Atelopus moropukaqumir, Herrera-Alva & Díaz & Castillo & Rodolfo & Catenazzi, 2020

Herrera-Alva, Valia, Díaz, Vladimir, Castillo, Ernesto, Rodolfo, César & Catenazzi, Alessandro, 2020, A new species of Atelopus (Anura: Bufonidae) from southern Peru, Zootaxa 4853 (3), pp. 404-420 : 408-415

Atelopus 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 m a.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. Díaz and J. Gamboa on 20 November 2018.

Paratypes. Ten total: MUSM 40364–69 , 40371 same data as the holotype ; MUSM 40376–78 collected at the type locality by E. Castillo, M. Fernández , V. Díaz and J. Gamboa on 13 June 2019 .

Characterization. (1) A small species of Atelopus with a mean SVL of 20.6 mm in adult males (19.9–21.6 mm, SD = 0.55 mm, n = 9) and 20.5 mm in 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 moropukaqumir is 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 Atelopus have part of the venter and ventral surfaces of the hands and feet reddish or pinkish: A. andinus Rivero ; A. dimorphus Lötters ; A. erythropus Boulenger ; A. loettersi De la Riva, Castroviejo-Fisher, Chaparro, Boistel & Padial ; A. oxapampae Lehr, Lötters & Lundberg ; A. pulcher Boulenger ; A. reticulatus Lötters, Haas, Schick & Böhme ; A. siranus Lötters & Henzl ; A. seminiferus Cope ; A. spumarius Cope (actually a species complex; Lötters et al. 2002); and A. tricolor Boulenger ; also, two undescribed taxa have the same red or pink coloration of the venter and ventral surfaces of the hands and feet: Atelopus sp. 10 and Atelopus sp. 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 mm in the only known male specimens), and Atelopus sp. 10 (SVL between 40 and 50 mm, according to Rueda-Almonacid et al. 2005). Furthermore, A. andinus , A. loettersi and A. pulcher have 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. loettersi and A. pulcher are smooth dorsally and laterally ( A. moropukaqumir bears numerous coni dorsally and laterally).

Atelopus siranus and A. seminiferus have a black dorsum with minute yellow spots ( A. seminiferus ) or yellow marks ( A. siranus ), and their skin lack coni; Atelopus sp. 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 mm for males), A. spumarius sensu stricto, the smallest form within A. spumarius sensu lato (SVL 19.3 mm in one male examined by Asquith & Altig, 1987), Atelopus oxapampae (SLV 19.1–22.1 mm), A. tricolor (SVL 20.4–27.0 mm), and Atelopus sp. 11 (SVL below 30 mm, according to Rueda-Almonacid et al., 2005). Of these eight species, A. dimorphus and A. siranus lack coni (present in A. moropukaqumir ), and their dorsum is uniformly yellow and black, respectively (green with red spots in A. moropukaqumir ). Atelopus spumarius sensu lato has 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 reticulatus has a pale dorsolateral line and greenish or yellowish reticulations (no dorsolateral lines or reticulations in A. moropukaqumir ) and coni are absent. Atelopus sp. 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 oxapampae has acuminate snout (subacuminate in A. moropukaqumir ), grey coni (green coni in A. moropukaqumir ) and the complete coloration in A. oxapampae consisting 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. moropukaqumir green with red spots and no reticulations). Atelopus tricolor has a broad, yellowish mustard colored dorsolateral line accompanied by irregular dorsal markings (no dorsolateral line and dorsal markings absent in A. moropukaqumir ). Atelopus pulcher and A. spumarius sensu lato possess tympanic membranes, and tympanic annuli (absent in A. moropukaqumir ).

Atelopus moropukaqumir is most similar to A. erythropus , known only from the holotype BMNH 1947.2.14.65, presumably male (see photograph of holotype in 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. 5 in Lötters & la Riva 1998; Fig. 4 in 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. erythropus from Manu ( Catenazzi et al. 2013), the specimens photographs from Megantoni ( Rodriguez & Catenazzi 2005), both in Cusco, and A. moropukaqumir reveal consistent differences: conspicuous coni in A. cf. erythropus (small coni in A. moropukaqumir ), longer head in A. cf. erythropus with 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 mm in 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 moropukaqumir and A. erythropus appear 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 Apurimac River ( Hazzi et al. 2018) and associated dry forest ecosystem, causes a deep incision to the Andean cordillera, interrupting the cloud forest between Ayacucho and 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 palaestes is 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 Apurimac in Cusco, where its sister species and ecologically similar B. gladiator occurs ( Köhler et al. 2010). The same pattern is seen in genera of Holoadeninae , with Phrynopus restricted to cordilleras north and west of the canyon of the Apurimac River, and Bryophryne , Microkayla , Psychrophrynella and Qosqophryne restricted to the Amazonian slopes of the Cordillera Oriental of Cusco and Puno south and east of the Apurimac canyon. Furthermore, Hyloscirtus armatus and A. tricolor , two stream-breeding frogs syntopic with A. erythropus , occur only south and east of the Apurimac canyon ( Rueda-Almonacid et al. 2005 and Stuart et al. 2008). Therefore, it is likely that the distribution of A. moropukaqumir is similarly restricted to the north-west of the Apurimac canyon.

The type locality of A. erythropus is Santo Domingo, in the Cordillera de Carabaya in Departamento de Puno at 6000 feet [= 1800 m a.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. erythropus from 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 Ucayali and Huánuco, but there are no vouchered specimens supporting these records. Consequently, we restrict A. erythropus to the population (and holotype) known from the type locality at 1800 m a.s.l. in Puno. Assuming the putative records from Cusco, ranging in elevation from 1900–2200 m a.s.l., belong to A. erythropus , the distribution of A. erythropus ‘sensu lato’ would be limited to an area ~ 320 km long from Megantoni National Sanctuary (Cusco) to Santo Domingo (Puno), in cloud forests of the eastern slopes of the Andes from 1800–2200 m a.s.l. Therefore, even after pooling all populations of A. cf. erythropus from Cusco, the distribution range of A. erythropus suggests that the Apurimac canyon 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 paratypes are given in Table 1.

Coloration of holotype in 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 holotype in 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 moropukaqumir is only known from the type locality (~ 4 km 2) in a montane forest from 2040–2110 m a.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 2018 at 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.

We found ten frogs (10) at the type locality, two of them under a rock in contact with water of the stream, and two (MUSM 40366, 40367) perched on leaves 0.3 m above the stream. Male MUSM 40369 was calling prior to capture, but we could not record the call. Syntopic species at the type locality include Pristimantis rhabdolaemus , P. bromeliaceus , Oreobates sp. and Hyalinobatrachium sp. We detected the presence of the pathogenic fungus Batrachochytrium dendrobatidis in 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 type locality of A. moropukaqumir are not indicative of an ongoing epizootic, species in the genus Atelopus are 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 type locality are being rapidly cleared for agriculture ( Fig. 7 ).

Conservation status. We suggest that A. moropukaqumir should 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. moropukaqumir occurs 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 moro means 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.

Figures

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 moropukaqumir in life. Photos by V. Díaz Vargas.

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 moropukaqumir at the type locality in Department of Ayacucho, Peru. Photo by V. Díaz Vargas.

FIGURE 7. Habitat surroundings of the type locality of Atelopus moropukaqumir in the Department of Ayacucho, Peru. Photo by M. Jaico. See habitat degradation along the river.