Atelopus nocturnus, Bravo-Valencia, Laura & Rivera-Correa, Mauricio, 2011

Bravo-Valencia, Laura & Rivera-Correa, Mauricio, 2011, A new species of harlequin frog (Bufonidae: Atelopus) with an unusual behavior from Andes of Colombia, Zootaxa 3045, pp. 57-67 : 58-65

Atelopus nocturnus , sp. nov.

( Figures 1–6 )

Holotype. MHUA 5280, adult female, from Reserva Natural “Arrierito Antioqueño” (06 58.842 N, 75 0 6.738 W), quebrada El Oso, vereda El Roble, municipio de Anorí, Departamento de Antioquia, Colombia, 1670 m elevation, collected by Laura Bravo-Valencia, Claudia Molina and Natalia Silva on 15 February 2007.

Paratopotypes. MHUA 5279, same data as holotype. MHUA 5281, 5282 (cleared-and-stained preparation), 5283-84, 5286, adult males, and MHUA 5285, adult female, all obtained from type locality by Laura Bravo-Valencia and Claudia Molina on July 2007.

Paratypes. MHUA 2472, adult male, from Bosque El Chaquiral (0659’N, 7507’W), vereda El Retiro, municipio de Anorí, Departamento de Antioquia, Colombia, 1875 m elevation, collected by Jenny Urbina and Sandra Galeano on 12 February 2003.

Diagnosis. This species described here is assigned to Atelopus because it has the combination of characters diagnostic of the genus (sensu McDiarmid 1971, Lynch 1993, Lötters 1996): head usually longer than broad, with the snout strongly acuminate from above and typically acute in lateral view, the lateral nares are close to the tip of the snout, an external tympanum absent, a prominent supratympanic crest present, first digit of the hand is reduced, evident sexual dimorphism in size and color, axillary amplexus, arboreal habits and individuals associated with streams. In addition, to lack the terminal phalange in the thumb (observed in the specimen cleared-and-stained, MHUA 5282). Atelopus nocturnus ( Fig. 1 , 2 A), is a harlequin frog distinguished from other species of Atelopus by the following combination of characters: (1) A moderate-sized species (SVL in females 33.0–34.3, n = 3; males 20.1–25.0, n =6); (2) hind limbs short (TL/SVL = 0.40–0.43, n = 9); (3) phalangeal formula of hand 1–2–3–3, basal webbing present; (4) foot webbing formula I (0- – 0) — (0+ – 1-) II (0- – 0) — (1 1/2–1 3/4) III (0 – 0+) — (2 – 3-) IV (2 – 3-) — (0 – 0+) V; (5) snout acuminate, protruding beyond lower jaw; (6) tympanic membrane, tympanic annulus and stapes absent; (7) dorsal surfaces of body bear a few scattered small warts and spiculae; (8) white coni over warts (cream in preservative) present on arm and postocular region; (9) postocular crest and vertebral neural processes conspicuous; (10) dorsum dark reddish brown to orange-brown on the flank surfaces in females, dorsum and flank surfaces dark brown in males; (11) venter uniform bright orange in females (cream in preservative) and white to cream in males with dark brown irregular stripes and blotches; (12) throat and ventral region smooth in females, and skin below vent areolate in males; (13) palmar hand and plantar foot dark orange in females and light orange in males; (14) iris bright yellow with fine reticulation and spots in brown and black.

