Aromobates ericksonae, Barrio-Amorós, César Luis & Santos, Juan Carlos, 2012

Barrio-Amorós, César Luis & Santos, Juan Carlos, 2012, A phylogeny for Aromobates (Anura: Dendrobatidae) with description of three new species from the Andes of Venezuela, taxonomic comments on Aromobates saltuensis, A. inflexus, and notes on the conservation status of the genus, Zootaxa 3422, pp. 1-31 : 12-16

Aromobates ericksonae sp. nov.

Holotype. CVULA 8309, an adult male from Los Ranchos, Santa Cruz de Mora, Estado Mérida, Venezuela (8.3989 N, 71.6801 W), elevation 1193 m, collected by the authors on June 1st, 2007.

Paratopotypes. Five adult males CVULA 8299, 8308, and 8310-12; and seven adult females CVULA 8300- 0 4, and 8313-14. All specimens with the same information as the holotype; with the exception of CVULA 8299- 304 that were collected by E. Arrieta on December 2003.

Referred specimens. CVULA 8305-07, from Santa Cruz de Mora via Los Ranchos, Estado Mérida, Ve n ez u - ela (8.4265 N, 71.6281 W), 937 m, collected by the authors on June 1st, 2007. CVULA 7180, from Río Frío, Municipio Córdoba, northwestern slope of the Cordillera de Mérida, Estado Mérida, Venezuela (8.8500 N, 71.2833 W), 676 m. CVULA 7344 from Cascada La Palmita, in the way from La Azulita to Santa Elena de Arenales, Estado Mérida, Venezuela (8.7333 N, 71.4333 W), 910 m; CVULA 8379-82 from Olinda, Estado Mérida, Venezuela (8.7373 N, 71.4681 W), 800 m.

Tadpoles. Unknown.

Definition: We assigned this species to Aromobates based on its phylogenetic position ( Figs. 1 and 2 ), the combination of the molecular synapomorphies ( Table 2 ), and the following characters. (1) Skin on dorsum smooth. (2) Paired dorsal scutes present on digits. (3) Distal tubercle on FIV present. (4) FIV length reaches half distal subarticular tubercle of FIII. (5) FI longer than FII. (6) Digital discs present. (7) Finger discs barely expanded. (8) Fringes present on fingers. (9) Metacarpal ridge absent. (10) FIII not swollen in adult males. (11) Carpal pad absent. (12) Male excrescences on thumb absent. (13) Thenar tubercle present, small. (14) Black arm gland in adult males absent. (15) Tarsal keel thick, long, to mid-tarsus, straight. (16) Toe discs weakly expanded. (17) Toe webbing basal. (18) Metatarsal fold absent. (19) External coloration with pale dorsolateral stripes; ventrolateral stripe absent; oblique lateral stripe formed by a series of diffuse yellow and white spots. (20) Gular-chest markings present, from fine reticulation to diffuse spotting. (21) Dermal collar absent. (22) Male throat coloration white with profusion of melanophores to dirty white with dark brown reticulation or spotting; female throat coloration white with a profusion of melanophores to white few irregular reticulation or spotting. (23) Male abdomen color immaculate white. (24) Female abdomen color pattern immaculate white. (25) Iris coloration golden with black, fine reticulation; gold-colored pupil ring. (26) Large intestine unpigmented. (27) Enlarged white testes. (28) Median lingual process absent. (29) Tympanum indistinct, tympanic annulus absent. (30) Vocal sac distinct. (31) Teeth present on the maxillary arch. (32) Body size small, males (n = 8) 20.5–24.4 mm, mean = 21.9 ± 1.1; females (n = 8) 22.3–25.7 mm, mean = 24.2 ± 1.4.

