Pristimantis totoroi, Paez, Nadia B. & Ron, Santiago R., 2019

Paez, Nadia B. & Ron, Santiago R., 2019, Systematics of Huicundomantis, a new subgenus of Pristimantis (Anura, Strabomantidae) with extraordinary cryptic diversity and eleven new species, ZooKeys 868, pp. 1-112 : 1

Pristimantis totoroi sp. nov.

Common name.

English: Totoras Rain Frog. Spanish: Cutín de Totoras.

Holotype.

QCAZ 25105, an adult male from Cashca Totoras Protected Forest, Bolívar Province, Ecuador (1.7188S, 78.9749W, 3200 m), collected by Rachel Kosoff and Ítalo G. Tapia on December 14, 2001. Figure 33A .

Paratypes

(41: 22 males, 5 females, 14 juveniles). Ecuador: Bolívar Province: Cashca Totoras Protected Forest: QCAZ 1021, QCAZ 1024, adult females, QCAZ 1020, QCAZ 1022-1023, juveniles, collected by Giovanni Onore in December 1987; QCAZ 14704-705, adult males, collected by Chris Funk in December 2000; QCAZ 16834-836, adult males, collected by Santiago Ron in January 2001; QCAZ 16916-922, adult males (1.7115S, 78.9781W, 3000 m), collected by Luis Coloma and Martín Bustamante in October 2000; QCAZ 12580, adult female (1.7200S, 78.9590W, 3200 m), collected by Felipe Campos and Stella de la Torre in December 1987; QCAZ 16718, QCAZ 16720-721, QCAZ 16731, adult males, QCAZ 16719, QCAZ 16725, QCAZ 16728, juveniles (1.7235S, 78.9802W, 2923 m), collected by Santiago Ron, Martín Bustamante, Ítalo Tapia and Mónica Guerra in August 2001; QCAZ 25122, QCAZ 25128, QCAZ 25135, adult males, QCAZ 25124, QCAZ 25127, QCAZ 25134, juveniles (1.7167S, 78.9667W, 2960 m), collected by Rachel Kosoff and Ítalo Tapia in December 2001; QCAZ 31505, adult female, QCAZ 31502, adult male, QCAZ 31501, QCAZ 31503-504, juveniles (1.7255S, 78.9806W, 2867 m), collected by Martín Bustamante and Galo Díaz in July 2002; QCAZ 32039, adult female, QCAZ 32040, adult male (1.7255S, 78.9806W, 2847 m), collected by Martín Bustamante in November 2002. Cotopaxi Province: QCAZ 58425, juvenile, from Pilaló surroundings (0.9713S, 78.9987W, 2258 m), collected by Santiago Ron, Pablo Venegas, Nadia Páez and Pamela Baldeón in November 2014. Bolívar Province: QCAZ 49511, adult male, QCAZ 49509, juvenile, from San Vicente (1.7120S, 79.0170W, 2408 m), collected by Luis Coloma and Ernesto Martínez in December 1984.

Referred specimens (1): KU 218025 from 70 km W Riobamba, Riobamba-Pallatanga road (1.9460S, 78.9468W, 2430 m), Chimborazo Province, Ecuador.

Diagnosis.