Comparison with congeneric species. The diagnostic characters readily distinguish Atelopus nocturnus from the all described Atelopus species. We compare with some similar species and other species with relatively close geographical distribution (in spite of micro-endemism known in the genus). Atelopus carauta differs from the new species by adult size is significantly larger, in having canthus rostralis and postocular crest yellowish, tubercles on flanks and thighs and belly yellow ( Ruiz-Carranza and Hernández-Camacho 1978). Atelopus chocoensis differs from the A. nocturnus by being larger, having snout more projected, postocular crest more developed, dorsum green-brown, cream yellow flanks with brown spots and belly yellow cream in females (Lötters 1992, Lötters 2005). Atelopus galactogaster is different from the new species by larger size, having a slate gray, green-black dorsal coloration, smooth flank lacking spiculae and coni, chest and belly immaculate white uniform except for a small black spot on the throat and a brown on the chest ( Rivero and Serna 1993). Atelopus famelicus is distinguished from A. nocturnus by having a more slender body, presence of dorsolateral stripes and absence to spiculae and coni ( Rivero and Morales 1995). Atelopus lynchi differs from A. nocturnus by having less project snout, presence of spots yellowish gray on the canthus rostralis and postocular crest, flanks very smooth, and belly bluish gray ( Cannatella 1981). Atelopus quimbaya is distinguished from the new taxon by having a dorsal surface grey and/or grey greenish with flecks, reticulate or lines brown and eventually yellow spots, a less projected snout, inconspicuous vertebral neural processes, a dark brown venter with yellows marks ( Ruiz-Carranza and Osorno-Muñoz 1994). Atelopus monohernandezii differs from A. nocturnus by having smooth dorsal surfaces on the head and body, presenting big warts in the flank surfaces and a brown-reddish venter color (Ardila-Robayo et al. 2002). Atelopus nicefori is distinguished from the new species by having a less developed postocular crest, green-yellowish flanks, a dark green or pink-brown dorsum, venter yellow-orange with brown markings on the throat and a green-yellowish palm hand and plantar foot ( Rivero 1963). Atelopus sanjosei is distinguished from the new taxon by a less projected snout, a smooth dorsal surface, green dorsum with brown marks in reticulate form and a white or yellow venter occasionally with a few small brown blotches ( Rivero and Serna 1989). Atelopus sernai differs from A. nocturnus in having a shorter snout, inconspicuous vertebral neural processes, a brown dorsum with bright green blotches and plantar hand, palmar foot, arm, and thigh surfaces yellowish ( Ruiz-Carranza and Osorno-Muñoz 1994). Atelopus simulatus differs from the new species by having inconspicuous vertebral neural processes, smooth dorsal head surface, dorsum reticulate green and venter yellowish green with brown blotches (Ruiz-Carranza and Osorno- Muñoz 1994). Atelopus sonsonensis differs from the new taxon by having a shorter snout, a blue-green with brown reticulate flanks in males, tibio-fibula length relatively longer and a cloacal opening at midlevel of the thighs (Vélez-Rodríguez and Ruiz-Carranza 1997).

Description of holotype. Head longer than wide, head width less than one third SVL (HDWD/SVL = 0.28); snout acuminate in dorsal view, slightly depressed; in lateral view, profile of tip of snout to the anterior margin of jaw curved and remarkably protuberant ( Fig. 1 ); nostrils slightly protuberant, directed laterally, situated at posterior of apex of lower jaw; canthus rostralis distinct, slightly concave from eye to nostril; loreal region concave; lips not flared; interorbital region flat, smooth; eyelid without distinct tubercles; postorbital crest present and conspicuous; tympanic areas covered with warts and coni; tympanic membrane and tympanic annulus absent ( Fig. 2 ); temporal area smooth; choanae small, elliptic, widely separated; vomerine teeth absent; tongue three times longer than wide, broadest posteriorly, free for half its length posteriorly, proximal end of tongue lacking pigmentation. Forearm relatively short (FAL/SVL = 0.31); palmar tubercle round; supernumerary palmar tubercles indistinct; thenar and subarticular tubercles distinct; digital tips with round pads; thumb relatively short (THBL/HAND = 0.32), having one phalange; webbing on hands basal, fingers lacking lateral fringes; relative length of fingers III>IV>II>I ( Fig. 3 ). Tibia relatively short (TIBL/SVL = 0.42); fold on distal half of inner edge of tarsus present; inner metatarsal tubercle oval; outer metatarsal tubercle round, raised, about two thirds length of inner metatarsal tubercle; supernumerary plantar tubercles inconspicuous and subarticular tubercles conspicuous; digital pads distinct; webbing formula of foot I 0- — 0+ II 0-— 1 1/ 2 III 0 — 3 - IV 3 — 0 V; relative length of toes IV>V> III> II> I. Lateral postocular surfaces bearing numerous warts with coni; undersides of arms tubercled; dorsal surfaces smooth with conspicuous vertebral neural processes and scattered warts and spiculae increasing in number toward arms and anterior and proximal upper surfaces of forelimbs, bearing numerous spiculae evenly distributed; throat, chest, belly, undersides of hind limbs smooth and free of warts; cloacae opens as an inconspicuous tube above the thighs, directed posteriorly; warts present lateral to cloacal opening.

Coloration in life. Dorsal surface of head and body dark reddish brown, upper surface of flanks brown to orange; warts with coni cream; throat, chest, belly, and ventral surfaces of limbs bright orange; fingers I and toes I and II pale yellow; palmar hand and plantar foot dark orange. Iris, bright yellow with spots brown and fine black reticulations.

