind limbs dark brown with well-defined white spots. The colour pattern in life is similar, but the dorsum is greyishbrown and the spots of posterior surfaces of thighs are orange. The ventral surfaces are white and the groin is yellowish-white. The iris is metallic yellow to orange with a transverse bold black stripe.

Variation: Males and females are similar in all but sexual qualitative external characters. Males commonly bear a single, white, glandular non-spinous nuptial pad on dorsal surface of each thumb, but some males have double nuptial pads. All breeding males present subgular vocal sac and vocal slits. Females are larger than males but are equal in head and limb proportions ( Table 5). Gravid females contain large unpigmented eggs on the oviducts. The dorsal pattern is quite constant, although varies in intensity of colours and contrast of stripes. Some specimens may have more reddish, greyish or yellowish-brown colorations. Some dark dorsal marks, as an interocular stripe, a W-shaped occipital mark, an X-shaped middorsal mark or sacral chevrons, can be present. The brown mottling on ventral surfaces also varies in intensity. In life, the colour of the spots of the posterior surface of thighs varies from yellow to intense orange; the spots can be anastomosed or well separated, and vary in density, with some specimens showing only one or two spots. Moreover, some specimens also show the pattern of spots in the anterior surface of the thighs. For example, eight (of nine) specimens from Boquerón (in Departamento La Paz, Bolivia) bear this pattern. In contrast to the holotype, some specimens have enlarged granules on the dorsum and eyelids. The shape and development of vomerine odontophores also varies, and the row of vomerine teeth can be single or double. Another character that varies in intensity is fringe development on fingers and toes, although it is always present to some extent. For measurements, see Table 5.

Etymology: The name is a patronym for Steffen Reichle, German herpetologist and friend, whose studies have greatly contributed to the understanding of Bolivian amphibian diversity.

Distribution: This species occurs from the Departamento Huánuco, in Amazonian Peru, along the Andean slopes and adjacent lowlands of Peru, Brazil and Bolivia. The southernmost record lies in the Chapare region of central Bolivia ( Fig. 8 ). It has been recorded in lowland Amazonian forest and humid montane forest of the Andean foothills up to 1500 m (Chaquisacha, Carrasco National Park, Bolivia). The parapatric altitudinal distribution of P. danae and P. reichlei , along most of their distributional ranges, makes some identifications uncertain. Doubtful records should be tested by means of morphometric, bioacoustic or molecular analyses. However, P. danae has been recorded from higher altitudes and seems to be restricted to southern Peru and northern Bolivia. Mean ± standard deviation in parentheses follows range (in mm).

Table 6. Summary of results of different comparative analyses applied to solve taxonomic problems of two species of Pristimantis

The southernmost record of P. danae corresponds to Valle de Zongo, Departmento La Paz, Bolivia (16°11′47.5″S, 68°07′35.5″W) .

Natural history: This species is active by night during the rainy season. Males call from low vegetation in the forest. It has been found only in primary and secondary forest formations.

Remarks: The advertisement calls described for P. peruvianus from Panguana ( Peru) by Schlüter (1980), Cocha Cashu ( Peru) by Rodríguez (1994) and Tambopata by Duellman (2005) correspond to P. reichlei . The last of these was reanalysed herein ( USNM tape 265/17; Table 1). The Bolivian record of P. danae by Köhler & Jungfer (1995) and the advertisement call of P. danae from Chapare 1250 m by Köhler (2000a) correspond to P. reichlei . The illustration and call of P. danae by Köhler & Lötters (2002) correspond to P. reichlei . The illustration of P. danae by De la Riva et al. (2000: 141) corresponds to P. reichlei . The illustration of P. peruvianus by De la Riva et al. (2000: 145) corresponds to P. danae . Specimens from Tambopata reported by Doan & Arizábal (2002) as P. peruvianus correspond to P. reichlei . Specimens cited by Padial et al. (2004) as P. danae for different localities in Bolivia correspond to P. reichlei and are now included herein as referred specimens (see above). Peruvian specimens reported by Padial & De la Riva (2005a) as P. cf. peruvianus (except KU 154863–5) also correspond to P. reichlei . Specimens identified by Padial, Bielskis & Castroviejo (2000) as P. cf. peruvianus from the Andean slopes of Department La Paz are P. fenestratus . The diagnosis and redescription provided by Köhler (2000a) for P. peruvianus matches qualitative characters of many Colombian, Ecuadorian and northern Peruvian populations assigned to this species. However, the taxonomic status of P. peruvianus remains uncertain because characters proposed by Lynch (1980) to separate it from P. conspicillatus seem invalid due to variability. This variability renders the diagnoses of some recently described Peruvian species of this group quite inconsistent ( Table 3). However, the resolution of these problems lies outside the scope of this paper and will be treated elsewhere.

Figures

Figure 8. Map of part of South America depicting the approximate distribution of Pristimantis danae, P. koehleri, P. fenestratus, P. reichlei, and P. samaipatae.

Figure 9. A, adult male of Pristimantis reichlei from Chalalán, Departamento La Paz, Bolivia (MNK-A 7178); B, adult male of P. danae from Huairuro, Departamento La Paz, Bolivia (one from the series MNCN 43054–64, 43067–8).