Atelopus pachydermus ( Schmidt, 1857 )

Coloma, Luis A., Lötters, Stefan, Duellman, William E. & Miranda-Leiva, Alfonso, 2007, A taxonomic revision of Atelopus pachydermus, and description of two new (extinct?) species of Atelopus from Ecuador (Anura: Bufonidae), Zootaxa 1557, pp. 1-32 : 4-11

Atelopus pachydermus ( Schmidt, 1857)

Phirix pachydermus Schmidt, 1857:15 . Holotype: KM 1013/1356 from “Neu-Granada”; Schmidt, 1858:257.

Phryniscus pachydermus: Hoffmann, 1878:635 (by implication).

Phryniscus cruciger (non Lichtenstein and Martens): Boulenger, 1882:154 (partim).

Atelopus cruciger (non Lichtenstein and Martens): Nieden, 1926:84 (partim).

Phirix pachydermus: Dunn, 1931:397 .

Atelopus subornatus (non Werner): Dunn, 1944:81.

A.[telopus] pachydermus: Rivero, 1963:107 .

Atelopus pachydermus: Rivero, 1965:138 (partim); Peters, 1973:34 –37 (partim); Lötters, 1996:39 –40 (partim), 2005:97 (partim).

Referred specimens. Peru: MUSM 6524 from Camporedondo, Departamento Amazonas; MUSM (field number 890081a), MUSM (field number 890085), MUSM 13810–12, MUSM 5984, 6507 collected from nearby Grutas of Parque Nacional Cutervo, Departamento Cajamarca, obtained on March 1984 by Alfonso Miranda-Leiva; Ecuador: MHNG 2259.8–9 from Valladolid-Yangana, approximately 2600 m above sea level, Provincia Zamora Chinchipe, obtained on September 1985 by Giovanni Onore and Luis A. Coloma.

Diagnosis. (1) A large species with mean SVL in adult males 51.3 mm (44.2–56.4, n = 7) and in adult females 55.9–61.6 (n = 2); (2) hind limbs short, tibiotarsal articulation reaching to temporal region, when leg carried forward along body (tibia length/SVL = 0.375–0.439, n = 9); (3) phalangeal formula of hand 2–2–3–3 (suspected from external examination), basal webbing absent; (4) foot webbing formula I (0+)—(1- to 1+) II (0+ to 1-)—(1 to 2+) III (1 to 2-)—(2+ to 3) IV (2 to 3+)—(0+ to 1-) V; (5) snout acuminate, with tip gently rounded in dorsal view; upper jaw slightly protruding beyond lower; (6) tympanic membrane absent; (7) dorsum with widely scattered or dense well-defined, rounded warts; (8) scattered spiculae on posterior and ventrolateral surfaces of body or absent; (9) vertebral neural processes inconspicuous; (10) dorsum yellow with dark brown pattern of marks, blotches and/or lines (dorsum cream, tan, or olive with pale to dark brown pattern in preservative); (11) venter white, occasionally orange or red (venter tan to yellow with pale to dark brown blotches in preservative); (12) gular region without warts, spiculae, or coni.

Atelopus pachydermus is distinguished from all Atelopus by its large size, except A. boulengeri Peracca, 1904 , A. arsyecue Rueda-Almonacid, 1994 , and A. laetissimus Ruíz-Carranza, Ardila-Robayo and Hernández-Camacho, 1994 . It differs from all of them by a different color pattern. Atelopus boulengeri usually has a uniform dorsum, and is larger than A. pachydermus (mean female SVL of A. boulengeri [after data in Coloma, 1997]) = 65.9 vs. 55.9–61.6 in A. pachydermus ). Atelopus arsyecue has large white, cream, creamy-yellow, round or elongated marks ( Rueda-Almonacid, 1994; Renjifo and Renjifo, 2005:57). Atelopus laettisimus has a reticulated pattern usually bearing an X-mark on the anterior dorsum ( Ruíz-Carranza et al., 1994; Galvis, 2005:83).