Coloration in preservative. Dorsum dark brown; flank surfaces, dorsal surfaces of fingers I and toes I and II cream, tips of digits of hand and foot cream dorsally; throat, venter, palmar and plantar surfaces uniform cream, outer metatarsal tubercle cream.

Measurements of holotype. SVL: 33.0, HLQS: 11.9, HDWD: 9.1, SW: 8.4, IOED: 8.5, IOID: 3.1, EYDM: 3.8, EYNO: 2.6, ITND: 3.1, NSD: 2.5, HAND: 8.3, THBL: 2.8, FAL: 10.1, FL: 14.4, TIBL: 13.8, FOOT: 12.6 Variation. Morphometric variation is described in Table 1 . Females are larger than males; the forearm of males is swollen; and nuptial pads are evident covering dorsum of finger I in males ( Fig. 4 ). One female (MHUA 5279) differs in having more numerous warts on the dorsum of the body and the flanks; another female (MHUA 5285) presents more warts with coni in the postocular region. In two males (MHUA 5281, 5283), the snouts are acuminate in dorsal view and the tops are sloped anteroventrally in lateral view. In life, dorsal color vary from uniform pale brown (MHUA 5284, male) to reddish brown (MHUA 5285, female); females are bright orange ventrally, whereas in males it varies from white to yellowish cream and has marks and irregular dark brown stripes ( Fig. 6 ); palmar hand and plantar foot dark orange in females and light orange in males.

Etymology. The specific name comes from the Latin adjective nocturnus (of the night), in reference to the nocturnal activity of this species, an unusual and previously unknown behavior in other species of the genus Atelopus .

Geographic distribution and natural history. The new species is known only from the type locality in the northern Cordillera Central, Municipio de Anorí, Departamento de Antioquia, Colombia, ca.1670 meters above sea level. ( Fig. 5 ). The habitat of A. nocturnus is composed of remnant secondary very humid pre-montane forest with a high abundance of arboreal ferns, bromeliads and other epiphytes. The annual mean temperature varies from 18 to 24 ºC, with 4000 to 8000 mm of annual precipitation ( Gutiérrez-Cardenas 2002). All specimens were collected during unusual dry season (In the area the wet season occurs in May-October and November-April, however, the rains fall in July decreasing significantly). The individuals were found sitting on leaves of shrubs and ferns at a maximum height of one meter near a stream and active during night, except for an individual (MHUA 2472) was found by day while sleeping. The adult females had convoluted oviducts and small white ova, males possessed nuptial excrescences and one pair was found in amplexus (MHUA 5284 and MHUA 5285; Fig. 7 ), suggesting reproductive activity in dry season. Four additional juveniles were observed and not collected. Calling behavior and tadpole are currently unknown. Atelopus nocturnus was found sympatric with the following other anurans: Rheobates palmatus, Pristimantis penelopus, Centrolene antioquiense, C. savagei, Espadarana sp.

Remarks. Knowledge of the alpha-level taxonomy of Atelopus continues to increase with new species descriptions, additionally to new taxa potentially estimated (e.g. Lötters et al. 2002; Barrio-Sanz and Venegas 2005; Acosta-Galvis et al. 2006, Coloma et al. 2007, Lehr et al. 2008, Venegas et al. 2008). However, efforts to understand phylogenetic relationships among harlequin frogs remain little known, because they have been poorly explored ( Coloma et al. 2002, 2007), in spite of some molecular approaches (e.g. Noonan and Gaucher 2005, Guayasamin et al. 2010, Lötters et al. 2010, 2011). Several authors have suggested that it is premature to recognize species groups in the genus Atelopus (Vélez-Rodríguez and Ruiz-Carranza 1997; Coloma et al. 2002, 2007; Lötters et al. 2002) because of intra-individual and intraspecific variation detected in the lack of a terminal phalanx on the thumb, which defines it. Recently, Lötters et al. (2011) demonstrated that the proposed species groups based on frog-like versus toad-like overall appearance (i.e. longirostris and ignescens groups) or phalangeal reduction in the thumb (i.e. flavescens group) are not monophyletic, thus characters used to define them are not recovered as synapomorphies. For that reason, we prefer not to assign A. nocturnus to any particular phenetic group, until this species is included in a rigorous phylogenetic analysis.

