Pristimantis asimus, Köhler & Glaw & Aguilar-Puntriano & Castroviejo-Fisher & Chaparro & De la Riva & Gagliardi-Urrutia & Gutiérrez & Vences & Padial, 2024

Köhler, Jörn, Glaw, Frank, Aguilar-Puntriano, César, Castroviejo-Fisher, Santiago, Chaparro, Juan C., De la Riva, Ignacio, Gagliardi-Urrutia, Giussepe, Gutiérrez, Roberto, Vences, Miguel & Padial, José M., 2024, Similar looking sisters: A new sibling species in the Pristimantis danae group from the southwestern Amazon basin (Anura, Strabomantidae), Zoosystematics and Evolution 100 (2), pp. 565-582 : 565-582

Pristimantis asimus sp. nov.

Remarks.

This species has been previously referred to as Eleutherodactylus peruvianus by Schlüter (1980) and Lehr (2002 [partim]); Eleutherodactylus fenestratus by Rodríguez (1994); Eleutherodactylus aff. conspicillatus by Schlüter (2005); Pristimantis cf. danae by Moravec and Aparicio (2005); Pristimantis reichlei by Padial and De la Riva (2009 [partim]), Moravec et al. (2020 [partim]), and Herrera-Alva et al. (2023 [partim]); Pristimantis peruvianus by Pinto-Sánchez et al. (2012), de Oliveira et al. (2020), and Fouquet et al. (2022); and Pristimantis cf. reichlei by Köhler et al. (2022).

Type material.

Holotype. MUSM 41241 ( FGZC 5342 , formerly ZSM 177 / 2017), adult male (Figs 2 , 3 ), from the Área de Conservación Privada Panguana (9.6166 ° S, 74.9333 ° W, 260 m above sea level), lower Río Yuyapichis , Provincia Puerto Inca, Departamento Huánuco, Peru, collected on 29 September 2017 by F. Glaw. GenBank accession number for 16 S: ON 710989 .

Paratypes. A total of 16 specimens: ZSM 1985 – 1986 / 2008 ( FGZC 3388 – 3389), two adult males, same locality as holotype, collected on 10 December 2008 by F. Glaw; MUSM 29073 – 29074 ( FGZC 3300, 3273), two adult males, MUSM 29028 ( FGZC 3274), an adult male (call voucher), same locality as holotype, collected between 26 November and 2 December 2008 by F. Glaw; FGZC 6334 (to be deposited in ZSM), an adult male, same locality as holotype, collected on 17 November 2019 by E. Castillo-Urbina, F. Glaw and J. Köhler; SMNS 6386, an adult female, same locality as holotype, collected on 11 November 1985 by A. Schlüter; SMNS 8856, an adult male, same locality as holotype, collected in 1972 by R. Aussem; MUBI 14816, a subadult female, CM 158675 , an adult male, from Campamento 4, between Quebrada Sungaro and Quebrada Esther, Río Sepahua (11.0801 ° S, 72.1258 ° W, 395 m a. s. l.), Distrito Sepahua, Provincia Atayala, Departamento Ucayali, Peru, collected on 3 and 6 March 2014, respectively, by J. M. Padial, L. A. G. Gagliardi, J. C. Chaparro and R. Gutiérrez; CM 158600 , an unsexed adult, from a track across the river from Campamento 2, Río Sepahua (11.0491 ° S, 72.4489 ° W, 408 m a. s. l.), Distrito Sepahua, Provincia Atayala, Departamento Ucayali, Peru, collected on 24 February 2014 by J. M. Padial, L. A. G. Gagliardi, J. C. Chaparro and R. Gutiérrez; CM 158894 , an adult male from a track ca. 4 km west of Breu, on the road to Victoria (9.5451 ° S, 72.7933 ° W, 223 m a. s. l.), Distrito Yurúa, Departamento Ucayali, Peru, collected on 12 February 2015, by J. M. Padial, L. A. G. Gagliardi, R. Gutiérrez, O. Rojas and S. Castroviejo-Fisher; MUBI 12368, an adult male, from Puesto de Control y Vigilancia La Novia, Río La Novia (9.9883 ° S, 70.7084 ° W, 262 m a. s. l.), Distrito Purús, Departamento Ucayali, Peru, collected on 25 January 2013 by J. M. Padial, L. A. G. Gagliardi, R. Gutiérrez and S. Castroviejo-Fisher; MUBI 9858, an unsexed adult from Porotobango (11.4311 ° S, 73.3471 ° W, 469 m a. s. l.) Provincia La Convención, Departamento Cusco, Peru, collected on 25 January 2010 by L. Tejada; NMP 6 V 72578 / 1 – 2, two adult males (also paratypes of P. reichlei ), from Bioceanica (11.1333 ° S, 69.3666 ° W, 290 m a. s. l.), Departamento Pando, Bolivia, collected on 25 January 2005 by J. Moravec.