Description of holotype. Adult male ( Fig. 1 ), well preserved; original colors apparently bleached; forearm twice as thick proximally as distally; keratinized areas on thumb. Head slightly longer than wide; head length and head width each less than one third SVL; snout acuminate, tip of snout with swollen gland, rounded in dorsal view, slightly protruding beyond anterior margin of the jaw in profile; nostrils not protuberant, barely visible from above, situated slightly behind level of apex of lower jaw; canthus rostralis distinct, convex from tip of snout to nostril, concave from nostril to eye, swollen posteriorly; loreal region concave, upper lip slightly flared, interorbital and occipital regions flat, smooth, eyelid flared without distinct tubercles; postorbital crest glandular; tympanic membrane absent; choanae minute, rounded; tongue twice as long as wide, broader anteriorly, less than its posterior half not attached to mouth’s floor. Forearm relatively short, length of forearm less than one third SVL; metacarpal tubercles distinct, round, outer about twice size of somewhat weaker inner; few weak supernumerary tubercles present; subarticular tubercles at joints of fingers IV and V; digital tips slightly broadened, with round pads; thumb relatively short, more than half length of hand, apparently having two phalanges; nuptial pads on inner or dorsal thumb absent; basal webbing and fringes on fingers absent; relative length of fingers II<III<V<IV. Tibia relatively short, 39 % of SVL; no fold on distal half of inner edge of tarsus; metatarsal tubercles distinct, rounded outer slightly larger than ovoid inner; supernumerary tubercles absent; subarticular tubercles present at joints of toes III–V, digital pads distinct; toe webbing formula I(0+)—(1) II (0+)—(2) III(2-)—(3) IV (3+)—(0+) V, webbing always becoming fringelike distally; relative length of toes I<II<III<V<IV.

Dorsum smooth, flanks wrinkled, both with scattered, round, flattened warts about 2 mm in diameter (no conspicuous spiculae); no warts on dorsum of head (present up to squamosal region) and sides of head including temporal region (warts behind angle of jaw and on postorbital crest). Wrinkling and warts on dorsum of upper arm, elbow, femur and knee. Ventral surfaces slightly wrinkled, without warts, spiculae or coni, except for smooth forearm and entire leg. Cloaca opening an inconspicuous tube slightly above midlevel of thighs, directed posteriorly; no warts around cloacal opening.

In preservative (~70% ethanol; Fig. 1 ), dorsally and ventrally cream, with pale brown almost symmetrical linear pattern and some pale brown warts on dorsum. Pale brown, round blotch (about diameter of eye) each on thigh, shank, inner and outer heel, foot, ventral tibia, proximal metatarsus, and elbow (on dorsal parts of hind limbs, blotches may be duplicate); upper thumb light brown, ventral femur, and entire rest of arm and hand cream. Pale brown area below cloaca; nares cream; eyes black.

Measurements (mm). SVL 52.9, TIBL 20.7, FOOT 23.5, HLSQ 14.9, HDWD 15.2, EYDM 4.6, EYNO 3.7, ITNA 4.5, SW 15.6, RDUL 16.7, HAND 14.8, THBL 9.3.

Variation. Meristic variation of seven adult males (including holotype) and two females is given in Table 1 . Two juveniles from Ecuador (MHNG 2259.8–9) have SVL 29.7 and 21.7, respectively. They are tentatively assigned to Atelopus pachydermus . All specimens resemble the holotype. The two available females (MUSM 5984, 6524) are larger than the males; the forearm of females is not swollen; nuptial pads, present in adult males (but absent in MUSM 6507), cover dorsum and inner margins of Finger II. The number of warts is more or fewer than in the holotype. Warts, and spiculae are highly visible. In MUSM 6524 spiculae are present behind the eye, on posterior part of dorsum and on the thighs, and in MUSM 13812 also ventrolaterally on the body. In some specimens warts are present in the interorbital region, but never anterior to it; laterally warts are present in the temporal region; warts also are present around the cloaca opening. In MUSM 5984 (female) some warts are present on the chest, and in MUSM (field number 890085, male) warts are present on the chest and the ventral surfaces of the thighs. Subarticular tubercles are present on joints of phalanges of all toes and fingers. Scattered supernumerary tubercles are present on the soles and palms of all individuals. Foot webbing ranges as follows: I (0+)—(1- to 1+) II (0+ to 1-)—(1 to 2+) III (1 to 2-)—(2+ to 3) IV (2 to 3+)—(0+ to 1-) V.

Atelopus petersi Atelopus pachydermus

Provincia Napo Provincia Chimborazo Departamentos Cajamarca & Amazonas Color variation in preservative (~70% ethanol): Dorsum and venter color pattern variation is depicted in Figure 2 . The dorsum is tan or olive with a pale to dark brown pattern, or blackish brown with tan to pale yellow pattern. The dorsal pattern consists of irregular or semi-symmetrical markings, blotches and/or lines; the anterior head, or at least its periphery, and most parts of the feet and hands are tan or pale yellow. The arms and legs are tan or olive with pale to dark brown semi-symmetrical dots and blotches, or blackish brown with tan or pale yellow markings. The venter is tan or yellow with few irregular pale to dark brown markings, most evident on the posterior part of the belly (at least brown markings below the cloaca); legs and arms always with markings, sole and palm in part or without markings, tarsal tubercles usually uniform yellow.

