A new species of Atelopus (Anura: Bufonidae) from southern Peru Herrera-Alva, Valia Díaz, Vladimir Castillo, Ernesto Rodolfo, César Catenazzi, Alessandro Zootaxa 2020 2020-09-23 4853 3 404 420 Herrera-Alva & Díaz & Castillo & Rodolfo & Catenazzi, 2020 Herrera-Alva & Díaz & Castillo & Rodolfo & Catenazzi 2020 [151,461,1518,1545] Amphibia Bufonidae Atelopus Animalia Anura 4 408 Chordata species moropukaqumir sp. nov.   Figs. 3–5.  urn:lsid:zoobank.org:act: 7818BF15-03EC-46E8-942B-AFDB7A9AC5ED     Holotype. MUSM 40370( Figs. 3–5) an adult male from near Anchihuay, at  2039 ma.sl., Distrito de Anco, Provincia La Mar, Departamento de Ayacucho, Peru( 12°59’S, 73°40’W), collected by V. Herrera, E. Castillo, M. Fernández, V. Díazand J. Gamboaon  20 November 2018.   Paratypes.Ten total:  MUSM 40364–69, 40371same data as the holotype;  MUSM 40376–78collected at the type locality by E. Castillo, M. Fernández,  V. Díazand J. Gamboaon  13 June 2019.  Characterization.(1) A small species of  Atelopuswith a mean SVLof 20.6 mmin adult males ( 19.9–21.6 mm, SD = 0.55 mm, n = 9) and 20.5 mmin adult females ( 18.8–21.5 mm, SD = 1.54 mm, n = 3); (2) body slim ( SW/ SVL= 0.26, n = 12), long limbs ( TIBL/ SVL= 0.42–0.52 mm, SD= 0.025 mm, n=12); (3) apparent phalangeal formula of hand by external examination 1–2–3–3, basal finger webbing absent; (4) webbing formula of toes: I(0)–(0)II(0)–(0)III(0)–(2)IV(2)–(1) V; (5) snout subacuminate in dorsal view, distinctly protruding beyond lower jaw; (6) tympanic membrane and tympanic annulus not visible externally; (7) dorsal and lateral surfaces (except for anterior surfaces of thighs) bearing numerous greyish green coni; venter lacking coni except for ventrolateral surfaces of upper arms, chest, and lateral margin of throat; (8) males with minute keratinized spines on dorsal and lateral surfaces of the thumb; (9) vertebral neural processes not visible externally; (10) in life, dorsum olive green with red spots surrounded by dark green circles; lateral surfaces of the dorsum yellowish green with red spots; arms and legs with smaller red spots and greyish white coni (in preservative, dorsum dark green with greyish yellow coni where the red spots used to be); (11) in life, ventral coloration bright red (pink to pink reddish in preservative) along the jaws, and covering hand and feet palms, and extending from the seat patch to the lower belly (in some specimens the coloration covers all venter) and armpits; ventral parts otherwise covered with white to cream blotches on a dark background (in some specimens, throat covered by orange spots on a light green background) ( Fig. 3A, 3B).   Diagnosis.  Atelopus moropukaqumiris readily distinguished from all its congeners by the combination of small size, numerous greyish-green coni covering dorsal and lateral body surfaces, and coloration consisting of dark olive green dorsum interspersed with numerous red spots ( Fig. 4A), and pelvic and ventral surfaces of hands and feet red ( Fig. 4B). Eleven described species of Peruvian  Atelopushave part of the venter and ventral surfaces of the hands and feet reddish or pinkish:  A. andinusRivero;  A. dimorphusLötters;  A. erythropusBoulenger;  A. loettersiDe la Riva, Castroviejo-Fisher, Chaparro, Boistel & Padial;  A. oxapampaeLehr, Lötters & Lundberg;  A. pulcherBoulenger;  A. reticulatusLötters, Haas, Schick & Böhme;  A. siranusLötters & Henzl;  A. seminiferusCope;  A. spumariusCope(actually a species complex; Lötters et al.2002); and  A. tricolorBoulenger; also, two undescribed taxa have the same red or pink coloration of the venter and ventral surfaces of the hands and feet:  Atelopussp. 10 and  Atelopussp. 11, as listed by Rueda-Almonacid et al.(2005). In six of these species, males are distinctly larger than in  A. moropukaqumir(SVL 19.9–21.6 mm):  A. andinus(SVL 26.4–27.5 mm),  A. loettersi(SVL 24.7–26.7 mm),  A. pulcher(SVL 25.2–29.3 mm),  A. seminiferus(SVL 33.8–35.2 mm),  A. siranus(SVL 22.5 and 23.5 mmin the only known male specimens), and  Atelopussp. 