Pristimantis pleurostriatus

Barrio-Amorós, César L., Heinicke, Matthew P. & Hedges, S. Blair, 2013, A new tuberculated Pristimantis (Anura, Terrarana, Strabomantidae) from the Venezuelan Andes, redescription of Pristimantis pleurostriatus, and variation within Pristimantis vanadisae, Zootaxa 3647 (1), pp. 43-62 : 48-57

Pristimantis pleurostriatus (Rivero, 1984 1982)

Eleutherodactylus pleurostriatus Rivero, 1984 "1982", Mem. Soc. Cienc. Nat. La Salle, 42: 88. Type locality: "San Eusebio, La Carbonera, 2.316 m. Edo. Mérida, Venezuela."

Eleutherodactylus (Eleutherodactylus) pleurostriatus Lynch and Duellman, 1997 , Univ. Kansas Mus. Nat. Hist. Spec. Publ., 23: 230.

Pristimantis pleurostriatus — Heinicke, Duellman, and Hedges, 2007, Proc. Natl. Acad. Sci. USA, Suppl. Inform., 104: Table 2.

Pristimantis (Pristimantis) pleurostriatus — Hedges, Duellman, and Heinicke, 2008, Zootaxa, 1737: 118.

Holotype: UPR 4971, by original designation. Examined through photographs ( Fig 3 ).

Referred specimens: seven (7) males (CVULA 7186–89, 7191–93) and one female (CVULA 7190) from cloud forest at Estancia la Bravera, 2352 m, 838’30’’N, 7122’59’’W, between San Eusebio and La Carbonera; collected on 10 July 2007 by C. L. Barrio-Amorós. Three unsexed specimens (CVULA 4904, 4926, 6017) from La Carbonera, Mérida.

Diagnosis: Pristimantis pleurostriatus is a small (males up to 25.3 mm SVL, only female known 31.1 mm) member of the unistrigatus species group sensu Lynch and Duellman (1997) . It is diagnosed by (1) dorsal skin with a profusion of small tubercles, some larger and pungent especially on the anterior part of the body; on upper eyelid are some small tubercles, usually one pungent; no occipital ridges, shagreen posteriorly; ventral skin areolate; (2) tympanum distinct, with a tympanic annulus, 35.5–47.5% of the ED; (3) snout semi-rounded to rounded in dorsal view, rounded in profile; canthus rostralis rounded, not well defined; (4) upper eyelid smooth in preservative, with a few low tubercles, one usually larger and pungent in life, on the posterior edge of the eyelid; (5) choanae small, round to oval; dentigerous processes of the vomers inconspicuous, covered by palatal shelf on males, small on females; tongue large, longer than wide, cordiform, posterior half free; (6) males without vocal slits, subgular vocal sac present; no apparent nuptial pads; (7) finger I shorter than II; (8) fingers with lateral keels, less evident on wellpreserved specimens; (9) ulnar tubercles present; (10) tarsal tubercles and conical heel tubercles present; (11) two metatarsal tubercles, inner oval, large; outer conical, small; (12) toes with well-marked lateral keels; webbing absent; toes III, IV and V with broad discs, slightly smaller than those on fingers III and IV; (13) in life, dorsal color light to orange-brown, with a post-occipital round mark, consistent brown diagonal stripes on whitish flanks, hidden surfaces of groin, thighs and shanks black with transverse white stripes or spots, and whitish venter with dark marbling on belly. Iris golden gray reticulated with fine venation; an orange dark brown area on each side of the black pupil; iris periphery blue. In preserve, same pattern as living frogs, but colors faded to greyish.

