Two New Harlequin Frogs (Anura: Atelopus) from the Andes of Northern Peru Pablo J

Southern Illinois University Carbondale OpenSIUC

Publications Department of Zoology

2008 Two New Harlequin Frogs (Anura: Atelopus) from the Andes of Northern Peru Pablo J. Venegas

Alessandro Catenazzi Southern Illinois University Carbondale, [email protected]

Karen Siu Ting

Jorge Carrillo

Follow this and additional works at: http://opensiuc.lib.siu.edu/zool_pubs Published in Salamandra , Issue 44 (2008) at http://www.salamandra-journal.com/ index.php?option=com_docman&Itemid=66

Recommended Citation Venegas, Pablo J., Catenazzi, Alessandro, Siu Ting, Karen and Carrillo, Jorge. "Two New Harlequin Frogs (Anura: Atelopus) from the Andes of Northern Peru." (Jan 2008).

This Article is brought to you for free and open access by the Department of Zoology at OpenSIUC. It has been accepted for inclusion in Publications by an authorized administrator of OpenSIUC. For more information, please contact [email protected]. Two new harlequin frogs from Peru

SALAMANDRA 44 3 163-176 Rheinbach, 20 August 2008 ISSN 0036-3375

Two new harlequin frogs (Anura: Atelopus) from the Andes of northern Peru

Pablo J. Venegas, Alessandro Catenazzi, Karen Siu-Ting & Jorge Carrillo

Abstract. Two new species of Atelopus (harlequin frogs) are described from the Andes of northern Peru, one from the northern Cordillera de Huancabamba (Departamento de Piura), 2,950 m elevation, and the other from an inter-Andean valley of the upper Marañon basin, Cordillera Central (Departamento de La Libertad), 2,620 m elevation. We also suggest the possible link between infection by the chytrid fungus and mortality of harlequin frogs in the upper Marañon basin in 999. Key words. Bufonidae, Atelopus patazensis sp. n., A. eusebiodiazi sp. n., Batrachochytrium dendrobatidis, Marañon basin, Cordillera de Huancabamba, Peru.

Introduction lations while Lips et al. (2008) rejected this hypothesis, suggesting that the loss of amphi- With more than 00 species Atelopus Du- bians in Central and South America are best méril & Bibron, 84 constitutes the most explained by Bd spreading through upland species-rich genus of Bufonidae in the Neo- populations. tropics (La Marca et al. 2005). Most Atelo- Atelopus currently includes 3 nominally pus species occur in montane habitats above described species in Peru, one third of which ,500 m elevation and have relatively restric- has been described in the last five years (Löt- ted distributions (e.g. Lötters 996). Atelo- ters & Henzl 2000, Lötters et al. 2002a, b, pus appears to belongs to be one of the most 2005a, Lötters 2003, 2007, Venegas & Bar- threatened amphibian genera worldwide, rio 2005, Coloma et al. 2007). One of the since populations of most of its species have main reasons for the recent increase in the dramatically declined over the past two de- number of known species is collecting from cades, even in sites little affected by anthro- unexplored areas throughout the Andes (e.g. pogenic alteration (La Marca et al. 2005). Rapid Biological Inventories, Lehr 2002). At Life history traits, dependence on montane least 7 additional forms of Peruvian Atelo- stream habitats and the restricted distribu- pus remain to be described, including those tions of Atelopus species seem to contribute that probably represent new taxa (Lötters to the vulnerability of these amphibians. La et al. 2005b). Most Atelopus species have re- Marca et al. (2005) reported that up to 75% latively small distribution ranges with many of the species in the genus with distributions species only known from a single populati- restricted to elevations over ,000 m have dis- on confined to one stream system (Lötters appeared. Chytridiomycosis, a fungal infec- 996). Population declines have already been tion caused by Batrachochytrium dendrobati- reported for Atelopus species in northeastern dis (Bd), has been associated with declining Peru (see Lips et al 2008). Bd is suspected to populations in at least nine species of Central be affecting the populations of Atelopus spe- and South American Atelopus (La Marca et cies in this country, but its occurrence – in al. 2005). Pounds et al. (2006) suggested a relation to time and space – remains largely link of Bd infection and climate change as the unexplored (La Marca et al. 2005, Lötters cause for declination of Andean frog popu- et al. 2005b).