Color in life ( Fig. 3 A): Lötters (2005:97) provided a color photograph of Atelopus pachydermus from Cutervo. As well, he provided a color in life description. “Dorsum very variable, mostly bright yellow with large black markings. The yellow color turns to white (occasionally orange or red) in ventral region.” Juveniles from Ecuador (MHNG 2259.8–9, color transparencies (QCAZ transparencies 2292–94, available at AmphibiaWebEcuador: http://www.puce.edu.ec/zoologia/vertebrados/amphibiawebec/anfibiosecuador/ bufonidae .html) have dorsum, dorsal surfaces of limbs and flanks yellow-green with black marks. The iris has a yellow ring around the pupil.

Distribution, ecology and current population status. Atelopus pachydermus is known from the Cordilleras de Tarros (at Cordillera Occidental) and Central of the Andes of northern Peru, departamentos Cajamar-ca and Amazonas, and from Cordillera Oriental of the Andes in southern Ecuador, Provincia Zamora Chinchipe at about 2600 m above sea level ( Fig. 4 ). In Peru, the area in which A. pachydermus occurs includes Humid Montane Forest, following the classification of types of vegetation of the Peruvian Andes as modified by Duellman (2004), who followed the system proposed by Tosi (1960). At the Peruvian Parque Nacional Cutervo (6º 00'– 6º 20' S 78º 40'– 78º 53' W, 2350–3350 m above sea level) annual mean temperature is 13.8 C. According to Duellman and Pramuk (1999), the vegetation in Peru of the humid montane forest of Cordillera Occidental is reduced to few trees, bushes ( Baccharis ) and bunch grasses; much of this forest has been cleared and cultivated, and at higher elevation Eucalyptus has been planted. In Ecuador, the locality is in Montane Cloud Forest ( Valencia et al. 1999) in the Nudo de Sabanilla. In its proximities, 2000 hectares of forest and paramo habitats are protected within the Reserva Tapichalaca, which is located south of the Parque Nacional Podocarpus. Annual mean precipitation in this region is 1000–2000 mm and annual mean temperature is 12–18 C ( Cañadas-Cruz, 1983).

In both adult females studied by us, eggs are visible through the skin of the venter.

The current population status of Atelopus pachydermus in Peru is unknown. Fieldwork by The University of Kansas in February 1989 in the vicinity of Cutervo, Departamento de Cajamarca revealed no Atelopus . Nonetheless, the most recent record is from 1994 or 1995, close to San Andrés caves in Parque Nacional Cutervo, when Heinz Plenge took the photograph shown in Lötters (2005). Searches for A. pachydermus were carried out by AML at Parque Nacional Cutervo in 1996 and nearby localities in Provincia Chota in 1997 and 1998; at north of San Andrés de Cutervo by Pablo Venegas in January 2007; they revealed no Atelopus . Also, people at these localities mentioned their absence. The San Andrés caves are located in Parque Nacional Cutervo, which has 8214 hectares of land protected by the Peruvian Government. In spite of its protection status, potato and artichoke field crops are located in the area of the Cutervo caves and there is extensive cattle ranching inside the park. The only record from Ecuador is from September 1985. Searches at the Ecuadorian locality were carried out on February and September 2001 and on April 2004; they revealed no Atelopus .

Comments. Rodríguez et al. (1993) and Lötters (2005) reported Atelopus pachydermus from the Andes of northern Perú (departamentos Amazonas, Cajamarca, and La Libertad). They failed to provide museum and specimen numbers, and specific locality data. Listing Departamento La Libertad was an error and referred to an undescribed smaller, but otherwise similar species from Pataz (see Catenazzi and Venegas, 2005:148).

Translation of the original description of Phirix pachydermus Oscar Schmidt (1857:14–15). " Phirix with robust fore- and hind limbs, head moderate; snout somewhat acute; skin thick, firm; color sulphur to whitish, light bluish pattern on dorsum and on femur as well as in cloacal region." For a translation from German into English of Schmidt´s 1858 description see Cochran and Goin (1970:120).

Etymology. The specific name pachydermus is Greek and means thick skin.

Figures

FIGURE 1. Holotype of Atelopus pachydermus (KM 1013 / 1356). Male, SVL = 52.9 mm.