Species comparison: This species is compared (characters of P. pleurostriatus in parentheses) with those of the lentiginosus group of Rivero (1984 1982), P. lentiginosus , P. mondolfii and P. melanoproctus , and tuberculated similar species ( P. vanadisae and P. conservatio sp. nov.) in the Cordillera de Mérida of Venezuela and Cordillera Oriental of Colombia. Pristimantis ameliae has dorsolateral folds (absent), lacks ulnar, tarsal and heel tubercles (present), webbing vestigial (absent). Pristimantis batrachites from Cordillera oriental of Colombia (Lynch 2003) has an acuminate dorsal and protruding in lateral views (subacuminate dorsally and rounded laterally), canthus rostralis sharp (rounded, ill-defined), upper eyelid lacking tubercles (present), vocal slits present (absent), and is smaller, with females up to 21.7 mm (31.1 mm). Pristimantis pleurostriatus differs markedly from P. lentiginosus , P. mondolfii and P. melanoproctus because these species lack conical heel tubercles and protuberant ulnar and tarsal tubercles (present), and all have light spots on the groin (absent). The most similar species, with which it is sympatric, is P. vanadisae . It is easily distinguishable because adult males are much smaller, up to 19.8 mm, mean 18.6 0.7 mm; n=9 (up to 25.3 mm, mean 24.30. 7 mm; n=7); has a subovoid and longer snout (shorter and rounded), well-defined and angular canthus rostralis (round, ill defined), canthal stripe always present and well-defined (if present, ill-defined; usually absent), an iris peripheric blue ring is lacking (present), belly without consistent pattern, usually cherry colored (marbled in black and white), and yellow spots on the groin and posterior surface of thighs usually outlined with black (absent).

Description of the referred series. Head slightly longer than wide, head width 35.7–39.9% of SVL. Snout subacuminate dorsally ( Fig. 4 a) and rounded in lateral view ( Fig 2 d, 3a), without pointed tubercles except one not collected juvenile specimen, which showed a distinct pungent papilla. EN shorter than ED; nostrils nonprotuberant, directed dorsolaterally; canthus rostralis rounded but ill-defined, loreal region slightly concave. Upper eyelid with low tubercles, largest one rounded to conical on the posterior part of the eyelid; tubercles sparse on head, especially on the interorbital region. Cranial crests absent. Tympanum distinct, 37.5–45.4% of ED, tympanic annulus not well-defined; supratympanic ridge covered by small tubercles hiding a small portion of its posterodorsal section. Choanae small, rounded, not concealed by palatal shelf of maxillary arch; vomerine dentigerous processes usually inconspicuous, not visible, only apparent by touch under palatal shelf, posterior and medial to choanae. Males usually have dentigerous processes concealed by the palatal shelf. CVULA 7188 exposes one tooth on the left process; CVULA 7189 one on the left, two on the right; the female CVULA 7190 has exposed dentigerous processes, bearing on the left process two teeth and on the right four. Tongue barely cordiform, posterior half free; vocal slits absent, vocal sac present.

Dorsal skin tuberculate, with dispersed small conical tubercles or spicules also covering the flanks; occipital ridges not defined; middorsal raphe present but vague; dorsolateral folds absent; throat and chest smooth, venter and inferior part of thighs areolate; ulnar, tarsal tubercles and conical heel tubercles present, prominent in males; in the female CVULA 7190 these tubercles are less developed.

Relative length of appressed fingers III>IV>II>I; first finger surpassing the disc on finger II when appressed to each other. Finger discs much broader than long, disc on finger III of right hand 2.5–2.8 times wider than adjacent phalanx; discs quadrangular except on Finger I, which is distinctly expanded but round and smaller than those on the other fingers. Lateral fringes on fingers ill-defined. Palmar and thenar tubercles distinct, the first deeply bifid, the last ovoid. Subarticular tubercles protuberant, single, round. Supernumerary tubercles protuberant, in rows under each finger.

Hind limbs relatively short; shank 49.2–55.4% of SVL. Heel reaches midway from eye to naris when held to the sagittal plane. Relative lengths of appressed toes IV>V>III>II>I. The IV toe disc slightly smaller than the III finger disc. Toes with lateral fringes, giving the appearance of basal webbing. Discs wider than long, except those on toes I and II, which are rounded; toe discs wider than phalanges, those on toes III, IV and V quadrangular. Inner metatarsal tubercle large, protuberant, oval; outer distinct, conical; subarticular tubercles protuberant, single, round; supernumerary tubercles distinct, in rows under each toe.