Definition.

A medium-sized species of the Pristimantis danae species group (based on molecular relationships and morphological similarity), with 27.7‒30.6 mm SVL in adult males (n = 7), and 37.9 mm SVL in adult females (n = 1), characterized by: (1) skin on dorsum finely shagreened, lacking enlarged tubercles or warts; throat smooth, venter areolate; discoidal fold inconspicuous; dorsolateral folds absent; upper eyelid lacking tubercles and granules; posterior surfaces of thighs smooth; (2) tympanic membrane and annulus distinct, slightly higher than long, their length less than half of eye diameter; supratympanic fold prominent, curved, slightly covering upper edge of tympanic annulus; (3) head slightly longer than wide; snout subacuminate in dorsal view, bluntly rounded in lateral profile; canthus rostralis straight in dorsal view, slightly rounded in profile; (4) cranial crests absent; (5) dentigerous process of vomers elongate, oblique, situated posteromedial to choanae; (6) males with vocal slits, single subgular vocal sac; indistinct nuptial asperities on dorsal surface of thenar tubercle; (7) hands with slender fingers, first finger slightly shorter or about equal in length to second; subarticular tubercles subconical, prominent; supernumerary tubercles absent; palmar tubercle cordiform; thenar tubercle prominent, elongated; terminal discs of inner two fingers enlarged and round, those of external fingers enlarged, truncate, about twice the width of digit proximal to disc; circumferential grooves conspicuous, ungual flap not indented; narrow lateral fringes on fingers weakly developed; basal webbing between fingers absent; (8) ulnar tubercles absent; (9) tubercles on heel and tarsus absent, tarsal fold present; (10) inner metatarsal tubercle prominent, ovate; outer metatarsal tubercle small, round, flat, barely recognizable in life, virtually absent in preservative; supernumerary tubercles absent; (11) toes long and slender; lateral fringes narrow, weak; basal toe webbing present; toe V reaching beyond distal level of penultimate subarticular tubercle of toe IV; tips of toes rounded to slightly ovate, enlarged; circumferential grooves conspicuous; (12) in life, dorsal coloration light brown, reddish-brown, or tan, usually with dark brown chevrons and flecks on dorsum; dark brown bars on dorsal surfaces of arms and legs; a pair of black spots dorsolaterally in scapular region; black supratympanic stripe; black canthal stripe; belly creamy white; throat with fine dark mottling in males; posterior surfaces of thighs blackish with yellowish-cream spots and flecking; iris bronze, with black reticulation in life; posterior iris periphery cream to turquoise; bones white; (13) advertisement call consisting of a single pulsatile note of 23–47 ms duration and with a dominant frequency of 3289–3628 Hz, repeated at irregular intervals, containing groups of 2–4 calls repeated in faster succession.

Diagnosis.