A species of the Pristimantis phoxocephalus group having the following combination of characters: (1) skin on dorsum shagreen with or without scattered small tubercles; middorsal fold; head with a middorsal row of two or more tubercles; dorsolateral folds absent; lateral folds on anterior half of dorsum; skin on venter coarsely areolate; discoidal fold evident; (2) tympanic membrane and tympanic annulus prominent, its upper and posterior margin covered by supratympanic fold; (3) snout moderately long, acuminate with a fleshy keel in dorsal view, protruding in profile; (4) upper eyelid with small tubercles; cranial crests absent; (5) dentigerous processes of vomers low to prominent, oblique, moderately separated, posteromedial to choanae; (6) vocals slits, vocal sac, and prominent nuptial pads present in adult males; (7) Finger I shorter than Finger II; discs of digits broadly expanded, rounded to elliptical; (8) fingers with broad lateral fringes; (9) small distinct ulnar tubercles; (10) heel bearing a subconical tubercle surrounded by smaller tubercles; outer edge of tarsus bearing subconical tubercles; inner edge of tarsus with a fold, followed or not by a row of small tubercles; (11) inner metatarsal tubercle ovoid, elevated, 5 times the size of round outer metatarsal tubercle; supernumerary tubercles numerous, elevated; (12) toes with broad lateral fringes; basal webbing present; Toe V much longer than Toe III (disc on Toe III reaches the middle of penultimate subarticular tubercle on Toe IV or slightly exceeds its distal edge, disc on Toe V reaches the middle of distal subarticular tubercle on Toe IV or slightly exceeds its distal edge); toe discs smaller than those on fingers, rounded to elliptical ( Fig. 9C ); (13) in life, dorsal coloration varies from cream to dark brown; flanks with dark diagonal bars; groins and posterior surfaces of thighs cream to brown with or without pale spots; venter white, bearing a midline extended or not to the throat; ventral surfaces of thighs light to dark gray, orange or cream; iris golden with a medial horizontal red streak and fine black reticulations ( Fig. 34 ); (14) average SVL in adult females: 33.0 ± 0.9 mm (31.9-34.3 mm; n = 7); in adult males: 26.8 ± 2.0 mm (23.2-29.4 mm; n = 21).

Comparison with other species.

Pristimantis totoroi is similar to P. atillo , P. jimenezi , P. phoxocephalus , P. teslai , P. torresi and P. verrucolatus sp. nov., which also have an acuminate snout with a fleshy keel. The texture of its skin is different from the other species. Pristimantis totoroi has a shagreen dorsal skin, which is tuberculate in P. atillo ; it lacks the large tubercles and warts on flanks present in P. verrucolatus sp. nov.; its tubercles and lateral folds are more prominent than those of P. atillo , P. jimenezi , P. phoxocephalus , and P. torresi . The coloration of the iris, golden with a red medial streak, helps distinguish P. totoroi from P. atillo (copper), P. jimenezi (copper to red), P. phoxocephalus (copper), P. teslai (copper), and P. verrucolatus sp. nov. (coppery brown). Additionally, the advertisement call of P. totoroi is different from the available calls of other species of the group. Notes of call of P. totoroi are shorter than those of P. jimenezi and P. verrucolatus sp. nov., inter-note intervals are longer than those of P. phoxocephalus , dominant frequency and frequency of the second harmonic are lower than those of P. jimenezi and higher than P. verrucolatus sp. nov. (Table 6).

Description of the holotype.

An adult male (QCAZ 25105, SC7093). Measurements (in mm): SVL 29.4; TL 13.9; FL 13.8; HL 10.2; HW 9.8; ED 3.6; TD 1.3; IOD 3.0; EW 3.0; IND 2.2; EN 2.9; TED 1.3. Head longer than wide, as wide as body; snout moderately long with a fleshy keel at the tip, acuminate in dorsal view, protruding in profile; cranial crests absent; nostrils slightly protuberant, narrow, directed anterolaterally; canthus rostralis concave in dorsal view, rounded in cross section; loreal region slightly concave; upper eyelid with several rounded tubercles, larger posteriorly; tympanic annulus prominent, upper and posterolateral edge concealed by supratympanic fold; tympanic membrane distinct; two prominent, subconical postrictal tubercles surrounded by smaller ones. Choanae median, ovoid, not concealed by palatal shelf of maxillae; dentigerous processes of vomers small, prominent, oblique, moderately separated, positioned posteromedial to choanae; each vomer bearing several indistinct teeth; tongue longer than wide, posteriorly notched, posterior half free; vocal slits slightly curved, located at posterior half of mouth floor in between tongue and margin of jaw; vocal sac present.