Comparisons. Aromobates ericksonae (characters in parenthesis) differs by its smaller size from large species of the genus, such as A. alboguttatus , A. leopardalis , A. meridensis , A. nocturnus , and A. capurinensis , all with maximum SVL> 31 mm (up to 25.5 mm). The eight other species of Aromobates ( A. cannatellai sp. nov., A. duranti , A. haydeeae , A. mayorgai , A. molinarii , A. orostoma , A. saltuensis , and A. serranus ) are similar in size to Aromobates ericksonae . Aromobates cannatellai is somewhat larger, with females up to 28.6 mm (25.7) in SVL, finger discs moderately expanded (barely expanded), toe discs moderately expanded (weakly expanded), and more extensive toe webbing (basal). Aromobates duranti is a larger frog, up to 30.7 mm (up to 25.7 mm), with its venter gray with white dots (unicolor white without dots), and toe discs not expanded (expanded). Aromobates haydeeae has no fringes on fingers (present), tarsal fold ill-defined (well defined), dorsal color reddish copper (dark to light brown), and ventral parts orange (white). Aromobates mayorgai has dorsal skin smooth with a few tubercles posteriorly (smooth without tubercles in preservative), FI shorter than FII or equal (FI longer than FII), ventral parts yellow in females (white), dark in breeding males with a suffusion of small white spots (only the throat is dark, belly whitish), and oblique lateral stripe absent (formed by small whitish spots). Aromobates molinarii is the geographically closest species but it is a larger frog with females up to 30.3 mm (up to 25.7 mm), it has FII and II equal in length (FI longer than FII), fringes absent on fingers (present), tarsal keel ill-defined (straight and well-defined), toes moderately webbed (basally webbed), and oblique lateral stripe absent (formed by diffuse whitish spots). Aromobates orostoma has a distinct tympanum (indistinct), FI shorter than FII (FI longer than FII), and no fringes on fingers (present). Aromobates saltuensis has FI and FII equal in length (FI longer than FII), dorsal skin smooth with a few tubercles posteriorly (smooth without tubercles in preservative), and supratympanic bulge absent (ill-defined but present). Aromobates serranus has a distinct tympanum (indistinct), dorsum brown with blotches or reticulum (usually uniform, but not reticulated), and belly parts creamy white with brown reticulation (immaculate white).

Description of the holotype. The holotype is an adult male of 21.7 mm ( Fig 7 A): body slender, quadrangular in cross-section; dorsal skin, including dorsal surfaces of hind limbs, and smooth in preservative; ventral skin is smooth except on belly sides, where it is granular; its head is longer than wide, HeL = 37.7% of SVL; HW = 33.6% SVL; its snout is subacuminate in profile, inclined posteroventrally, rounded in dorsal and ventral view; its nares are situated laterally to the tip of snout; its narial openings are barely visible when viewing the head from the front, they are not visible from the dorsal side, and visible when viewing from the ventral aspect; its canthus rostralis is sloping, the loreal region is flat; interorbital region is little wider than the upper eyelid; snout longer than ED; tympanum is indistinct, only barely visible on its anteroventral portion, and concealed posterodorsally by a low supratympanic bulge formed by the superficial slip of m. depressor mandibulae; tympanum is positioned closely behind eye and lower, close to the angle of jaws; teeth present on maxillary arch; vocal slits large, arched from midlevel of tongue to anterior to the angles of jaws; tongue is short, oval, and half-free posteriorly.

Hand has a moderate size (27.6% SVL); relative lengths of adpressed fingers are III> I> II> IV; discs of all fingers are slightly expanded, horizontally oval; FIII disc is barely wider than distal end of adjacent phalanx; the base of palm has a large, rounded palmar tubercle; and on base of FI there is a smaller (approximately 1/3 of the palmar tubercle), oval thenar tubercle; one or two subarticular tubercles on fingers (one each on FI and FII, two each on FIII and FIV, the distal one of FIV inconspicuous); and all tubercles are flat and round or oval; without supernumerary tubercles. Fringes on fingers are low and indistinct on FI and FIII of right hand (well preserved), and very notable on all fingers of left hand except FI (somewhat dehydrated). However, we think that these differences are obviously due to preservation and consider them of somehow doubtful validity for taxonomy of Aromobates .

Hind limbs are of moderate length, SL = 51.1% of SVL; relative lengths of adpressed toes are IV> III> V> II> I; TI is moderately long, the tip reaching the mid-subarticular tubercle of TII; toe discs are moderately expanded, TIV about 1.8 times wider than distal end of adjacent phalanx; feet are basally webbed; fringes on toes are present but low; one to three are non-protuberant and small subarticular tubercles are present (one on TI and TII, two on TIII and TV, three on TIV, proximal one almost indistinct); two metatarsal tubercles are present, including a small oval outer, and a similar in size elongated inner tarsal tubercle; on right foot there is a mid-tarsal tubercle (lacking on left foot), this tubercle is double size of the two others; tarsal keel is well-defined, thick, straight, and transverse across tarsus, located from the proximal edge of inner metatarsal tubercle to mid-tarsus; cloacal opening is located at upper level of thighs, with a short tube flap or anal sheath.

