Five new (extinct?) species of Atelopus (Anura: Bufonidae) from Andean Colombia, Ecuador, and Peru Author Coloma, Luis A. Author Duellman, William E. Author C, Ana Almendáriz Author Ron, Santiago R. Author Terán-Valdez, Andrea Author Guayasamin, Juan M. text Zootaxa 2010 2574 1 54 journal article 10.5281/zenodo.197448 f404d861-6038-451d-b7d6-a76a97606159 1175-5326 197448 Atelopus podocarpus sp. nov. Holotype . QCAZ 6801, adult female, from Lagunas del Compadre ( 4°10' S , 79°06' W ; ca. 3300 m ), Parque Nacional Podocarpus , Provincia Loja, Ecuador , collected on 1 December 1994 by Jenny Rudston. Paratypes . EPN 1223–26 , from Lagunas del Compadre ( 4°10'20" S , 79°06'42" W ; 3400 m ), Parque Nacional Podocarpus , Provincia Loja, Ecuador , no collection date stated on field notes, but possibly collected on September 1981 , by Luis H. Albuja V.; EPN 2143–45 , from Cerro Toledo ( 4°23' S , 79°06' W ; 2900 m ), Provincia Loja, Ecuador , collected on 11 September 1981 by Luis H. Albuja V.; EPN 3235, 3237, Mirador path nearby the Centro Administrativo Cajanuma of the Parque Nacional Podocarpus ( 3°58'09" S , 79°08'06" W ; 2850–2990 m ), Provincia Loja, Ecuador , obtained on 16–18 November 1986 by Ana Almendariz; KU 120389 , from 15 km east of Loja ( 2700 m ), Provincia Zamora Chinchipe, Ecuador , obtained on 10 June 1968 by John D. Lynch; KU 165004–5, from 13 km east of Loja ( 3°58' S , 79°06' W ), Abra de Zamora, Provincia Loja, Ecuador ; KU 178418, from Provincia Zamora Chinchipe: 13.7 km east of Loja ( 3°58' S , 79°06' W ), Provincia Loja, Ecuador ; KU 201115 –7, from 3.7 km south of Saraguro ( 3°38'49" S , 79°14'42" W ; 2800 m ), collected on 0 8 March 1984 by J. E. Simmons; QCAZ 2838 (cleared and double stained skeleton), from Centro Administrativo Cajanuma ( 4°07' S , 79°09' W ; 2800 m ), Parque Nacional Podocarpus , obtained on 25 June 1987 by Luis A. Coloma, Mario García Saltos, and Renato León. Referred specimens. KU 196633–40, from west slope Cerro Chinguela on Huancabamba–San Ignacio trail, Departamento Piura, Peru , obtained on 14–15 October 1977 by Gary R. Graves; KU 196641–42, from Cerro Chinguela, 5 Km NE Zapalache, 2900 m , Departamento Piura, Peru , obtained on 13 and 20 July 1980 respectively, by L. J. Barkley. Diagnosis. (1) A species with mean SVL in adult females 47.7 mm (39.5–52.9, SD = 3.1, n = 22) and in adult males 37.7 mm (34.4–40.9, SD = 2.6, n = 5); (2) hind limbs short, tibia length/SVL 0.322–0.424 ( n = 27); (3) phalangeal formula of hand 2-2-3-3; webbing absent; (4) foot webbing formula I( 0)—(1) II( 1 1/2)— (3) III( 1)—(3–) IV (2 2/3)—(1+) V ; (5) snout acuminate, protruding beyond lower jaw; (6) tympanic membrane and tympanic annulus absent; (7) dorsal surfaces of body smooth; arms and legs surfaces warty; ventral surface weakly aerolate; (8) red-orange spiculae (cream in preservative) on flanks and some extending to the dorsum; (9) vertebral neural processes inconspicuous; postorbital and cranial crests present; (10) dorsum entirely black, flanks with or without cream marks; (11) no minute gray stippling on dorsum of body; (12) venter and throat pale green and cream (cream or yellow in preservative), with or without dark marks; (13) gular region lacking warts, spiculae, or coni. Atelopus podocarpus sp. nov. is most easily confused with A. petersi from the north and east-central flanks of the Ecuadorian Cordillera Oriental of the Andes. The two species have similar color patterns and body proportions. However, A. podocarpus can be easily differentiated by having numerous minute brownred-orange spiculae (in life) on the flanks (18–71 spiculae on the flanks between the arms and legs counted in a straight line); in contrast, A. petersi has white spiculae aggregated into few small warts (1–21 spiculae per wart; 8–15 warts on flanks between arms and legs counted in a