The purpose of this paper is to describe nol. We studied four individuals collected in two new species of Atelopus, one from the 993 (MUSM 5893-5896) and three collec- northern portion of the Cordillera of Huan- ted in 999 (MUSM 283-285), all from the cabamba and the other from the northern type locality. Skin samples measured appro- portion of the Cordillera Central in the up- ximately 5 × 0 mm and were obtained from per Marañon basin. We also document the vertical sections in the inner part of thighs earliest known record of Bd in Atelopus in the and from longitudinal sections in the toes to northern Andes of Peru. maximize the length of stratum corneum in the sample. We examined at least three replicates of thigh sections and three replicates Materials and methods of toe section for each individual. All skin samples were dehydrated, cleared, embed- We followed the format of Coloma et al. ded in paraffin, cut into 5 μm thick sections (2000) along with some diagnostic charac- and stained with Hematoxylin and Eosin and ters of Lötters et al. (2005a). We describe PAS (Periodic Acid Schiff), thus following the webbing formulae using the system of Sa- the procedure described by Druny & Wal- vage & Heyer (969), as modified by Myers lington (980). We examined samples at & Duellman (982) and Savage & Heyer 400x and 000x and categorized them as ne- (997). Sex was determined through exter- gative when we could not find any structu- nal sexually dimorphic characters typical in re of Bd, and positive when we encountered the genus (e.g. Lötters 996). Morphome- zoospores or other structures of the fungus tric data to the nearest 0. mm were taken (see L. Berger, R. Speare & A. Kent: Dia- with dial callipers, following the character gnosis of chytridiomycosis in amphibians by definitions of Gray & Cannatella (985), histologic examination: http://www.jcu.edu. except for length of flexed forearm and sac- au/school/phtm/PHTM/frogs/histo/chhisto. rum width (see Coloma et al. 2000). Ab- htm – latest access: 20 November 999). breviations of measurements used are: snout vent length (SVL); tibia length (TIBL); foot length (FOOT); head length from the squa- Atelopus eusebiodiazi sp. n. mosal (HLSQ); head length from the exoc- (Figs. -4) cipital (HLEX); interorbital distance (IOD); head width (HDWD); eye diameter (EYDM); Atelopus sp. 8: Venegas & Cisneros 2005: eye to nostril distance (EYNO); internari- 54. al distance (ITNA); length of flexed forearm (RDUL); hand length (HAND); thumb Holotype: MUSM 738, an adult female length (THBL) and sacrum width (SW). from Huamba, 22 km ESE (airline) of Aya- Data on other Atelopus species were taken baca (4°43’7.2” S, 79°3’50.88” W) at elevation from literature sources (as mentioned th- 2,950 m, near Cerro Mayordomo, Provincia roughout text) and examination of preserved de Ayabaca, Departamento de Piura, Peru, material at Museo de Historia Natural de la obtained by Eusebio Diaz between 9 and 25 Universidad Nacional Mayor de San Marcos September 987. (MUSM), Lima. Paratopotypes: MUSM 733, 735-737, We used histological preparations to stu- adult males, MUSM 734, 74, 739 adult fe- dy the infection with Bd in skin tissues of males. one of the new species described. Skin samples were examined from specimens that had Diagnosis: () Large-sized Atelopus (SVL been fixed in 0% formalin after collection in males 35.9-4.0 mm, x = 38.3, n = 5; females the field, and have been stored in 70% etha- 43.4-47.4 mm, x =4.4, n = 3); (2) hind lim-