Dorsal surfaces of body shagreen with scattered small tubercles; thin middorsal fold; one tubercle between nostrils and eyes, one interorbital, two postocular and two scapular tubercles forming an inverted “V”; skin on head and loreal region bearing small rounded tubercles; dorsolateral folds absent; evident lateral folds on anterior half of flanks; skin on flanks having more prominent and larger tubercles than on dorsum; skin on chest and belly coarsely areolate, that on throat shagreen, ventral surfaces of limbs smooth, ventral surfaces of thighs coarsely areolate; discoidal fold present. Low and rounded ulnar tubercles; outer palmar tubercle bifid, slightly bigger than ovoid thenar tubercle; subarticular and supernumerary tubercles at the base of fingers prominent, rounded; fingers bearing broad lateral fringes; Finger I shorter than Finger II; discs on Fingers broadly expanded, rounded; pads on fingers surrounded by circumferential grooves on all fingers ( Fig. 9C ).

Hindlimbs slender; dorsal surfaces of hindlimbs shagreen with scattered tubercles; posterior surfaces of thighs smooth, ventral surfaces of thighs coarsely areolate; heel bearing a median, prominent, subconical tubercle surrounded by indistinct tubercles; outer edge of tarsus bearing distinct median subconical tubercles; inner tarsal fold present; inner metatarsal tubercle ovoid, elevated, five times the size of round outer metatarsal tubercle; plantar surface with small but distinct supernumerary tubercles; subarticular tubercles prominent, rounded; toes bearing broad lateral fringes; basal webbing between toes IV and V present; discs on toes smaller than those on fingers, expanded, rounded; all toes having pads surrounded by circumferential grooves; relative lengths of toes: I <II <V <III <IV; Toe V much longer than Toe III (disc on Toe III reaches distal edge of penultimate subarticular tubercle on Toe IV, disc on Toe V reaches distal edge of distal subarticular tubercle on Toe IV; Fig. 9C ). Coloration of the holotype in preservative is shown in Figure 33A ; coloration in life unknown.

Coloration of holotype in preservative. Dorsal surfaces of body dark brown, dorsum with faint middorsal longitudinal line slightly darker than background coloration; brown supratympanic stripe; dorsal surfaces of thighs with cream transversal reticulations; groins, anterior and posterior surfaces of thighs brown with cream spots; ventral surfaces of body dusty cream, venter with a faint brown longitudinal midline and faint brown flecking ( Fig. 33A ).

Coloration of holotype in life. Unknown.

Variation.

Based on the 43 specimens of the type series and photographs of five individuals. Variation of live and preserved individuals is shown in Figures 34 , 35 . Coloration in life is given in parenthesis. Dorsal coloration varies from light to dark brown (tan to dark brown); middorsal fold is dark brown to black. Dorsum may bear irregular chevrons, a broad middorsal band or parallel longitudinal stripes; scattered black flecks or white spots may be present on dorsum; head bears a black or brown supratympanic stripe, sometimes an interorbital band or stripe, and labial bars; flanks usually bear dark diagonal bars. Dorsal surfaces of thighs bear pale transversal bands, sometimes formed by rows of pale spots. Groins and hidden surfaces of thighs are cream to brown (reddish cream to brown) with or without small pale flecks or spots. Venter is cream to dusty cream with a brown midline extending from the belly to the throat; brown or gray flecks on belly, chest, and throat may be present (in males, throat varies from white to yellow). Iris is golden with a medial horizontal red streak and fine black reticulations; sclera varies from white to cream. Skin ornamentation, as middorsal fold, dorsolateral folds, and dorsal tubercles, may fade in preservative.

Advertisement call.

Based on recordings of QCAZ 25105 (December 14, 2001; 20h00), and a non-collected individual from the type locality (December 14, 2001; 21h40; 10.2 °C). The advertisement call consists of a series of 2-6 sharp peep-like notes ( Fig. 6C ); each of these notes lasts about 0.13 s (range 0.10-0.15 s) and is separated of the following note by 0.34 s (range 0.31-0.37 s). The peak time occurs exactly in the middle of the note. Fundamental frequency is the same as dominant frequency, on average 2895 Hz (range 2776-3013 Hz). Frequency increases along the note (2551-2620 Hz on average). Descriptive statistics for bioacoustic parameters are shown in Table 6.

Distribution, natural history, and conservation status.