Following the IUCN Red List categories and criteria (IUCN 2001), A. nocturnus should be categorized as Data Deficient (DD), because of the lack of studies on demography, genetic structure, or reproductive behavior. However, we believe that given the critical situation facing the genus (i.e. 62 species of the Andean Atelopus are Critically Endangered or possibly extinct, Stuart et al. 2008), it is necessary to have some estimate of the conservation status of all Colombian species. Atelopus nocturnus currently is known only from a range of less than 10 km 2, and a dozen individuals (in exhaustive searches for more than five years). Additionally, several threats are acting (e.g. habitat fragmentation and inundation by the Porce III-IV basin hydroelectric project near to the type locality) Thus, we recommend placing A. nocturnus in the category Critically Endangered (CR). We advocate urgent field surveys (including scientific collections of the larval, adults and tissues samples), for assessment of the unsolved taxonomic status of many species, and studies of risk to external harmful agents (i.e. assess presence of Batrachochytrium dendrobatidis ). Given this, it helps to refining the information on the conservation status of the harlequin frogs in the Andean region, and be possible to establish adequate conservation measures. With the aim of this species is recognized by the local community, we tentatively propose the common name sapo arlequín nocturno (nocturnal harlequin toad). We hope that contributions like this will motivate the government, environmental NGO's, owners of private nature reserves, to facilitate biodiversity studies and to reveal the real amphibian’s richness of Colombia.

Figures

FIGURE 1. Atelopus nocturnus sp. nov. (MHUA 5280, holotype; adult female in life, SVL = 33.0 mm). Photograph by L. Bravo-Valencia.

FIGURE 2. Lateral (left) and dorsal (right) aspects of the head of Atelopus nocturnus sp. nov. (MHUA 5280, holotype). Scale bar = 5 mm. Drawings by M. Rivera-Correa.

FIGURE 3. Hand (left) and foot (right) of Atelopus nocturnus sp. nov. (MHUA 5280, holotype). Scale bar = 5 mm. Drawings by M. Rivera-Correa.

FIGURE 4. Arrow indicating nuptial excrescences (keratinous spines) on Finger I of the hand of an adult male Atelopus nocturnus sp. nov. (MHUA 5283, paratopotype). Photograph by M. Rivera-Correa.

FIGURE 5. Distributional map of Atelopus nocturnus sp. nov. in Colombia. Solid circles indicate type localities and the unique distribution current known for the new species.

FIGURE 6. Ven t ral color pattern v ariation of male Atelopus nocturnus sp. nov. Left to right: MHUA 2472 (SVL = 25.0 mm), MHUA 5281 (SVL = 22.5 mm), MHUA 5282 (SVL = 24.1 mm), MHUA 5283 (SVL = 20.1 mm), MHUA 5284 (SVL = 23.4 mm), MHUA 5286 (SVL = 24.2 mm). Photograph by M. Rivera-Correa.

FIGURE 7. Amplexus in Atelopus nocturnus sp. nov. (MHUA 5284, adult male paratopotype, SVL = 23.8; MHUA 5285 adult female paratopotype, SVL = 34.3 mm). Photograph by L. Bravo-Valencia.

Tables

TABLE 1. Variation in measurements (in mm) of the type series of Atelopus nocturnus sp. nov. See text for abbreviations.

Measurement (mm) SVL	Females (n=3) Mean SD 33.8 0.70	Max. 34.3	Min. 33.0	Males (n=6) Mean SD 23.4 1.69	Max. 25.0	Min. 20.2
HLQS HDWD	11.5 0.48 8.6 0.50	12.0 9.2	11.0 8.2	9.1 0.74 6.5 0.17	10.0 6.7	8.1 6.3
SW IOED IOID EYDMD EYNO ITND	8.1 0.25 8.2 0.55 3.1 0.15 3.2 0.52 2.7 0.06 3.0 0.23	8.4 8.6 3.3 3.8 2.8 3.1	8.0 7.8 3.0 2.8 2.7 2.7	6.6 0.32 6.5 0.29 2.5 0.20 2.5 0.20 2.1 0.21 2.2 0.15	7.0 6.8 2.8 2.8 2.5 2.5	6.1 6.0 2.2 2.4 1.9 2.1
NSD HAND THBL FAL	2.1 0.45 7.9 0.42 2.4 0.35 10.0 0.65	2.5 8.3 2.8 10.6	1.6 7.5 2.2 9.3	1.7 0.25 5.5 0.38 1.8 0.12 7.2 0.83	2.0 5.9 2.0 8.3	1.3 5.0 1.7 6.2
FL TIBL	14.4 0.09 13.6 0.17	14.4 13.8	14.3 13.5	10.1 0.51 9.8 0.70	11.0 10.7	9.6 8.7
FOOT	12.6 0.62	13.2	11.9	8.9 0.62	9.6	7.8