164 Two new harlequin frogs from Peru

Fig. 1. Lateral and dorsal views of holotype of Atelopus eusebiodiazi. Bars equal 5 mm. bs short, tibiotarsal articulation reaching at least to temporal crest when leg adpressed forward along body (TIBL/SV L = 0.3-0.37, n = 8); FOOT > TIBL; (3) phalangeal formula of hand 2-2-3-3 (determined by external examination), finger webbing absent; (4) foot Fig. 2. Palm and sole of holotype of Atelopus eus- webbing formula I (0)–(0) II (0)–(0 to 0+) ebiodiazi. Bars equal 5 mm. III (0 to -)–(0+ to 2-) IV (0+ to 2-)–(0 to 0+) V; (5) head longer than wide; snout acumi- 992 (including its junior synonym A. negreti nate with blunt point in dorsal view, protru- Ruiz-Carranza, Vélez-Rodriguez & Ar- ding beyond lower jaw; (6) tympanic memb- dila-Robayo, 995), A. galactogaster Rivero rane and tympanic annulus absent; (7) dorsal & Serna, 99, A. longirostris Cope, 868, A. surface of body bearing few warts and scatte- lynchi Cannatella, 98, A. nicefori Rivero, red coni, more dense on the posterior half of 963, A. petersi Coloma, Lötters, Duell- dorsum and dorsal surface of thighs; (8) yel- man & Miranda-Leiva, 2007 and A. subor- low or cream coni (in preservative) and some natus Werner, 899. Atelopus chocoensis can spiculae in the postorbital region, flanks, be distinguished by having a prominent su- and dorsolateral region; (9) vertebral neural pratympanic crest and a more elongate snout processes inconspicuous; (0) in preservati- (Lötters 992); A. famelicus differs by have, dorsal surface black or dark brown with ving with numerous black dots on the ven- yellow or cream irregular marks and with an ter (Castro & Bolivar 2005: 76); A. galac- irregular cream or yellow stripe that extends togaster is distinguished by lacking spiculae dorsolaterally from the tip of the snout to and coni on flanks and by exhibiting white the groin; flanks black; () venter yellowish ventral coloration (Rivero & Serna 99); A. cream with  or 3 small black blotches in the longirostris and A. lynchi differ by possessing gular region and blotches on palms and soles; a more protruding snout, a slender body and (2) gular region with coni. different ventral coloration in life, i.e. white Based on the combination of these cha- in A. longirostris and bluish gray in A. lynchi racters, A. eusebiodiazi can be distinguished (Peters 973, Cannatella 98); A. nicefori from all described Atelopus species. Several can be distinguished through its more pro- harlequin frogs from Ecuador and Colom- truding snout, slender body and smaller size bia share with A. eusebiodiazi an acuminate (Rivero 963); A. petersi is distinct because snout with blunt point in dorsal view and pro- of the presence of cream spiculae on fore- truding beyond lower jaw and/or dark dorsal arms, flanks and dorsal surface of thighs and coloration (black or brown) with clear venter by lacking coni in the gular region (Coloma (yellow or cream): Atelopus chocoensis Löt- et al. 2007); A. subornatus differs by lacking ters, 992, A. famelicus Rivero & Morales, coni and spiculae on the flanks and through

165 Pablo J. Venegas et al.

Description of holotype: body robust; no neural spines externally visible; head longer than wide; head length less than one third of SVL (HLSQ/SVL 0.297, HDWD/SVL 0.253); snout acuminated with blunt tip from above, protruding beyond lower jaw in dorsal and lateral views, dorsally slightly depressed (Fig. ); nostril blunt, slightly protuberant, cur- Fig. 3. Dorsal and ventral views of holotype of ved laterally, situated anterior to mandibular Atelopus eusebiodiazi. symphysis; canthus rostralis distinct, straight from palpebrum to tip of snout, weakly flared, concave from eye to nostril; EYNO longer than EYDM (EYNO/EYDM .090); loreal region concave; lips slightly flared; interorbital region and occiput flat; palpebrum not flared; postorbital crest distinct, not glandular; postorbital area covered with coni and some scattered spiculae; tympanic membrane and tympanic annulus (and thus expectably colu- Fig. 4. Dorsal and ventral views of male paratopo- mella) absent; choanae rounded, widely se- type MUSM 7135 of Atelopus eusebiodiazi. parated; tongue about two or three times as long as wide; broadest anteriorly, free for two smaller size (Lötters 996). Other Peruvian thirds of its length. Atelopus species with similar characters such Forearm relative short, less than one third as having an acuminate snout and/or dark of SVL (RDUL/SVL 0.9); palmar tuber- dorsal coloration include A. erythropus Bou- cle indistinct; thenar tubercle absent; rest of lenger, 903, A. pachydermus O. Schmidt, palm weakly wrinkled without defined sub- 857, A. peruensis Gray & Cannatella, 985, articular tubercles at any joints of fingers; tips A. seminiferus Cope, 874, A. tricolor Bou- of digits with rounded pads (not expanded) lenger, 902 and the new species described and no circum-marginal groove; thumb ap- below. Atelopus erythropus differs from A. eu- parently with two phalanges, relatively short sebiodiazi by having a slender body, an almost (THBL/HAND 0.355); hand webbing and la- entirely smooth skin and by its smaller size teral fringes on fingers absent; relative length (Lötters 2003); A. pachydermus is distinct of fingers: I