FIGURE 2. Color pattern variation of dorsum and venter of Atelopus pachydermus. Specimens are those listed under Referred specimens from Peru plus one individual (lower row at center), unnumbered at MUSM, which was neither measured nor examined in detail here.

FIGURE 3. (A) Atelopus pachydermus from Cutervo, Peru (no museum number associated, photo AML); (B, C) A. bomolochos from 10 Km S Cutchil, Provincia Azuay (KU 217443 – 44, photos LAC); (D) A. bomolochos from 19 Km S Cutchil, Provincia Azuay (KU 217445, photo LAC); (E, F) A. onorei from Río Chipla, Provincia Azuay (no numbers associated, photos LAC).

FIGURE 4. Map of southern Ecuador and northern Peru showing localities of Atelopus pachydermus. 1 = Provincia Zamora Chinchipe: Valladolid-Yangana; 2 = Departamento Amazonas: Camporedondo; 3 = Departamento Cajamarca: Cutervo.

Tables

TABLE 1. Measurements of Atelopus petersi and A. pachydermus, respectively. Mean ± one SD, and range are given. Abbreviations follow Gray and Cannatella (1985) and Coloma et al. (2000). They are: SVL = snout-vent length; TIBL = tibia length; FOOT = footh length; HLSQ = head length; HDWD = head width; EY DM = eye diameter; EYNO = eyenostril distance; ITNA = Internarial distance; RDUL = radio-ulna length; HAND = hand length; THBL = thumb length; SW = sacrum width. All measurements are in mm.

	Males (n = 16) Females (n = 7) Females (n = 3)	Males (n = 7)	Females (n = 2)
SVL	38.9 ± 2.0 46.1 ± 2.08 45.6 ± 3.3 (35.2–42.1) (43.5–50.2) (43.3–49.3) (n = 8)	51.3 ± 3.9 (44.2–56.4)	58.8 (55.9– 61.6)
TIBL	14.6 ± 1.14 16.5 ± 1.3 16.9 ± 0.8 (13.1–17.2) (14.2–17.9) (16.2–17.7)	21.2 ± 1.16 (19.4–23.1)	22.8 (22.4–23.1)
FOOT	15.9 ± 1.6 18.7 ± 1.1 16.6 ± 2.9 (13.8–18.4) (16.8–19.9) (14.7–19.9)	21.6 ± 1.86 (19.0–23.7)	23.3 (22.9–23.6)
HLSQ	11.7 ± 0.7 13.3 ± 0.7 13.1 ± 1.7 (10.5–12.8) (12.2–14.3) (11.5–14.8)	16.4 ± 1.38 (14.1–17.8)	17.1 (16.9–17.3)
HDWD	11.7 ± 0.8 12.9 ± 0.8 12.3 ± 1.3 (10.4–13.1) (12.0–14.0) (11.0–13.5)	15.6 ± 0.97 (13.8–16.9)	16.6 (16.4–16.7)
EYDM	3.7 ± 0.3 4.5 ± 0.7 4.4 ± 0.7 (3.3–4.1) (4.4–4.5) (3.9–5.2) (n = 8) (n = 2)	5.1 ± 0.51 (4.3–5.8)	5.1 (4.7–5.5)
EYNO	2.8 ± 0.1 (2.7–2.9)	3.7 ± 0.38 (3.2–4.1)	3.8 (3.6–4)
ITNA	4.3 ± 0.6 4.5 ± 0.6 4.6 ± 0.2 (3.5–5.4) (3.4–5.1) (4.4–4.7)	4.6 ± 0.27 (4.2–5.1)	5.15 (4.9–5.4)
RDUL	11.4 ± 1.3 13.8 ± 1.7 12.9 ± 1.1 (9.6–14.9) (11.6–17.2) (12.2–14.2)	16.1 ± 1.02 (14.9–17.9)	17.8 (17.3–18.3
HAND	10.0 ± 0.75 12.1 ± 0.8 11.1 ± 1.0 (8.7–11.3) (10.9–12.9) (10.3–12.3)	13.8 ± 0.98 (12.5–15.2)	15.7 (15.4–15.9)
THBL	6.4 ± 0.5 7.8 ± 0.8 7.4 ± 0.9 (5.6–7.2) (6.7–8.7) (6.6–8.4) (n = 13)	8.7 ± 0.54 (8.0–9.5)	10.1 (9.9–10.3)
SW	12.6 ± 1.61 13.8 ± 0.1 12.5 ± 2.3 (10.7–15.3) (12.4–14.9) (9.9–14.0) (n = 8)	16.8 ± 1.36 (15.1–18.8)	19 (17.1–20.9)