10 (SVL between 40 and 50 mm, according to Rueda-Almonacid et al. 2005). Furthermore,  A. andinus,  A. loettersiand  A. pulcherhave a dark brown or black dorsum with irregular green or greenish-yellow dorsal and dorsolateral markings (red spots on a green background in  A. moropukaqumir);  A. loettersiand  A. pulcherare smooth dorsally and laterally (  A. moropukaqumirbears numerous coni dorsally and laterally).   Atelopus siranusand  A. seminiferushave a black dorsum with minute yellow spots (  A. seminiferus) or yellow marks (  A. siranus), and their skin lack coni;  Atelopussp. 10 has a broad, cream dorsolateral stripe (absent in  A. moropukaqumir), and smooth skin. The snout-vent length in males of eight species is similar to that of  A. moropukaqumir(SVL 19.9–21.6 mm):  A. dimorphus(SVL 21.6–24.9 mm),  A. erythropus(SVL 15.9–20.4 mm),  A. reticulatus(SVL 24.7 mmfor males),  A. spumarius sensu stricto, the smallest form within  A. spumarius sensu lato(SVL 19.3 mmin one male examined by Asquith & Altig, 1987),  Atelopus oxapampae(SLV 19.1–22.1 mm),  A. tricolor(SVL 20.4–27.0 mm), and  Atelopussp. 11 (SVL below 30 mm, according to Rueda-Almonacid et al., 2005). Of these eight species,  A. dimorphusand  A. siranuslack coni (present in  A. moropukaqumir), and their dorsum is uniformly yellow and black, respectively (green with red spots in  A. moropukaqumir).  Atelopus spumarius sensu latohas dorsum dark brown or black (dorsum green with red spots in  A. moropukaqumir) with green or yellow dorsal markings, dorsolateral lines often interrupted by annuli (no dorsolateral lines in  A. moropukaqumir), and smooth skin (skin with numerous coni in  A. moropukaqumir).  Atelopus reticulatushas a pale dorsolateral line and greenish or yellowish reticulations (no dorsolateral lines or reticulations in  A. moropukaqumir) and coni are absent.  Atelopussp. 11 has a pale dorsolateral stripe (no stripes in  A. moropukaqumir), dorsum uniformly dark brown (green with red spots in the new species), and dorsal skin in males slightly granular.  Atelopus oxapampaehas acuminate snout (subacuminate in  A. moropukaqumir), grey coni (green coni in  A. moropukaqumir) and the complete coloration in  A. oxapampaeconsisting of a narrow dark brown middorsal stripe, cream dorsolateral stripe, arms, and legs dark brown with grayish brown reticulation (no middorsal and dorsolateral stripes, general dorsal coloration in  A. moropukaqumirgreen with red spots and no reticulations).  Atelopus tricolorhas a broad, yellowish mustard colored dorsolateral line accompanied by irregular dorsal markings (no dorsolateral line and dorsal markings absent in  A. moropukaqumir).  Atelopus pulcherand  A. spumarius sensu latopossess tympanic membranes, and tympanic annuli (absent in  A. moropukaqumir).   FIGURE 3.Dorsal (A) and ventral (B) views of preserved male holotype of  Atelopus moropukaqumir(MUSM 40370), SVL: 20.7 mm. Photos by S. Riva-Regalado.   FIGURE 4.Lateral (A) and ventral view (B) of holotype (MUSM 40370) of  Atelopus moropukaqumirin life. Photos by V. Díaz Vargas.   Atelopus moropukaqumiris most similar to  A. erythropus, known only from the holotypeBMNH 1947.2.14.65, presumably male (see photograph of holotypein Lötters 2003: 174). The two species differ in snout shape, skin texture and coloration (in parenthesis for  A. moropukaqumir): snout shape “blunt” (subacuminate), tiny spiculae only, skin appears to be smooth as seen in Fig. 5in Lötters & la Riva 1998; Fig. 4in Lötters 2003(dorsal skin of males bearing coni), and coloration in preservative brown dorsally and white beneath, with lower surface of thighs and feet vermilion ( Boulenger 1903: 555) (coloration in preservative dorsally dark olive-green covered by white spots, pink on seat patch, lower belly, axillae, feet, and hands). The morphological comparison between  A.cf. erythropusfrom Manu ( Catenazzi et al. 2013), the specimens photographs from Megantoni ( Rodriguez & Catenazzi 2005), both in Cusco, and  A. moropukaqumirreveal consistent