166 Two new harlequin frogs from Peru panic region with dense coni and scattered lars small black blotches on sole. Coloration spiculae; dense coni and some spiculae on in life is unknown. entire flank and in dorsolateral region; dorsal Measurements of holotype (in mm): SVL surface of forearm with coni in the proximal 47.4, HDWD 2.0, HLSQ 4., HLEX 2.6, portion; dorsal surface of in the thigh with EYDM 3.3, IOD 3.3, ITNA 3.6, EYNO 3.6, coni; ventral surface wrinkled; gular region TIBL 5.2, FOOT 7.0, RDUL 9., HAND 0.7, wrinkled distally. THBL 3.8, SW 3.2. In preservative, dorsal surface of body, flanks and limbs chocolate brown with ir- Variation: meristic variation of the type se- regulars black blotches and some yellowish ries (four females and four males) is given in cream blotches on flanks; ventral surface Table . Two individuals (MUSM 733, 736) cream including palm and sole with irregu- resemble the holotype in preservative colora-

Fig. 5. Map of northern Peru showing the known distributions of Atelopus eusebiodiazi and Atelopus patazensis.

167 Pablo J. Venegas et al. tion, whereas the other paratopotypes have the tip of the snout to the groin. The ventral a black dorsum with some irregular yello- coloration of all paratopotypes is similar to wish cream marks and a yellowish cream ir- that of the holotype, although three indivi- regular dorsolateral stripe that extends from duals (MUSM 737, 739, 734) have one or

Tab. 1. Measurement (in mm) and proportions of type series of Atelopus eusebiodiazi and A. patazensis. Mean followed by range in parentheses. A. eusebiodiazi A. patazensis males (n = 5) females (n = 6) males (n = 6) females (n = 4) SVL 38.3 4.4 37.6 46.7 (35.9-4.0) (33.4-47.4) (34.8-39.8) (42.7-48.8) TIBL 3.9 3.7 4. 5.9 (3.6-4.6) (2.4-5.2) (0.9-5.5) (5.8-6.2) FOOT 6.0 5.4 6.3 9.3 (4.6-7.5) (3.2-7.0) (6-7) (8.9-20.2) HLSQ 2.5 3.2 .2 2.6 (.8-3.4) (.9-4.) (0.6-.7) (.5-3.9) HLEX . .4 2.2 3.2 (0.7-2.0) (9.9-2.6) (.4-3.) (2.3-3.7) IOD 3.4 3.3 3.9 4.2 (3.3-3.6) (3.3-3.4) (3.-4.4) (3.8-4.7) HDWD 0.5 0.8 .9 2.6 (0.-.0) (9.9-2.0) (0.9-3.3) (.8-3.3) EYDM 3.3 3.4 3.3 3.9 (2.9-4.0) (3.3-3.6) (2.4-3.9) (3.7-4.2) EYNO 2.9 3.3 2.7 3.2 (2.8-3.0) (2.7-3.7) (2.4-3.2) (3.-3.4) ITNA 3.5 3.4 3.3 3.4 (3.0-4.2) (3.4-3.6) (3-3.9) (3.2-3.7) RDUL 8.8 9. 9.5 2.2 (8.3-9.8) (8.5-9.6) (8.3-0.5) (.7-2.8) HAND 9.3 9.4 9.6 .3 (8.8-0.0) (7.9-0.7) (8.-) (0.9-.7) THBL 2.8 3.3 4.8 5.9 (2.4-3.) (2.9-3.8) (4.3-5.7) (5.6-6.) SW .2 .5 .2 3.6 (0.3-2.5) (9.7-3.2) (0.6-.6) (2.4-4.6) TIBL/SVL 0.36 0.337 0.36 0.347 (0.34-0.38) (0.32-0.37) (0.047-0.49) (0.329-0.372) HLSQ/SVL 0.325 0.323 0.299 0.274 (0.35-0.333) (0.297-0.353) (0.276-0.325) (0.25-0.294) HDWD/SVL 0.274 0.265 0.36 0.274 (0.268-0.28) (0.24-0.296) (0.273-0.35) (0.24-0.292) RDUL/SVL 0.230 0.222 0.25 0.264 (0.22-0.25) (0.9-0.254) (0.236-0.269) (0.257-0.274) THBL/HAND 0.295 0.353 0.5 0.522 (0.266-0.38) (0.34-0.367) (0.4-0.654) (0.504-0.539)