Color in life and variation: CVULA 7187 in life ( Fig. 4 a) is dark brown dorsally, on the head is a brown light interorbital bar and frontal; the upper eyelids and the anterior edge of the interorbital bar are greenish. The canthal and supra-tympanic stripes are dark brown, as are three upper lip bars. There is a much darker brown dorsal chevron; the flanks are white-barred with dark brown stripes. Hind limbs are orange-brown crossbarred with dark brown. Finger pads are greenish. Ventrally the throat and chest are translucent white, while the belly is white with a striking black marbling. Iris golden gray reticulated by fine venation with an orange dark brown area on each side of the black pupil; the iris periphery is blue.

Consistent color features are the presence of a round light post-occipital spot crossed by the anterior part of the middorsal raphe, in all males, from most visible in the holotype and CVULA 7193 to less visible in CVULA 7188 and absent in CVULA 7192. The pattern is much darker on the female ( Fig. 4 b) and not easily distinguished. All seven males and the only female have the striking diagonal dark brown stripes bordered by white on the flanks, being lighter on CVULA 7189 and darker on CVULA 7190, with more contrast on CVULA 7188 ( Fig. 4 c) and CVULA 7193. One male photographed at night ( Fig 4 d) is green dorsally, including hind limbs and arms. The contrasting diagonal stripes on the flanks are bright white. In all specimens there is a black background on the anterior and posterior surfaces of the thighs, crossed by transverse white stripes, or dotted with white spots. However, this cannot be confused with the flash marks found in other species. A very distinct specimen is CVULA 7188 ( Fig. 4 c), exhibiting light brown to orange-brown with a complex design of dorsal undulating wavy stripes surrounded by white lines. Other specimens can be less contrasting, with a pale brown-orange dorsum, shanks and tarsi, with diagonal white stripes on dark brown flanks. Ventrally, all specimens have a distinguishing marbled pattern, but this pattern can be less or more contrasting. CVULA 7188, 7192 and 7193, darker on CVULA 7192 and 7193, and lighter on 7189. The female CVULA 7190 is greyish brown ventrally, also with a striking dark marbled pattern. Some juveniles are gray with black broken canthal and complete supratympanic stripes, some orange irregular spots on the dorsum and shanks, white arms, but always with the distinct diagonal stripes on the flanks.

Remarks: The original description by Rivero (1984 1982) was based on only two specimens (holotype and paratype), and these apparently are atypical compared with the larger series examined for this work. Rivero mentioned that those specimens have vomerine odontoids, while in our sample they are usually absent, and if present, small. He mentions as well a smooth dorsal skin, with just a few tubercles, while our sample is quite tubercular. The most striking difference is that he does not mention especially the presence of tarsal and conical heel tubercles, when in our sample they are well-developed. And finally, the color reported for the holotype in life is not close to what we observed in the studied sample plus many other specimens not collected. Rivero describes a longitudinally striped pattern; with a vertebral line, paravertebral and dorsolateral stripes, and purple color beneath. In no specimen from our sample have we observed this pattern and color. However, we are hesitant to describe a new species at this time based in these discrepancies without direct examination of the holotype. Rivero (1984 “1982”) also gives contradictory data about the presence of vocal slits for P. pleurostriatus . On page 89 he states that the “dimorfismo sexual consistente, hasta donde se sabe, de un saco vocal subgular muy bien diferenciado, pero sin hendeduras bucales (“sexual dimorphism consists, as far as is known, of a well-differentiated vocal sac, but without vocal slits) while on page 122 he states that the species differs from others “en tener los machos saco y hendeduras bucales (“in the males having vocal sac and slits). Without examining the holotype at UPR (Universidad de Puerto Rico), is impossible to state which one is the correct character.