Pristimantis asimus differs from other species in the Pristimantis danae species group as follows: The new species differs from P. albertus , P. attenboroughi , P. bounides , P. clarae , P. cosnipatae , P. humboldti , P. ornatus , P. pharangobates , P. puipui , P. rhabdolaemus , P. sagittulus , P. similaris , P. stictogaster , and P. toftae , at least by the lack of dorsolateral folds (versus presence). Furthermore, P. attenboroughi , P. bounides , P. humboldti , and P. puipui have stout bodies with relatively shorter legs when compared to P. asimus . Pristimantis attenboroughi and P. puipui lack a tympanum (prominent in the new species), and P. attenboroughi lacks vocal slits in males (present in the new species). Pristimantis clarae additionally differs from the new species by dorsal and ventral color pattern, advertisement call, and smaller adult male size (12.9 – 15.6 versus 27.7–30.6 mm). As the new species, P. aniptopalmatus lacks dorsolateral folds ( Duellman and Hedges 2005) but differs by its smaller adult male size (16.5 ‒ 23.2 versus 27.7‒30.6 mm), presence of a tubercle on the upper eyelid, and color pattern ( Duellman and Lehr 2009). Pristimantis cuneirostris lacks dorsolateral folds but differs from the new species by a long wedge-shaped snout (unique in the P. danae species group; Duellman and Pramuk 1999; Duellman and Lehr 2009), lack of toe webbing (versus basal webbing present), and posterior surfaces of thighs uniformly brown (versus blackish with yellowish-cream blotches and flecks). Pristimantis scitulus mainly differs from the new species by the presence of a single conical tubercle on upper eyelid (absent), dentigerous processes of vomers absent (present), presence of a conical tubercle on heel (absent), and webbing on toes absent (basal webbing present) ( Duellman 1978).

Morphologically, P. asimus is most similar or even cryptic to P. danae and P. reichlei . However, as a tendency, nominal P. danae (from Kosñipata valley, Peru) exhibit a more contrasting dorsal color pattern in life (see, e. g., Duellman and Lehr 2009: fig. 150) when compared to P. asimus . Moreover, in dorsal view, the snout in P. danae is rounded (versus subacuminate in P. asimus ). From P. reichlei , the new species seems to differ by a very small, round, flat outer metatarsal tubercle, barely recognizable in life and virtually indistinguishable in preservative (versus distinct, ovate, subconical, recognizable in life and in preservative; Fig. 4 ). Moreover, there are slight differences in the dorsal outline of the canthus rostralis, with a relatively smaller portion of the nostrils being visible when viewed from straight above in P. asimus compared to P. reichlei , where nostrils are almost completely visible from above as the canthus rostralis shows a curved indentation around the nostrils (Fig. 5 ). The new species differs from both P. danae and P. reichlei by substantial differentiation in the 16 S gene and differences in the advertisement call (see above).

The new species occurs in sympatry with some species of the P. conspicillatus group, which superficially may have a similar appearance. However, these are distinguishable from P. asimus by molecular phylogenetic relationships, differences in advertisement calls, and most of them by different relative finger lengths, i. e., the first finger being longer than the second. However, the sympatric P. iiap has the first and second fingers equal in length but differs from the new species at least by exhibiting distinct dorsolateral folds ( Padial et al. 2016).

Description of the holotype.