168 Two new harlequin frogs from Peru two small black blotches in the gular region. Bosque de Cuyas without finding a single tra- Webbing formula varies as follows: I (0)–(0) ce of any harlequin frog. However, another II (0)–(0 to 0+) III (0 to -)–(0+ to 2-) IV (0+ patch of forest on the eastern slope of Cer- to 2-)–(0 to 0+). ro Mayordomo, El Toldo or Bosque de Tres Sexual dimorphism: in males, the canthus Cruces (4º40’S 79º3’W, ca. 700 ha), has not rostralis, palpebrum and postorbital crest are been surveyed so that there is still a chance more flared than in females. Males have small that A. eusebiodiazi can be found here. warts on flanks, in dorsolateral region and on Considering the current situation of most fore and hind limbs. Females have coni and Andean Atelopus (La Marca et al. 2005, some small spiculae on the entire flanks and Lötters 2007) and the apparent absence of coni on the fore and hind limbs. The gular A. eusebiodiazi during recent visits, we con- and pectoral regions in males have more coni sider this species to be at least near to extinc- than in females and the distal portion of the tion (IUCN Red List status: Critically Endan- gular region in females is finely wrinkled. gered). Males present nuptial excrescences covering the entire dorsum of Finger I and a narrow Etymology: The specific name is a patronym patch covering less than a quarter of the in- for Eusebio Diaz, taxidermist at MUSM, ner part of the dorsal surface of Finger II. who collected this new species and in recognition of his years of invaluable collaboration Distribution: Atelopus eusebiodiazi is known in field work and at MUSM. only from the type locality (Fig. 5), in the northern portion of the Cordillera de Hu- ancabamba, Departmento de Piura, in nor- Atelopus patazensis sp. n. thwestern Peru, at an elevation of 2,950 m. (Figs. 6-9)

Natural history and conservation: Atelopus Atelopus pachydermus (non O. Schmidt): eusebiodiazi inhabits the cloud forest around Rodríguez et al. 993: 6 (partim). Cerro Mayordomo. Several individuals Atelopus sp. 2: Catenazzi & Venegas were observed in leaf litter and along small 2005: 48. streams in September 987 and some were found again in October 997 (E. Diaz, pers. Holotype: MUSM 5893, an adult female from comm.). The cloud forest surrounding Aya- Quebrada Los Alisos (7o47’32” S, 77o35’45” baca and the type locality of A. eusebiodiazi is W) at elevation 2,620 m, in the vicinity of Pa- threatened by habitat destruction because of taz, Provincia de Pataz, Departamento de La an increase in cattle grazing and agricultural Libertad, Peru, obtained by Fonchii Chang areas. One of us (PJV) visited the type locali- in October 993. ty and adjacent areas in May and September Paratopotypes: MUSM 5894-5896, obtai- 2006 but failed to ﬁnd A. eusebiodiazi. The ned along with the holotype, MUSM 283- forest on the western slope of Cerro May- 285, obtained by A. Catenazzi and L.O. ordomo (known as Huamba) is fragmented Rodríguez on 2 June 999, MUSM 2308, with patches of less than 00 ha. The largest 7475-7476 (adult males), obtained by P. Bal- patch of montane forest near Cerro Mayor- tazar and R. Tejada on 2 August 990. domo is found in the neighbouring locality of Anchalá. This isolated forest is known as Diagnosis: () Large-sized Atelopus (SVL Bosque de Cuyas (4º 40’S 79º3’W, ca. 800 males 37.8-39.8 mm, x = 37.6, n = 6; females ha) and is completely surrounded by crop- 42.7-48.8 mm, x = 46.7, n = 4); (2) hind limbs lands (Flanagan & Vellinga 2000). In Fe- short, tibiotarsal articulation reaching at least bruary 200, PJV surveyed the amphibians of to temporal crest when leg adpressed for-

169 Pablo J. Venegas et al.

Fig. 6. Lateral and dorsal views of head of holotype of Atelopus patazensis. Bar equals 5 mm.

Fig. 8. Dorsolateral view of male individual of Atelopus patazensis in life (not a collected individual).