Pristimantis totoroi is known from Western Montane Forest of Bolívar, Chimborazo and Cotopaxi Provinces, between 2258-3200 m ( Fig. 2 ). This species occurs in primary and secondary forests and pastures. Individuals found at night were on low vegetation up to 1.6 m above the ground or inside bromeliads up to 3 m above the ground. During the day they were found only inside bromeliads. Calling males have been found in October, December, and January on low vegetation during the night.

Following the B1ab(iii) + 2ab(iii) IUCN criteria, we consider P. totoroi to be Endangered because: (i) it is only known from three localities (sensu IUCN 2017); (ii) its habitat is gradually degraded by human settlements, cattle raising, and agriculture; (iii) its Extent of Occurrence <5000 km2 (346 km2); and (iv) its Area of Occupancy <500 km2 (28 km2). Its distribution overlaps with one small protected area, Cashca Totoras Protected Forest. Unfortunately, the protection of the forest is not enforced and, as a result, it is being destroyed by logging.

Etymology.

The specific epithet is a noun in the genitive case that refers to the type locality of this species, the Cashca Totoras Protected Forest. This small reserve contains Western Montane Forest and Paramo natural regions. It is one of few protected areas in the western slopes of the Andes of central Ecuador, which are part of a biodiversity hotspot. Therefore, its effective protection is urgent to preserve unique assemblages of Andean biodiversity.

Remarks.

Pristimantis totoroi has been mistakenly referred to as P. phoxocephalus (e.g., Hedges et al. 2008). Here, we recognize it as a different species and assign it to the P. phoxocephalus species group.

Figures

Figure 2. Distribution of Pristimantis, subgenus Huicundomantis. Records are based on specimens deposited at the Museum of Zoology, Pontificia Universidad Catolica del Ecuador (QCAZ). Candidate species numbers correspond to those of the text and Figure 3. Locality information is shown in Suppl. material 2. Abbreviations: CCS = confirmed candidate species, UCS = unconfirmed candidate species.

Figure 6. Comparison of advertisement calls of Pristimantis jimenezi sp. nov., P. phoxocephalus, P. totoroi sp. nov. and P. verrucolatus sp. nov. A Pristimantis jimenezi: QCAZ 46977 B Pristimantis phoxocephalus: non-collected individual from Pilalo (type locality). C Pristimantis totoroi: non-collected individual from Cashca Totoras (type locality) D Pristimantis verrucolatus: QCAZ 46981. Oscillograms are shown above spectrograms. X axis for time (s); Y axis for frequency (kHz) in spectrograms.

Figure 9. Palmar and plantar surfaces of Pristimantis teslai sp. nov., Pristimantis torresi sp. nov., Pristimantis totoroi sp. nov., and Pristimantis verrucolatus sp. nov. Photographs of hand and foot of the holotypes of the following species: A Pristimantis teslai sp. nov.: QCAZ 46213, male B Pristimantis torresi sp. nov.: QCAZ 47342, female C Pristimantis totoroi sp. nov.: QCAZ 25105, male D Pristimantis verrucolatus sp. nov.: QCAZ 46982, male. All specimens are shown at the same scale.

Figure 33. Holotypes of Pristimantis totoroi sp. nov. and P. verrucolatus sp. nov. Photographs of preserved holotypes of A P. totoroi (QCAZ 25105, male) and B P. verrucolatus (QCAZ 46982, male). Dorsal view on the left, ventral view on the right. Specimens are shown at the same scale.

Figure 34. Color variation in live individuals of Pristimantis totoroi sp. nov. A QCAZ 16718 (male, SVL 24.7 mm) B QCAZ 16721 (male, SVL 24.1 mm) C QCAZ 16725 (juvenile female, SVL 23.7 mm). Dorsolateral view on the left, ventral view on the right.

Figure 35. Color variation in preserved individuals of Pristimantis totoroi sp. nov. A Dorsal view of (from left to right): QCAZ 32039 (female), QCAZ 16918 (female), QCAZ 16834 (male) B Dorsal view of: QCAZ 16920 (male), QCAZ 25124 (juvenile female), QCAZ 25135 (male), QCAZ 31502 (male) C Ventral view of specimens in (A) D Ventral view of specimens in (B) See Suppl. material 2 for locality data. All specimens are shown at the same scale.