differences: conspicuous coni in  A.cf. erythropus(small coni in  A. moropukaqumir), longer head in  A.cf. erythropuswith HLEX/SVL= 0.82, n = 5 (HLEX/SVL= 0.69, n = 12 in  A. moropukaqumir), bigger size in females of  A.cf. erythropus, up to SVL= 28.1 mm(SVL= 18.8–21.5, n = 3 mmin females of  A. moropukaqumir), presence of a whitish labial stripe (absent in  A. moropukaqumir) and red irregular blotches on dorsal surfaces in  A.cf. erythropus(well-defined spots in  A. moropukaqumir), yellow greenish coloration on ventral surfaces with red coloration on seat patch, hands, feet, jaws, throat and superior part of the chest in  A.cf. erythropus(bright red along the jaws, and covering hand and feet palms, and extending from the seat patch to the lower or all belly and armpits; ventral parts otherwise covered with white to cream blotches on a dark background or throat covered by orange spots on a light green background in  A. moropukaqumir).   Atelopus moropukaqumirand  A. erythropusappear to be restricted to high elevation cloud forests on the eastern slopes of the Andes, but these forests do not occur continuously along the Andean cordillera. An important biogeographic barrier, the canyon of the ApurimacRiver ( Hazzi et al. 2018) and associated dry forest ecosystem, causes a deep incision to the Andean cordillera, interrupting the cloud forest between Ayacuchoand Cusco. This barrier likely interrupts gene flow for high-elevation amphibians adapted to cold and moist environments ( Lehr & Catenazzi 2008), as seen in many other amphibian lineages. For instance, the distribution of  Boana palaestesis restricted to two localities in the Department of Ayacucho( Duellman et al. 1997) and this species has not been found south of the canyon of the River Apurimacin Cusco, where its sister species and ecologically similar  B. gladiatoroccurs ( Köhler et al. 2010). The same pattern is seen in genera of Holoadeninae, with  Phrynopusrestricted to cordilleras north and west of the canyon of the ApurimacRiver, and  Bryophryne,  Microkayla,  Psychrophrynellaand Qosqophrynerestricted to the Amazonian slopes of the Cordillera Oriental of Cuscoand Punosouth and east of the Apurimaccanyon. Furthermore,  Hyloscirtus armatusand  A. tricolor, two stream-breeding frogs syntopic with  A. erythropus, occur only south and east of the Apurimaccanyon ( Rueda-Almonacid et al.2005and Stuart et al.2008). Therefore, it is likely that the distribution of  A. moropukaqumiris similarly restricted to the north-west of the Apurimaccanyon. The type locality of  A. erythropusis Santo Domingo, in the Cordillera de Carabaya in Departamento de Punoat 6000 feet[= 1800 ma.s.l.]. Specimens collected in the Departament of Cusco, in Manu National Park and Megantoni National Sanctuary, display similarities with  A. erythropus, but the identification will remain uncertain until new specimens, photographs and gene sequences from the type locality become available. Records of  A. erythropusfrom other regions ( Rueda-Almonacid et al.2005, Marent 2008, and Stuart et al.2008) are likely incorrect. For example, Rodríguez et al.1993, suggest the species might be present at lower elevations in Ucayaliand Huánuco, but there are no vouchered specimens supporting these records. Consequently, we restrict  A. erythropusto the population (and holotype) known from the type locality at 1800 ma.s.l. in Puno. Assuming the putative records from Cusco, ranging in elevation from 1900–2200 ma.s.l., belong to  A. erythropus, the distribution of  A. erythropus‘sensu lato’ would be limited to an area ~ 320 kmlong from Megantoni National Sanctuary ( Cusco) to Santo Domingo ( Puno), in cloud forests of the eastern slopes of the Andes from 1800–2200 ma.s.l. Therefore, even after pooling all populations of  A.cf. erythropusfrom Cusco, the distribution range of  A. erythropussuggests that the Apurimaccanyon is an important barrier to the movement of these high elevation species.   Description of holotype.