Measurements of holotype (in mm). SVL: 21.7; SL: 11.1; FL: 10.8; HeL: 8.2; HW: 7.3; ETS: 3.5; EN: 2.2; ED: 3.1; TD: -; HD: 6.0; 1FiL: 3.5; 2FiL: 3.0.

Color. The specimen in life had its dorsum patternless dark brown except for the interorbital area where it was paler irregular with diffuse markings ( Fig. 7 A). Two golden cream dorsolateral stripes are present from the tip of snout through the canthus rostralis and over the eyelid to the sacral area. Flanks are blackish brown immediately inferior to the dorsolateral stripes, including the loreal region; flanks below the dark brown area present a pale grey coloration with a diffuse to whitish spotting. The oblique lateral stripe is evidenced by diffuse spots ranging from yellow at the inguinal zone to dirty white for the remaining of the stripe. The length of the oblique lateral stripe begins at the inguinal zone and ends at mid flank. The upper lips are dark grey with striking white irregular large spots. Arms are greyish brown, with a pale cream area on the upper insertion of the arm, and they have a diffuse dark brown longitudinal stripe on the anterior side of the arm. Fingers are uniformly grey. Hind limbs are pale brown in their dorsal side and ornamented with darker crossbars.

After preservation, the holotype presents some evident coloration changes. The dorsolateral stripes became strikingly white and the crossbars are clearly visible on both arms and hind limbs. On the ventral side, the specimen presents a dark brown reticulation on throat and chest while the belly remained white. Palms and plants are pale grey in coloration.

Variation. Preserved specimens appear to have smooth skin, while living animals have shagreen to granular dorsal and lateral skin ( Figure 7 C). Some color variation is evidenced on the granules of the thighs and some of them are white in coloration. The dorsal pattern observed in the holotype is similar as in three other males (CVULA 8299, 8311-12) though the pale dorsolateral stripes are much more evident on the holotype. Variation was observed and some males are paler (orange brown in life) dorsally, with less marked crossbars on the limbs (CVULA 8306, 8308, 8310 and 8305). On CVULA 8299, 8308 and 8311, the dorsolateral stripes are ill-defined. Females are slightly larger in SVL than males, with 6 of 8 specimens having a dark brown dorsal background with only one specimen (CVULA 8303) having well-defined dorsolateral stripes. All specimens have a oblique lateral stripe ranging from more or less defined to a ill-defined by a series of white spots ( Fig 7 A). A vocal sac is evident on the male CVULA 8299. Ventrally, the coloration of this species is sexually dimorphic. Breeding males usually have dark throats but a more whitish belly with some variation. For example, the holotype and CVULA 8299, 8311, and 8312 have their chins, throats, and chests strongly to diffusely reticulated, CVULA 8306 has a diffusely spotted throat, and CVULA 8305, 8308 and 8310 have dirty white coloration (with only a profusion of melanophores on the chin under magnification). Females also present some variation in their chin and throat coloration ranging from uniformly dirty white (CVULA 8313-14) or little spotted (CVULA 8300) to evidently irregular markings without reticulation as in CVULA 8303-04, 8301-02.

In life, the dorsal coloration can be dark brown to orange brown, and without pattern to one consisting of small dark brown spots with paravertebral distribution. The dorsolateral stripes can be white, pale yellow to orange ( Fig. 7 B). Ventrally, all specimens photographed are pale grey on the throat, immaculate white on the belly; the inguinal area, the thighs and shanks are pale yellow ( Fig. 7 D). The anal sheath is evident in the holotype and CVULA 8308, 8305, 8310, and 8299; but it is not evident in the males CVULA 8306, 8311-12. The anal sheath is also present in females except on CVULA 8301 and 8314. The anal sheath was found to be variable and most likely caused by preservation artifacts ( Grant et al., 2006).

Distribution and natural history. We found four populations of Aromobates ericksonae ( Fig. 3 ). The topotypic population is located on a deep creek outside the small village of Los Ranchos, with males calling from the leaf litter, and females in close proximity. However, the frogs were never seen directly in the creek, which suggest that this species is riparian. All individuals were active during the day. Several small tadpoles were seen but not captured in small pools in the creek. One juvenile of Scinax manriquei Barrio-Amoros, Chacon & Orellana, 2004 , was also seen in the same location.