An adult male, in good state of preservation (Fig. 3 ), with subgular vocal sac and vocal slits. Head slightly longer than wide (HL / HW = 1.08); snout subacuminate in dorsal view, bluntly rounded in profile; nostrils oriented posterolaterally; canthus rostralis straight in dorsal view, slightly rounded in profile; loreal region slightly concave; lips not flared; upper eyelid without tubercles; cranial crests absent. Supratympanic fold prominent, long, slightly curved, covering uppermost tympanic annulus; tympanic membrane and annulus distinct; tympanic membrane slightly higher than long, its length slightly less than half the eye diameter; one flat round postrictal tubercle. Choanae not concealed by palatal shelf of the maxillary arch when roof of mouth is viewed from below; choanae large, oval, separated by distance equal to five times diameter of a choana; dentigerous process of vomers present, but barely evident, flat, elongate, not in contact, oblique, situated posteromedial to choanae, bearing vomerine teeth; tongue removed for tissue sample; vocal sac subgular, vocal slits placed posterolaterally. Skin on dorsum finely shagreened, lacking enlarged tubercles or warts; dorsal surfaces of hind limbs finely shagreened, dorsal surfaces of forearms and flanks finely shagreened; skin on throat and chest smooth, that on belly areolate; occipital folds absent; dorsolateral folds absent; discoidal fold indistinct. Arm without ulnar tubercles; palmar tubercle cordiform, about double in size to elongate thenar tubercle; supernumerary tubercles absent; subarticular tubercles prominent, subconical; fingers long and slender; finger tips enlarged, rounded on inner two fingers, on two outer fingers truncate, their width about twice the width of digit proximal to disc; circumferential grooves conspicuous, ungual flap not indented on outer fingers; lateral fringes and keels on fingers weak, barely recognizable; basal webbing between fingers absent; relative length of fingers III > IV > II ≥ I; nuptial asperities on dorsal surface of thenar tubercle indistinct. Toes long and slender (FootL 47 % of SVL); heel and tarsus lacking tubercles; tarsal fold present; inner metatarsal tubercle ovate, prominent; outer metatarsal tubercle not recognizable; supernumerary tubercles absent; subarticular tubercles prominent, subconical; narrow lateral fringes on toes present, weakly developed; basal toe webbing present; toe tips enlarged, rounded, their width about 1.5 times the width of toe proximal to disc; circumferential grooves conspicuous; relative length of toes IV > V > III > II > I; toe V reaching slightly beyond distal level of penultimate subarticular tubercle of toe IV. Tibiotarsal articulation reaching distinctly beyond tip of snout when hindlimb flexed parallel to axis of body; heels broadly overlapping when hind limbs flexed perpendicular to axis of body. For morphological measurements, see Table 1 .

In life (Fig. 2 ), dorsal ground color light brown, with darker brown chevron-shaped marking slightly anterior to sacral region; irregular dark brown U-shaped line in scapular region, bordered posteriorly by orange-brown blotch; irregular indistinct dark brown markings and lines on dorsum; minute cream flecks, irregular in outline, scattered on dorsum; triangular cream fleck on snout tip; dark brown bars on dorsal surfaces of arms and legs; dark brown interorbital line, partly interrupted, not extending to upper eyelids; a pair of small black spots dorsolaterally in scapular region; black supratympanic stripe; broad blackish canthal stripe; lips dark brown to black, irregularly barred with cream; flanks light brown with irregular dark brown markings; belly creamy-white; anterior throat grayish-white with scattered fine gray mottling, posterior throat yellowish with irregular fine brown mottling; chest pinkish-white; ventral surfaces of thighs and shanks pinkish-gray; posterior surface of thighs blackish with irregular yellow-cream blotches and flecks; tarsus, plantar, and palmar surfaces dark brown; iris bronze, with black reticulation, with a dark reddish-brown median streak; posterior iris periphery cream with a turquoise tint; bones white. After six years in preservative (Fig. 3 ), the general color pattern remains the same as in life. Brown ground coloration turned to grayish-tan, with some pinkish tint, particularly on upper eyelids; brown flecks, bars, and markings on dorsum slightly faded; chest and ventral surfaces of thighs yellowish-cream; belly creamy-white; throat creamy-white with gray mottling.

Variation.

For variation in morphological measurements among type specimens, see Table 1 . Females are significantly larger than males, approximately reaching 25 % greater SVL. We observed some limited variation in color and color pattern among the specimens studied. In some individuals, the dorsal ground coloration is yellowish-tan to yellowish-brown in life (e. g., ZSM 1985 / 2008; Fig. 6 a ), whereas in most specimens, the dorsal ground color was reddish-brown in life (e. g., ZSM 1986 / 2008, MUSM 29074, CM 158600 ; Fig. 6 b, c, d ), as it was in the holotype. Darker dorsal markings might be more or less distinctly outlined with fine cream lines, with some individuals seemingly lacking these fine cream lines (Fig. 6 a, b ). A dark interorbital stripe is present in all specimens but narrow, less conspicuous, and barely extending on upper eyelids in the holotype and some paratypes (Figs 2 , 6 a, b ), whereas a broader, distinct stripe outlined with fine cream lines extends to the upper eyelids in other specimens (Figs 6 c, d , 7 ). Scattered dorsal cream spots and flecking might be present to different extent or completely absent. The contrasting color pattern on the posterior surfaces of thighs (dark brown with yellow-orange flecking) is present in all studied specimens, with CM 158600 having some orange color extending to the groin (Fig. 6 d ). Some males exhibit shades of yellow on the throat in life (Fig. 6 ). Remarkably, the male paratype MUBI 14816 exhibits a well-marked, W-shaped occipital fold that is lacking in other specimens.