Fig. 9. Diseased female (infected with Bd) of Atelo- Fig. 7. Palm and sole of holotype of Atelopus pa- pus patazensis found in June 1999. tazensis. Bars equal 5 mm. ward along body (TIBL/SVL= 0.329-0.392, n ral processes inconspicuous; (0) in life, dor- = 0); FOOT > TIBL; (3) phalangeal formula sal surface orange with a larger black vermi- of hand 2-2-3-3 (determined by external ex- culated or irregular marks including limbs, amination), finger webbing absent; (4) foot or dorsum black with orange vermiculated or webbing formula I(0)–(0 to 0+) II (0)–(0 to irregular marks; () venter immaculate oran- +) III (0+ to -)–( to 2-) IV ( to 2+)–(0 to ) ge including palm and sole; (2) presence of V; (5) head about as long as wide; snout trun- spiculae below angle of jaws and on posterior cated in dorsal view, slightly protruding bey- throat in males. ond lower jaw; (6) tympanic membrane and Based on the combination of these charac- tympanic annulus absent; (7) dorsal surface ters, A. patazensis can be distinguished from of body with warts, in females (only) also all described Atelopus species. Similar spe- with coni; (8) females with coni and spicu- cies in northwestern Peru include A. pachy- lae in the postorbital region, dorsolateral re- dermus, A. peruensis and A. eusebiodiazi. The gion and flanks; males with dorsolateral row new species differs from all of them by pre- of enlarged warts, no spiculae or coni from senting a truncate snout in dorsal view (ver- postorbital region to groin; (9) vertebral neu- sus acuminate in A. pachydermus and A. euse-

170 Two new harlequin frogs from Peru biodiazi, subacuminate in A. peruensis; Gray sum and smaller size (Coloma et al. 2000). & Cannatella 985, Coloma et al. 2007). Atelopus ignescens differs from A. patazensis In addition, A. patazensis is smaller than A. by having a completely black dorsum, plus pachydermus (having male SVL > 5.3mm, fe- spiculae and coni on the pectoral region (Co- male SVL > 55.9 mm) and A. peruensis differs loma et al. 2000). from the new species by having in life a green dorsum with white spiculae on flanks (ver- Description of holotype: body robust; no sus orange dorsum with larger black vermi- neural spines externally visible; head about as culated or irregular marks or dorsum black long as wide; head length less than one third with orange vermiculated or irregular marks of SVL (HLSQ/SVL 0.288, HDWD/SVL and absence of white spiculae in A. patazen- 0.286); snout truncated, protruding beyond sis; Gray & Cannatella 985, Coloma et lower jaw in dorsal and lateral view, dorsal- al. 2007). Ecuadorian species which are si- ly depressed; nostril oval, not protuberant, milar to A. patazensis include A. bomolochos curved laterally, situated at level of mandi- Peters, 973, A. boulengeri Peracca, 904, bular symphysis; canthus rostralis distinct, A. exiguus Boettger, 892, A. guanujo Co- flared, slightly curved from palpebrum to tip loma, 2002, A. ignescens (Cornalia, 849), of snout, concave from eye to nostril; EYNO A. onorei Coloma, Lötters, Duellman & about three fourths of EYDM (EYNO/EYDM Miranda-Leiva, 2007 and A. petersi. These 0.068); loreal region concave; lips fleshy; in- species share with A. patazensis similar dor- terorbital region and occiput flat; palpeb- sal and ventral coloration and/or skin textu- rum fleshy; postorbital crest prominent and re. The new species is distinguished from A. glandular; postorbital area with small warts; bomolochos (its conditions given in parenthe- tympanic membrane and tympanic annu- ses; information on coloration referred to, if lus (and thus expectably columella) absent; not mentioned otherwise, is in preservative) choanae small, rounded, widely separated; by having dorsal warts (usually quite smooth), tongue about two or three times as long as orange or orange-yellow coloration with lar- wide, broadest anteriorly, free two thirds of ge black vermiculated or irregular marks co- its length. vering dorsal parts including limbs (may be Forearm relatively short, less than one yellowish, yellow-green or light brown) and third of SVL (RDUL/SVL 0.260); palmar tu- orange venter (yellow) (Peters 973, Colo- bercle well defined, elliptical and rounded; ma et al. 2007). Atelopus boulengeri differs thenar tubercle small, rounded and not well from A. patazensis by having smooth skin on defined; rest of palm wrinkled without defi- the dorsal surfaces and flanks (Peters 973). ned subarticular tubercle in any joints of fin- Atelopus guanujo, A. onorei and A. petersi gers; tips of digits with rounded pads (not ex- can be distinguished from A. patazensis by panded), on which a circummarginal groove having an acuminated snout in dorsal view, is absent; thumb apparently with two pha- dorsum uniformly orange or green (in A. gu- langes; relatively short, distance from tip to anujo and A. onorei) and by the presence of outer edge of palmar tubercle less than half whitish spiculae on the forearms, flanks and hand length (THBL/HAND 0.26); webbing thighs in the case of A. guanujo and A. pe- in hands absent, finger lacking lateral fringes; tersi (Coloma 2002, Coloma et al. 2007). relative length of fingers: I