( Figs. 3–5) Adult male. Body slim (SW/SVL= 0.25), head longer than wide (HSLQ/ HDWD = 1.22), snout subacuminate in dorsal view, with tip of snout distinctly protuberant from anterior margin of jaw. Nostrils slightly protuberant anteriorly, directed laterally, not visible from above, situated anterior to level of apex of lower jaw. Canthus rostralis distinct and covered with coni, convex from tip of snout to nostril, nearly straight from nostril to eye; loreal region slightly concave; lips not flared. Interorbital and occipital regions flat, rostral area concave, all bearing coni; eyelid flared bearing coni; postorbital crests slightly raised, narrow; tympanic membrane and tympanic annulus not visible externally. Tympanic area covered with coni. Choanae small, rounded, widely separated, concealed by palatal shelf of maxillae; tongue about 3.33 as long as wide, its posterior two-thirds not attached to the mouth’s floor; ostia pharyngeal and vocal slits absent. Forearm relatively short (RDUL/SVL = 0.28), 1.3 times as thick proximally as distally; nuptial pad on dorsal and outer surfaces of thumb consisting of minute keratinized spines, without magnification barely distinguishable from black pigmentation of thumb; palmar and subarticular tubercles distinct; digital tips with round pads; thumb short (THBL/HAND = 0.29), apparently having one phalange; basal webbing on fingers absent, fingers lacking lateral fringes; relative length of fingers I <II <IV <III ( Fig. 5A). Tibia long (TIBL/SVL = 0.50); fold on distal half of inner edge of tarsus absent; inner metatarsal tubercle indistinct; outer metatarsal tubercle conical, low raised; supernumerary plantar and subarticular tubercles indistinct; digital pads distinct; webbing formula of toes I(0)–(0)II(0)–(0)III(0)–(2)IV(2)–(1)V; relative lengths of toes I <II <III <V <IV ( Fig. 5B). Vertebral neural processes not protruding under dorsal skin; dorsal and lateral surfaces (except for anterior surfaces of thighs) bearing numerous grey coni; skin of throat, chest, and belly smooth; venter lacking coni except for ventrolateral surfaces on upper arms, chest and posterior margin of throat; cloacal opening slightly above midlevel of thighs, directed laterally; skin lateral to cloacal bearing coni.  Variation in measurements.Meristic variation for males, females, and juveniles paratypesare given in Table 1.   TABLE 1.Measurements (mm) of  Atelopus moropukaqumir: holotype male MUSM 40370 (in bold); paratypes: males MUSM 40368–40370, females MUSM 40365, 40378, and juveniles MUSM 40374, 40377) paratypes.    Character  MUSM 40370 MUSM 40368 MUSM 40369 MUSM 40365 MUSM 40378 MUSM 40377 MUSM 40374  SEX /AGE  Male Male Male Female Female Juvenile Juvenile  SVL  21.6 20.0 21.3 21.1 21.5 15.3 13.5  TIBL  10.7 9.9 10.4 10.1 10.4 7.9 5.7  FOOT  9.3 9.0 9.1 9.3 9.5 5.6 5.1  HLSQ  7.2 5.5 5.3 5.4 6.9 4.7 5.0  ITOR  2.3 2.4 2.3 2.8 2.7 1.9 1.6  HDWD 5.9 5.8 6.0 6.0 6.2 4.8 4.4  EYDM  2.1 2.1 2.1 2.1 2.4 1.9 1.4  EYNO  1.7 1.8 1.8 1.9 2.0 1.7 1.4  ITNA  2.4 2.3 2.5 2.8 2.5 2.2 1.8  RDUL  6.1 5.9 5.9 6.0 6.2 4.7 3.9  HAND  5.4 4.9 5.4 6.0 5.3 4.1 2.8  THBL  1.6 1.7 1.7 1.8 2.6 1.0 0.9  HLEX  7.1 6.8 7.0 6.8 7.7 5.0 4.8  SW  16.5 5.0 5.7 5.9 5.2 4.1 3.1  Coloration of holotypein preservative.Dorsum and dorsolateral areas dark green with greyish coni (red spots appear pink in preservative); venter covered with cream blotches on a black background; hand palms, feet palms, axillae and seat patch pink reddish; throat cream yellowish on a pale green background ( Fig. 3).  Coloration of holotypein life.Dorsum olive green with red spots surrounded by dark green circles, red spots on arms, legs and dorsolateral areas smaller than on dorsum; ventral coloration bright red along jaws, and covering hands palms, feet palms, seat patch and axillae; ventral surfaces otherwise covered with white to cream blotches on a black background. Throat covered with orange spots on a light green background ( Fig. 4).  Tadpoles.Unknown.   Distribution and natural history.  