Another close population of Aromobates ericksonae was discovered in a different habitat in the locality of Santa Cruz de Mora via Los Ranchos. This collection site is an open stream within a deciduous forest, where other species of dendrobatid are present ( Mannophryne collaris, Barrio-Amorós et al. 2010b ). The three individuals of A. ericksonae collected there were found on the forest floor or close to tree roots along the banks of a stream. Remarkably, these A. ericksonae were not as agile as Mannophryne and much easier to collect. Along the stream, several large individuals of fishing spiders ( Sparassidae ) were seen syntopically with both A. ericksonae and M. collaris . CBA has seen events of predation by these spiders on Mannophryne and they might also prey on Aromobates .

A third population of Aromobates ericksonae is present at the lower mountain forest along the road from La Azulita to Santa Elena de Arenales, where males can be heard from forests along the road from La Palmita to Olinda in rainy days. The fourth population of A. ericksonae is located around Río Frío and its based on a single specimen. At this locality, the individual was found in a secondary forest close to a mountain stream flowing to Río Frío and sympatric with Mannophryne urticans ( Barrio-Amorós et al. 2010b).

Vocalization. A single call was analyzed from a recording collected at 22.3 ºC (substrate temperature) and dusk on June 1st, 2007 at the type locality. It is a constant trill lasting for several minutes ( Fig. 8 A shows the waveform and 8A' the spectrogram). Seven consecutive notes were chosen at random from the spectrogram to determine spectral and temporal variables. The dominant frequency range is 3730.0 – 4314.0 Hz. Pulse rate was about one pulse per second. Note and inter-note duration with their mean, SD and range in seconds are indicated as follows (1) note duration, 0.20 ± 0.005 (0.20–0.21) and (2) inter-note, 1.08 ± 0.045 (1.05–1.16). Both, the waveform and the spectrogram are shown in Fig. 8 B and B'.

Phylogenetic relationships. The sister clade of Aromobates ericksonae is the saltuensis group composed by A. cannatellai and A. saltuensis . The distribution of A. ericksonae suggests that the last common ancestor radiated during rise of the modern Cordillera de Mérida during the Pliocene.

Etymology. Ericksonae is a patronym for Ronna Erickson, a research engineer and astronomer at the University of Massachusetts Amherst USA. She has greatly supported the field research of the senior author. The name of this species is used in genitive feminine.

Remarks. CVULA 5572 presents an abnormality on the right foot. Specifically, the TIV is shorter than normal, lacking the distal phalanx, but having otherwise an apparently normal disc. Abnormalities on limbs and digits have been observed in many species of Venezuelan dendrobatids (e.g. Mannophryne cordilleriana and M. riveroi , see Barrio-Amorós et al. 2010b, 2010c).

Figures

FIGURE 1. Maximum likelihood phylogenies of Aromobates, other dendrobatids, and closely related hyloids. The phylogenies were inferred using mitochondrial (12 S rRNA - tRNA Val- 16 S rRNA) and nuclear (POMC and NACA) genes. Nodal support based on 200 non-parametric bootstrap replicates and Bayesian posterior probabilities. Museum voucher numbers and GenBank accession numbers are provided.

FIGURE 2. Boostrap consensus of maximum parsimony trees of Aromobates, other dendrobatids, and closely related hyloids. The phylogenies were inferred using mitochondrial (12 S rRNA - tRNA Val- 16 S rRNA) and nuclear (POMC and NACA) genes.

FIGURE 3. Collection localities including type localities of Aromobates (squares) along the Cordillera de Mérida, Serranía de Perijá, and northern Eastern Cordillera of Colombia. Several species might be sympatric and syntopic.

FIGURE 7. Aromobates ericksonae sp. nov. (A) Male holotype, CVULA 8309. (B) Female paratopotype, CVULA 8310. (C) Dorsal view of CVULA 8310, showing skin texture. (D) Ventral view of CVULA 8310. Photos by CBA.

FIGURE 8. (A) Waveform and (A') spectrogram of a 60 seconds sequence of the trill call of Aromobates ericksonae sp. nov. Indistinct harmonics can be seen at around 6700 Hz. (B) Waveform and (B') spectrogram of a 10 seconds sequence of the trill call of Aromobates ericksonae sp. nov., showing seven notes; harmonics can be seen at around 6700 Hz. Background noise from runing water has been reduced and frequencies below below 100 – 500 Hz were filtered from the spectrograms.