Natural history.

At Panguana, individuals of this species have been observed being active at night, perching on small trees and bushes within disturbed primary forest. Schlüter (1980) reported males calling from vegetation mainly at 1‒2 m height, with calling activity being most intense at dusk and at dawn, which is confirmed by our own observations. Schlüter (1980) described a vertical calling position with the head down as typical, but we observed calling males in a horizontal position on the upper side of leaves. Individuals of this species have some limited ability to change color, with nocturnal color being characterized by a light brown loreal region, whereas diurnal color is characterized by a dark loreal region and upper lip, turning dark brown to almost black (see Fig. 7 ). The habitat close to the type locality has recently been impacted by illegal gold mining activities, which constitute a potential threat to the anuran fauna of Panguana.

Vocalization.

Advertisement calls of Pristimantis asimus , emitted by the male MUSM 29028, were recorded on 29 November 2008, at dusk (18: 15 h) at the type locality (ambient temperature not recorded). The calling male was sitting on top of a horizontally oriented leaf at approximately 2.1 m height within the forest. The call consists of a single short pulsatile note, repeated at somewhat irregular intervals (see below). In our recording, 4 to 14 calls were emitted in succession and then interrupted by few seconds of silence. Each call (= note) has a clearly pulsatile structure, although ‘ pulses’ are largely fused and, in most cases, barely countable. However, in some cases, distinct and thus countable energy peaks (4 ‒ 10 / call) are recognizable in the oscillograms of calls. In these calls, the pulse rate varies between 300 and 375 pulses / second. There is further amplitude modulation recognizable within each call, with maximum call energy being present around the center of each call, rapidly decreasing to a lower level, and further fading towards the call’s end. Calls were usually emitted in slow succession but regularly contained sections of more rapidly repeated calls, usually 2–4 calls emitted at shorter intervals, altering the relatively regular pattern of call repetition (see Fig. 8 a ). In other words, call repetition rate may change temporarily from ca. 140 calls / min to ca. 900 calls / min. The character of calls in these rapidly repeated sections did not differ from other calls. It remains unknown whether this increased speed in call succession has a different function (e. g., territorial) or is just part of the ordinary advertisement call. Numerical parameters for 65 analyzed calls of the mentioned male are as follows: call duration (= note duration) 23–47 ms (36.0 ± 7.1 ms); inter-call interval in slow calling sections 305–597 ms (394.6 ± 73.6 ms); inter-call interval in rapid calling sections 26–37 ms (31.8 ± 4.6 ms); dominant frequency 3289–3628 Hz (3518 ± 97 Hz); second frequency peak at around 2000 Hz; prevalent bandwidth 1600–5400 Hz.

Schlüter (1980) described the call from the same locality (under the name Eleutherodactylus peruvianus ). The spectrogram and numerical parameters (call duration ca. 40 ms) provided by him agree with our analysis. The call described by Rodríguez (1994) as that of Eleutherodactylus fenestratus from Cocha Cashu, Manu National Park, Madre de Dios, Peru, is also clearly referable to P. asimus . The parameters described by Duellman (2005) for calls of P. fenestratus from Cusco Amazónico clearly differ from those of P. asimus , but the corresponding audiospectrogram and oscillogram are in disagreement with the numerical parameters provided and may possibly correspond to P. asimus . Although difficult to compare according to another terminology used, the call described for E. fenestratus from Manaus, Brazil, by Zimmerman and Bogart (1984) seems to agree with that of P. asimus .

Distribution.