Natural history: The males call from 1830h to at least 2100h, after light rains in the evening, from heights of 1 to 3 m, easily visible on bushes without much foliage ( Fig. 4 d). Three specimens were heard calling from bromeliads, one 3 m above the forest soil. The only female was on a leaf 50 cm above the ground, in the same microhabitat where all P. vanadisae from that site were observed. In our experience males of this species are never found less than 1 m from the ground, while the sympatric P. vanadisae is usually perched from 0.25 to 1.5 m above the forest floor. Pristimantis pleurostriatus appears to be rarer than sympatric P. vanadisae (8 specimens collected of P. pleurostriatus versus 24 P. vanadisae in the same period of time). Pristimantis pleurostriatus is highly seasonal, appearing only in the wet season (never seen or heard by us in March, December or January), whereas P. vanadisae can be seen throughout the year. Other amphibians observed at La Bravera and surroundings include Centrolene altitudinale (Rivero) , C. venezuelense (Rivero) , Hyalinobatrachium duranti (Rivero) , Gastrotheca nicefori Gaige , Dendropsophus meridensis (Rivero) , Hyloscirtus platydactylus (Boulenger) , Bolitoglossa orestes Brame & Wake, and the introduced Lithobates catesbeianus (Shaw) . The area was once habitat for Atelopus carbonerensis Rivero , which is currently believed to be extinct at this locality (C.L. Barrio-Amorós, pers. obs.).

Vocalization: Two series of vocalizations were recorded at 13.6 ºC the night of 3 July 2012. The call consists of one single pulsed note, that can be repeated up to 11 times, but most common is a call of one to four notes. If single, it is repeated as a short and low whistle (see Fig. 5 for single pulse oscillogram (a) and spectrogram (a’)). Fig. 6 depicts a series of 12 pulsed calls, (a) oscillogram and (a’) spectrogram. The fundamental frequency is at 2009 Hz, the dominant frequency is at 2316 Hz; the duration of the twelve-note call is 1.65 sec. Note and inter-note duration with their mean, SD and range in seconds are indicated as follows: (1) note duration, n =12, 0.03 0.01 (0.01 – 0.04) and (2) inter-note, n = 11, 0.20 0.03 (0.15–0.25). The recorded call can be heard at AmphibiaWeb.

Distribution: Pristimantis pleurostriatus is known from the cloud forests surrounding Páramo El Tambor, at the southwestern edge of the Sierra de la Culata of the Cordillera de Merida ( Fig. 2 ). The cloud forests around Páramo El Tambor are isolated and some other amphibians are known to be endemic, like Atelopus carbonerensis , Aromobates meridensis and A. mayorgai (Rivero, 1978) .

Etymology: pleurostriatus , from Greek pleuron, meaning side, and from Latin striatus, meaning stripes, due to the evident diagonal stripes on the flanks of all specimens studied.

Variation within Pristimantis vanadisae

There are two available descriptions of P. vanadisae : that of Eleutherodactylus vanadise by La Marca (1984) and that of Eleutherodactylus cerasoventris by Rivero (1984 “1982”). Even though the descriptions were based on 29 and 36 specimens, the variation in nature is not fully represented. We describe herein chromatic variation of this species more in accordance with the spectrum exhibited in wild populations.

We report four different patterns, each of which occurs at multiple localities ( Fig 7 ). Our description is based on a sample of 98 adults and subadults (specimens over 15 mm) of P. vanadisae from four localities: San Javier del Valle, Sierra La Culata, approx. 2000 m (n=1), La Bravera, between San Eusebio and La Carbonera, 2200 m (n=11), La Mucuy Alta, type locality of P. vanadisae, 2300 m (n=25), and Monte Zerpa, northeast of Merida city, 2000 m (n=61). Fig. 2 shows all localities.

Pattern A (plain) ( Fig. 7 a,b): dorsum unicolor, dark green, beige, pale yellow, or gray, patternless except for illdefined leg cross bars, and normally pigmented groin and posterior surfaces of thighs (usually black, cherry red with pale spots in adults, lacking this pattern in juveniles). Canthal and supratympanic stripes are always present and well defined (usually black but also dark brown). Forty-seven specimens in our sample have this pattern, representing 47.9%. The following specimens have this pattern: CVULA 0 186, 0 283, 0 632, 1118, 1163, 1234, 1513–14, 1642, 1648–49, 1651–52, 1680, 1682, 1684–85, 1687, 1690, 1692–94, 2014, 2020, 2022, 2208, 2317, 2356, 2428–29, 2431, 2605, 3115, 3118, 3190–21, 3123–24, 3127–29, 7185, 7200–1, 7203, 7205.