171 Pablo J. Venegas et al. rounded, inner metatarsal tubercle larger lateral region, postocular region and flanks than outer, rounded (distally expanded); rest covered by warts without coni or spiculae, of sole wrinkled with indistinct subarticu- except for forearms and near the arm inser- lar tubercles including joints of phalanges of tions. Venter is finely wrinkled with spiculae toes II-V; foot webbing formula is I (0)–(0+) and coni only under the angles of jaws, distal II (0)–() III (0+)–(2-) IV (2-)–(0+) V; relati- portion of throat and on the ventral surfaces ve length of toes: Itoads were observed along the ries (six males, four females) is provided in streams. On 2 June 999, AC surveyed the Table . Dorsal coloration in A. patazensis stream Los Alisos which cuts across the town varies from almost black dorsum and limbs of Pataz and a small effluent of Los Alisos. with orange vermiculation or irregular blot- Three freshly deceased and two dying speci- ches to orange dorsum with black mottling. mens were recorded after intensive searches One female (MUSM 5895) differs from the along the main stream from 5:30 to 6:00 other type specimens by having some small h. The small stream was located north of the spiculae in the interorbital space and the pos- town along the road connecting Pataz with terior surface of palpebrum. the mining concession of Compañia Mine- Webbing formulae varies as follows: I (0)– ra La Poderosa. Two deceased and one appa- (0 to 0+) II (0)–(0 to +) III (0+ to -)–( to rently healthy male of A. patazensis were ob- 2-) IV ( to 2+)–(0 to ) V. served at this site from 6:5 to 7:00 h. Tad- Sexual dimorphism: males develop scat- poles were observed along the main stream tered warts on dorsum without coni or spi- of Los Alisos. A dissected gravid female culae, a row of enlarged warts in the dorso- (MUSM 284; SVL 48.8 mm, mass at capture

172 Two new harlequin frogs from Peru

9.5 g), found dead on 2 June 999 at Quebra- chydermus (Coloma et al. 2007) caused the da Los Alisos, contained 348 eggs of diameter review of the original description and type .8-2.0 mm (n = 0). The eggs were cream in material of A. bomolochos by Coloma et al. preservative. Surveys on 5 July 2000 along (2000), resulting in the description of a new Quebrada Los Alisos and its effluent failed species, A. onorei, based on an Ecuadorian to detect adult A. patazensis. Merely a single population previously allocated to A. bomo- tadpole was found in a small pool along the lochos (e.g. Lötters 996, Coloma et al. main stream channel. 2000). With regard to the unclear status of An examination of skin sections of A. pa- A. bomolochos, the characters of A. patazen- tazensis revealed that four specimens collec- sis satisfactorily differentiate these two forms ted in 993 were not infected by Bd, whereas (see the comparison above). two of three specimens (MUSM 283, 285) Rodríguez et al. (993) reported A. pachy- collected in 999 contained Bd zoosporangia dermus from the Departmentos de Amazo- (Fig. 0). This proves the presence of Bd in nas, Cajamarca and La Libertad, Peru, based northern Peru for the year 999 and may also on MUSM collections but without providing explain the abrupt population declines in A. reasons for applying this name (at that time peruensis and A. pachydermus (e.g. Lötters applied to material from northern Ecuador; et al. 2005b; Coloma et al. 2007). These spe- see Coloma et al. 2007). The record from La cies were abundant during the 980s and be- Libertad of Rodríguez et al. (993) apparent- ginning of the 990s in many localities of the ly refers to A. patazensis since this is the only Cajamarca-Celendin and Cutervo ranges re- Atelopus from this department at MUSM that spectively, but apparently declined between was tentatively identified as A. pachydermus 995 and 998 and have not been observed in the museum catalogue. since 998 despite increased efforts to find them (PJV, unpubl.). We lack observations of A. patazensis for Discussion the time after 999. However, considering the current situation of most Andean Atelo- Peters (973) used FOOT > TIBL and re- pus in general (La Marca et al. 2005) and latively long thumbs (with apparently two the apparent presence of Bd in A. patazensis, phalanges) to define a phenetic Atelopus ig- we consider this species to be at least near to nescens group. Thumb length as used by Pe- extinction (IUCN Red List status: Critically ters (973) was reviewed by Lynch (993), Endangered). who considered this character as a way of re- cognizing Atelopus species groups and hypo- Etymology: The specific name refers to the thesized that species with phalangeal reduc- type locality. tion in the thumb might reflect a monophy- letic assemblage (i.e. flavescens group sensu Taxonomic remarks: According with Colo- Lynch 993). Atelopus eusebiodiazi and A. ma et al. (2000, 2007), the status of Atelopus patazensis share FOOT > TIBL and relatively bomolochos has been uncertain, basically be- long thumbs with other species of Atelopus. cause of the concept of A. ignescens sensu lato However, we agree with Coloma et al. (2000, applied by Peters (973) and the recogniti- 2007) and Coloma (2002) that defining on of an A. exiguus-bomolochos complex by Atelopus species groups in a phylogenetic Gray (983) including several populations of sense may be premature. As a result, we can- Atelopus from southern Ecuador. The recent not state whether similarities shared among clarification of the taxonomic status of A. ig- Andean Atelopus do reflect synapomorphies, nescens sensu stricto (Coloma et al. 2000), plesiomorphies or just convergence. A. exiguus (Coloma et al. 2000) and A. pa- The majority of Andean Atelopus species