straight line) ( Figs. 10 , 11 A–B). Atelopus podocarpus differs from A. bomolochos (from the southern Andes of Ecuador ) and A. pachydermus O . Schmidt (from south Andean Ecuador and northern Peru ) in the dorsal coloration in life; A. podocarpus has a black dorsum, whereas A. pachydermus has a yellow and brown dorsum and A. bomolochos has a yellow to dark green dorsum ( Coloma et al. 2007 : Fig. 3 A–D). Atelopus peruensis Gray and Cannatella (from northern Peru ) is slightly smaller than A. podocarpus (SVL in A. peruensis = 32.8–38.5 in adult males; 38.4–45.2 mm in adult females; Venegas 2005 ), has, in life, black flanks with white warts (red flanks in A. podocarpus ), and a non-protruding snout (protruding in A. podocarpus ). Atelopus podocarpus and A. ignescens (from the northern Andes of Ecuador ) are similar in size and coloration (in preservative), but A. ignescens bears a patch of spiculae and coni on the gular and pectoral regions of females (absent in A. podocarpus ). Genetically, A. podocarpus is clearly differentiated from A. ignescens , A. bomolochos , A. onorei , and A. peruensis . A molecular phylogenetic analysis shows A. halihelos Peters as the sister species of A. podocarpu s ( Guayasamin et al. 2010 ). These two species are differentiated by size (male SVL of A. podocarpus = 34.4–40.9 vs 25.3 in holotype of A. halihelos ), color pattern (in preservative, black dorsum in A. podocarpus , light brown dorsum in A. halihelos ), the presence of a discontinuous dorsolateral line of warts in A. halihelos (absent in A. podocarpus ), and flanks with some warts with multiple spiculae in A. halihelos (warts never have more than one spiculae in A. podocarpus ). FIGURE 10 .— Atelopus podocarpus from Parque Nacional Podocarpus , Provincia Loja, Ecuador: (A) EPN 3235 from Mirador path nearby the Centro Administrativo Cajanuma of the Parque Nacional Podocarpus, 2850 m ; (B) EPN 1223 from El Compadre. Photos by AA and Luis H. Albuja V., respectively. FIGURE 11 .—Lateral view of two species of Atelopus , with detail on the distribution of spiculae on flanks. (A) Atelopus podocarpus ; (B) A. petersi . Note that multiple spiculae are clustered in A. petersi . Description of holotype . ( Figs. 12 A–C, virtual animation). Female. Head about as long as wide; head length and head width less than one third SVL (HLSQ/SVL = 0.276; HDWD/SVL = 0.278); snout acuminate in dorsal view, protruding beyond anterior margin of jaw; nostrils slightly protuberant; canthus rostralis distinct; loreal region concave, lips flared; interorbital region flat and smooth, eyelid without tubercles; postorbital and cranial crests present; tympanic membrane and tympanic annulus absent, tympanic area warty; postorbital and cranial crests. Forearm relatively short (RDUL/SVL = 0.291); palmar tubercle round; supernumerary palmar tubercles present; subarticular tubercles not prominent; digital tips with round pads; thumb relatively long (THBL/ HAND = 0.677) having two phalanges; hand webbing absent; fingers lacking lateral fringes; length of fingers II<III<V<IV. Tibia relatively short (tibia/SVL = 0.335); outer metatarsal tubercle conical, inner metatarsal tubercle not distinctive because the plantar surface is cream (same color as the tubercle); supernumerary plantar tubercles absent; subarticular tubercles not prominent; digital pads rounded; webbing formula I( 0)— (1) II 1 (1/2)—(3) III( 1)—(3–) IV( 2 2/3)—(1+) V ; webbing becoming fringe-like distally; length of toes I<II<III<V<IV. Dorsum smooth; numerous cream-brownish spiculae on flanks; low warts on tympanic area; low warts on dorsal surfaces of arms and legs; ventral surface weakly areolate; area surrounding the cloacal opening warty. In preservative (~70 % ethanol), dorsum and flanks black; no minute gray stippling regularly distributed on dorsum of body; dorsal surfaces