Atelopus moropukaqumiris only known from the typelocality (~ 4 km 2) in a montane forest from 2040–2110 ma.s.l. in the valley of a tributary of Río Apurímac(Provincia de La Mar), in Departament of Ayacucho. We first found the species on 19 November 2018at 20:00, during night surveys. We found frogs among wet rocks in a small stream ( Figure 6). Most frogs were jumping away from the stream and towards the forest as we approached them.   FIGURE 5.Ventral views of hands (A) and foot (B) of the holotype (MUSM 40370) of  Atelopus moropukaqumir. Photos by E. Castillo Urbina.   FIGURE 6.Microhabitat (small streams) of  Atelopus moropukaqumirat the type locality in Department of Ayacucho, Peru. Photo by V. Díaz Vargas. We found ten frogs (10) at the typelocality, two of them under a rock in contact with water of the stream, and two (MUSM 40366, 40367) perched on leaves 0.3 mabove the stream. Male MUSM 40369 was calling prior to capture, but we could not record the call. Syntopic species at the typelocality include  Pristimantis rhabdolaemus,  P. bromeliaceus,  Oreobatessp. and  Hyalinobatrachiumsp. We detected the presence of the pathogenic fungus  Batrachochytrium dendrobatidisin 15% of sampled individuals of  A. moropukaqumir(n=13). Infection loads in the two infected individuals were 4.2 and 7.3 zoospore equivalents (ZE). These values are low but confirm the presence of Bd in this population ( Catenazzi et al.2011, 2014). Furthermore, a larger analysis including all frogs sampled from 2000–2200 m(and including the specimens of  A. moropukaqumir) estimates prevalence at ~7% (n = 61), with none of four infected individuals exceeding the value of 7.3 ZE. These values are much lower than values observed in other montane forests in southern Peru, and values of animals displaying symptoms of chytridiomycosis ( Catenazzi et al.2011, 2014, 2017). Although Bd prevalence and abundance at the typelocality of  A. moropukaqumirare not indicative of an ongoing epizootic, species in the genus  Atelopusare highly susceptible to chytridiomycosis, and mass mortalities events have been observed in Peru( Venegas et al.2008). In addition to the threat of chytridiomycosis, forests surrounding the typelocality are being rapidly cleared for agriculture ( Fig. 7).   FIGURE 7.Habitat surroundings of the type locality of  Atelopus moropukaqumirin the Department of Ayacucho, Peru. Photo by M. Jaico. See habitat degradation along the river.  Conservation status.We suggest that  A. moropukaqumirshould be listed as Critically Endangered under criteria B2a,b of the IUCN Red List because 1) a single population is known; 2) the single locality lies outside of any protected natural area, and there is ongoing habitat degradation caused by forest clearing and agriculture ( Fig. 7); and 3) the fungal pathogen  Batrachochytrium dendrobatidis(Bd), which is a known cause of population extirpations for harlequin frogs, is present at this locality (see natural history paragraph). Future studies should investigate whether  A. moropukaqumiroccurs in other valleys in Department Ayacucho.   Etymology.The specific name is a combination of adjectives in Quechua and refers to the dorsal coloration of the frogs, green frog with red spots, where moromeans spots, puka, red and q’umir, green. We chose a name combining words in Quechua to show the importance of the language of the Inca Empire, which is gradually being lost by Peruvian rural communities. 3032927302 2018-11-20 V V. Herrera & E. Castillo & M. Fernández & V. Díaz & J. Gamboa Peru Provincia La Mar 2039 -12.983334 Anchihuay 1291 -73.666664 Distrito de Anco 4 408 MUSM 40370 1 Ayacucho holotype 3032927304 [448,1041,1770,1797] 2018-11-20 MUSM V. Herrera & E. Castillo & M. Fernández & V. Díaz & J. Gamboa Peru Provincia La Mar 2039 -12.983334 Anchihuay 1291 -73.666664 Distrito de Anco 4 408 MUSM 40364-69, 40371 1 Ayacucho paratype 3032927303 MUSM Castillo & M. Fernandez Peru 4 408 MUSM 40376-78 1 Ayacucho paratype 3032927301 [634,1087,1806,1833] 2019-06-13 V J. Gamboa Peru Diaz 4 408 1 Ayacucho paratype