173 Pablo J. Venegas et al.

Acknowledgements

We thank J. Cordova and C. Aguilar for allo- wing access to the collection of the MUSM. We thank J. Cernaqué (Lab. de Enfermedades Infec- ciosas, Dep. de Microbiología, Universidad Peru- ana Cayetano Heredia) and J. Sandoval (Lab. de Patología, Hospital Dos de Mayo, Lima) for assis- tance with histological analysis of skin sections. The 999 and 2000 ﬁeld excursions to the Rio Abi- seo National Park were kindly organized by APE- CO (Asociación Peruana para la Consevación de la Naturaleza).

References

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174 Two new harlequin frogs from Peru

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Rivero, J.A. & M.A. Serna (99): A new species Appendix of Atelopus (Amphibia, Bufonidae) from Anti- oquia, Colombia. – Brenesia, 36: 5-20. Material examined in addition to the new species Savage, J.M. & W.R. Heyer (967): Variation and Atelopus pachydermus sensu stricto: PERU: Caja- distribution of the tree frog genus Phyllomedu- marca: Grutas Cutervo, MUSM 7027-703; De- sa in Costa Rica, Central America. – Beiträge partamento Amazonas: Camporedondo, MUSM zur Neotropischen Fauna, 5: -3. 6524. Atelopus peruensis: PERU: Cajamarca: Ca- jamarca Hacienda Taulis MUSM 3602-3603, Ya- Savage, J.M. & W.R. Heyer (997): Digital web- nac, MUSM 3604-3606, Cumbe, MUSM 383- bing formulae for anurans: a reﬁnement. – 386, Cordillera de Kunulka, MUSM 904-92; Herpetological Review, 28: 3. Ancash: Yurayacu, MUSM 920-929, Charco, Venegas, P.J. & J. Barrio (2005): A new species MUSM 6596-660, 728-73. of harlequin frog (Anura: Bufonidae: Atelopus) from the northern Cordillera Central, Peru. – Revista Española de Herpetología, 29: 03-2. Venegas, P. & D. Cisneros (2005): Atelopus sp. 8. – pp. 54 in Rueda-Almonacid, J.V., J.V. Rodríguez-Mahecha, S. Lötters, E. La Marca, T. Kahn & A. Angulo (eds.): Ranas arlequines. – Bogotá, Conservación Internaci- onal. Panamericana Formas e Impresos S. A.

Manuscript received: 18 January 2008 Authors’ addresses: Pablo J. Venegas, Investigador Asociado-Centro de Ornitología y Biodiversidad (CORBIDI), Santa Rita 117, Huertos de San Antonio, Surco, Lima, Peru, E-Mail: [email protected]; Alessandro Catenazzi, Department of Biological Sciences, Florida International University, Miami FL 33199, USA; Karen Siu-Ting, Departamento de Herpetología, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256, Lima, Peru; Jorge Carrillo, Departamento de Ciencias Biológicas y Fisológicas, Universidad Peruana Cayetano Heredia, Lima, Peru.

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