of tips of fingers and toes cream, in contrast to adjacent black phalanges; Fingers II and III, and Toes I–III cream; venter and throat cream with irregular dark marks on throat and a discontinuous dark mid-stripe on belly; palms and soles black with cream marks; inner surfaces of arms cream; inner part of thighs and shanks black and cream. Measurements of holotype ( mm ): SVL 50.8, TIBL 17.0, FOOT 19.5, HLSQ 14.0, HDWD 14.1, ITNR 4.5, EYDM 4.5, RDUL 14.8, HAND 12.4, THBL 8.4, SW 11.0 Variation. Meristic variation is given in Table 7. Low warts on the arms and legs are evident is some specimens (EPN 1225, 2143, 3235, 3237, KU 201115 , 201117 ) and absent in others (EPN 1223, 1224, 2144, KU 201116 ); some individuals lack warts in the tympanic area (EPN 1223, 3237); three specimens have spiculae on the tympanic area (EPN 3235, KU 201116 –17). FIGURE 12 .—Holotype of Atelopus podocarpus (QCAZ 6801): (A) adult female, SVL = 50.8 mm; (B) ventral view of right hand, enlarged 3.3 times of A; (C) ventral view of right foot; enlarged 3.3 times of A. TABLE 7. Measurements (in mm) of the type series of Atelopus podocarpus . Mean ± standard deviation (range). 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; EYDM = eye diameter; EYNO = eye–nostril distance; ITNA = internarial distance; RDUL = radio-ulna length; THBL = thumb length; SW = sacrum width. All measurements are in mm.

Females( n = 21)	Males ( n = 5)
SVL	46.6 ± 3.13 (39.5–52.9)	37.7 ± 2.6 (34.4–40.9)
TIBL	16.8 ± 1.31 (15.0–19.5)	15.0 ± 0.9 (13.5–15.9)
FOOT	18.2 ± 1.48 (15.7–21.8)	15.4 ± 1.7 (13.0–17.1, n = 4)
HLSQ	13.3 ± 1.11 (11.0–14.8)	12.0 ± 0.7 (11.0–12.8)
HDWD	12.4 ± 1.04 (10.7–14.1)	11.1 ± 0.6 (10.2–11.6)
EYDM	4.2 ± 0.38 (3.5–4.9)	4.2 ± 0.3 (3.8–4.5)
ITNA	4.6 ± 0.58 (3.6–5.8)	4.1 ± 0.2 (3.9–4.4)
RDUL	13.7 ± 0.83 (12.4–15.2)	11.7 ± 0.6 (10.9–12.3)
HAND	11.6 ± 0.88 (9.7–13.6)	10.1 ± 0.6 (9.6–10.8, n = 4)
THBL	7.3 ± 0.68 (6.0–8.6)	6.1 ± 0.2 (6.0–6.2, n = 2)
SW	13.5 ± 1.39 (10.4–15.4)	12.3 ± 1.8 (10.4–15.3)
TIBL/SVL	(0.322–0.413)	(0.366–0.424, n = 2)
HLSQ/SVL	(0.258–0.318)	(0.310–0.326)
HDWD/SVL	(0.237–0.29)	(0.273–0.310)
RDUL/SVL	(0.269–0.319)	(0.290–0.340)
THBL/HAND	(0.535–0.677)	(0.622–0.645)

Ventral coloration varies among individuals ( Fig. 13 A–D); some have a black thick longitudinal band on the middle of the throat (EPN 1223, 1225); one individual has black throat and venter with cream marks (EPN 2143); one individual has black throat with two cream marks at the sides at the level of the articulation of the jaw (EPN 2144); generally the inner part of thighs are cream, but they may be black (EPN 2143); the inner part of shanks can be black (EPN 1223–25 , 2143–44 ), cream (EPN 3237) or black with cream marks (EPN 3235, KU 201115 –7). The venter varies from cream to yellowish (KU 201115 –7). Fingers and toes are mostly black (except for the tips), but Finger II (EPN 1223–25 , 2143–44 , 3235, 3237) and Toe I (EPN 1225, 2144, 3237) and Toe II (EPN 1223–24 ) are entirely cream in some individuals. The inner surface of the arms is black (EPN 2143), cream (EPN 1223–24 , 3235, 3237, KU 201115 , 201117 ) or black with cream marks (EPN 1225, 2144, KU 201116 ). The dorsum and flanks may be the same color, but the flanks may have some cream marks (EPN 2144). KU 196633–42: Dorsum and flanks uniform black; throat, chest, belly, and ventral surfaces of limbs dull cream. Palmar surfaces dull cream to pale brown, but black with cream palmar tubercles in KU 196633, 19636, and 196641–42. Tips of fingers cream and inner and outer metatarsal tubercles cream in most specimens. Color in life. ( Fig. 10 A–B). The following is based on color slides taken by AA (EPN 3235, dorsolateral view) and Luis H. Albuja (EPN 1223, ventral view) at Parque Nacional Podocarpus : Dorsum and dorsal surfaces of arms and legs black; flanks and spiculae in flanks orange red; face black; belly light green, throat cream with black mark in the center; palms and inner surface of arms cream; inner surface of thighs cream. FIGURE 13 .