As far as known and confirmed by bioacoustic and / or genetic data, P. asimus occurs in lowland rainforests from the southern Departamento Huánuco (Panguana, type locality) and eastern Departamento Ucayali (Breu, Río Yurua) southward across most of the lowlands of southeastern Peru, reaching the border of Machiguenga Communal Reserve (Departamento Cusco) and Manu National Park (Departamento Madre de Dios) in the south as well as northernmost Bolivia (Bioceanica, Departamento Pando) to the east (Fig. 9 ). All known localities are at elevations between 220 and 470 m a. s. l. The new species occurs in syntopy with P. reichlei at least in Alto Purús National Park (La Novia, Departamento Ucayali, Peru) and probably in other places in southeastern Peru and northern Bolivia. The new species most likely also occurs further east in the Brazilian Amazon, as indicated by the call description of Zimmerman and Bogart (1984) from Manaus, but respective records are in need of clarification (see Discussion).

Etymology.

The specific epithet is a Latinized adjective derived from the Greek άσημος (ásimos), meaning ‘ inconspicuous, nameless’. It refers to the morphologically cryptic nature of the new species and the fact that it has been associated with different species names in the past, missing its status as a separate species to be named.

Figures

Figure 2. Male holotype of Pristimantis asimus sp. nov. (MUSM 41241, FGZC 5342) from Panguana, Departamento Huánuco, Peru, in life (SVL 30.6 mm): a. Dorsolateral view; b. Dorsal view (showing posterior thighs coloration); c. Ventral view.

Figure 3. Preserved male holotype of Pristimantis asimus sp. nov. (MUSM 41241, FGZC 5342) from Panguana, Departamento Huánuco, Peru: a. Dorsal view; b. Ventral view; c. Palmar surface of the right hand; d. Lateral view of the head.

Figure 4. Comparative plate showing plantar surfaces of the right feet of preserved type specimens of Pristimantis asimus sp. nov. (all from Panguana, Huánuco, Peru) and P. reichlei (all from Chapare, Cochabamba, Bolivia). Red arrows point to the outer metatarsus, showing the virtual absence versus the presence of an outer metatarsal tubercle. Not to scale.

Figure 5. Schematic line drawings of dorsal views of the heads of male Pristimantis asimus sp. nov. and P. reichlei, exemplifying the differing outlines of the canthus rostralis (bold line), resulting in the visibility of different portions of the nostrils (red) in straight dorsal view. Not to scale.

Figure 6. Paratypes of Pristimantis asimus sp. nov. in life (dorsolateral and ventral views): a. ZSM 1985 / 2008 (FGZC 3388; SVL 30.6 mm); b. ZSM 1986 / 2008 (FGZC 3389; SVL 28.4 mm); c. MUSM 29074 (FGZC 3273; SVL 28.3 mm), all from the type locality Panguana, Huánuco, Peru; d. CM 158600, from Río Sepahua, Ucayali, Peru.

Figure 7. Male paratopotype (FGZC 6334) of Pristimantis asimus sp. nov. in life at: a. Night coloration in situ; b. Day coloration the day after collection, demonstrating a limited ability of color change. Note the dark brown, almost black, loreal region and upper lip in the day coloration, resulting in a dark facemask.

Figure 8. Audiospectrograms and corresponding oscillograms of the advertisement calls of Pristimantis asimus sp. nov. from the type locality Panguana, Peru (emitted by paratype MUSM 29028) and Pristimantis reichlei from close to its type locality in the Chapare region, Bolivia, at the same temporal and spectral scale (4000 ms and 10 kHz, respectively). Oscillograms at the bottom show respective calls (those highlighted in gray in the oscillograms above) at an expanded time scale of 300 ms. Recording of P. asimus high-pass filtered at 700 Hz and that of P. reichlei band-pass filtered at 900–3600 Hz.

Figure 9. Schematic map of central-western South America showing the known distribution of species of the Pristimantis danae group referred to in the text, as inferred by molecular genetics and / or bioacoustic data. Broadly overlapping symbols may refer to the same locality. Square symbols refer to the type localities of the respective species.