Pattern B (dorsoconcolor) ( Fig. 7 c): Dorsum (including snout, eyelids, head and back) beige, cream or pale yellow. Flanks pale brown, delimited from the dorsum by the dorsolateral folds, sometimes plain, sometimes with diagonal bars. Hind limbs with or without cross bars. Canthal and supratympanic stripes are always present and well defined. This is a less abundant pattern, found only in 3 of 98 specimens (3%). The following specimens have this pattern: CVULA 0 185, 7196 and 7204.

Pattern C (spotted) ( Fig. 7 e, f): This is the most complex and variable pattern. Dorsal color variable, yellow, green, brown, or grey in different tonalities, but always spotted on dorsum, head (always with an interorbital bar, canthal and supratympanic stripes), and cross-barred on limbs. Usually a black or dark brown “W on the scapular area. Twenty-eight of 98 (28.5%) specimens bear this pattern. The following specimens exhibit pattern C: CVULA 0745–46, 0 878, 1122, 1166, 1235, 1643, 1645–46, 1653, 2017, 2019, 2355, 2358, 2430, 3107–08, 3110–11, 3113, 3116–17, 3125–26, 7184, 7194, 7198, 7206, 7981.

Pattern D (dorsolateral stripes) ( Fig. 7 d): Main dorsal and flank color uniform, brown to grey. Interorbital bar and limb cross bars ill-defined. Two dorsolateral stripes, usually narrow, extend from the canthal above eyelid to the supratympanic stripe to the mid body, sometimes reaching sacrum area, yellow to orange. While this pattern is rarely seen in La Bravera (1 of 11=9%), it is more common at Monte Zerpa (16 of 61=26.2%). In total, this pattern represents 20.4% of the sample. Samples with pattern D: CVULA 0 285, 0 879, 1116–17, 1650, 1681, 1683, 1686, 1688, 1691, 1695, 2018, 2021, 2156, 2353–54, 2357, 3114, 7119, 7199.

Independent of the pattern variation, all specimens show canthal and supratympanic black stripes, clearly diagnostic when compared to sympatric P. pleurostriatus , and the groin and posterior surface of the thighs are dark with pale spots.

Figures

FIGURE 2. Distribution of tuberculated Pristimantis in the Cordillera de Mérida, northwestern Venezuela. Black square: 1: Black circle: Pristimantis conservatio sp. nov. 2: Pristimantis pleurostriatus (also locality for P. vanadisae). White circles: Pristimantis vanadisae. 3: La Mucuy. 4: San Javier. 5: Monte Zerpa. 6: La Macana.

FIGURE 3. Holotype (UPR 4971) of Eleutherodactylus pleurostriatus (= now Pristimantis pleurostriatus). Photos courtesy of F. Bird.

FIGURE 4. Pristimantis pleurostriatus in life. (a) male CVULA 7187; (b) female CVULA 7190, (c) male CVULA 7188, (d) uncollected calling male at the type locality.

FIGURE 5. (a) oscillogram and (a’) spectrogram of one pulsed note of a sequence of the call of Pristimantis pleurostriatus. Background noise has been strongly reduced and frequencies below 100 - 1500 Hz were filtered from the spectrogram.

FIGURE 6. (a) oscillogram and (a’) spectrogram of a 12 notes call of Pristimantis pleurostriatus. Background noise has been strongly reduced and frequencies below 100 - 1500 Hz were filtered from the spectrogram.

FIGURE 7. Pattern variation in Pristimantis vanadisae. (a) uncatalogued specimen photographed alive, and (b) CVULA 7203: Pattern A. (c) CVULA 7204: Pattern B. (d) CVULA 7199: Pattern D. (e) CVULA 7206 and (f) CVULA 7198: Pattern C.