—Ventral color variation in Atelopus podocarpus in preservative: (A) EPN 2145; (B) EPN 2144; (C) EPN 2143; (D) EPN 1223. KU 165004 (field color notes and slide in dorsolateral view taken by WED on 7 March 1975 ) from Abra de Zamora, 13 km E Loja, 2850 m : Dorsum dull brownish black with dull red tubercles laterally on body. Venter green with tan streak on throat and black stripe on throat and chest. Palmar and tarsal tubercles and tips of digits white. Iris dark brown with bronze wing around pupil. Distribution, ecology and current population status. Atelopus podocarpus is only known from paramo and subparamo habitats in the southern Cordillera Oriental of Ecuador (Provincias Loja and Zamora Chinchipe) to Departamento Piura in Cordillera de Huancabamba in northern Peru ( Fig. 5 ). In Ecuador , it occurs in the following Natural Formations (classification proposed by Valencia et al. 1999 ): Herbazal Lacustre Montano, Páramo Arbustivo, Bosque Siempre Verde Montano Alto, and Bosque de Neblina Montano. These habitats lie between 2700–3400 m ( Fig. 5 ). Annual mean rainfall is 1000–2000 mm and annual mean temperature is 7–18 ºC ( Cañadas-Cruz, 1983 ). The area of its extent of occurrence is of about 2475 km 2. Habitat and other features of the Podocarpus National Park were described by Rivera-Rosi (2007) . KU 120388 –89 (John D. Lynch field notes, 10 June 1968 ) from Abra de Zamora, 15 Km E Loja, 2800 m were found under stones on dirt banks. KU 165004 (WED field notes, 7 March 1975 ) from Abra de Zamora, 13 km E Loja, 2850 m was found under a rock by day, in elfin, wind-swept scrub with a thick layer of moss, many lichens and liverworts, bromeliads on ground and on bushes, and bamboo. During the day of collection, the temperature was 8.5–18.0˚C and rainfall was 6 mm . Atelopus podocarpus is considered to be Critically Endangered (Possibly Extinct) (A2ace, IUCN Red List categories and criteria). The species is tagged as Possibly Extinct until further surveys confirm otherwise. The population has declined dramatically (more than 80 %) in the last two decades probably because of climate change and the impact of pathogens, which have affected many other montane species of Atelopus . The amphibian chytrid fungus has not been reported yet from Loja or Zamora Chinchipe provinces. The closest record of the chytrid is Azuay Province ( Ron and Merino 2000 ). The risk factor of potential threat caused by the chytrid for anuran amphibian species calculated by Rödder et al. (2009: Fig. 2 C) is high at the area of its distribution. In Ecuador , the last living individual (QCAZ 6801) was seen on 1 December 1994 . It was collected in an unhealthy condition at Lagunas del Compadre in Parque Nacional Podocarpus ; the animal died while being transported. Collecting efforts at several localities of its distribution (Abra de Zamora in September 2001 , August 2003 , December 2009 ; nearby Saraguro in June 2008 , Lagunas del Compadre in November 2009 ) revealed no individuals. In Peru , no individuals have been found since 20 July 1980 . Etymology. The specific name is a noun in apposition and refers to the Podocarpus National Park, where this species formerly lived. Podocarpus takes its name from having the country's largest contingent of the Podocarpus or romerillo tree, the only conifer native to Ecuador . Ecuador's southernmost national park ranges from 1000 meters in the river valleys to 3600 meters in the higher reaches of the Nudo de Sabanilla mountain range, part of the larger Cordillera Oriental. This park of 360,000 hectares shelters an array of cloud forests, subparamo, paramo, a series of small lakes, and many endemic species of flora and fauna.