Aromobates saltuensis ( Rivero, 1978 )

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 : 20-24

Notes on Aromobates saltuensis ( Rivero, 1978)

Taxonomic history. Aromobates saltuensis was described originally as Colostethus saltuensis by Rivero (1978) from a single unsexed adult UPRM 5147. This specimen was collected by J.A. Rivero and A.E. Esteves on June 3rd, 1971 along the road between La Fría and Michelena, Estado Táchira, Venezuela, at an elevation of 830 m. The approximate coordinates of the type locality are 7.9676 N and 72.2612 W with an uncertainty of at least 5 km. Grant et al. (2006) provided information of two putative populations of C. saltuensis in northern Colombia and transferred this species to Aromobates . However, the information about the specimens identified by Grant et al. (2006) as A. saltuensis has some limitations (see distribution and phylogenetic relationships below). To this date, the distribution, conservation, and natural history of A. saltuensis are little known.

Referred specimens. In 2007, we collected several specimens and we referred them as A. saltuensis . CVULA 8315–20, from the road between San Félix and San Juan de Colón, Estado Táchira, Venezuela, 8.0736 N, 72.2293 W, 751 m; CVULA 8321–24 from Rio Negro (Parque Nacional ‘El Tamá’), Estado Táchira, Venezuela, 7.5787 N, 72.1790 W, elevation 482 m.

Diagnosis. (1) Skin on dorsum smooth to finely granular. (2) Paired dorsal scutes present on digits. (3) Distal tubercle on FIV present. (4) FIV length reaches half distal subarticular tubercle of finger III. (5) FI longer than II. (6) Digital discs present. (7) Finger discs weakly expanded. (8) Finger fringes mainly absent. (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, ending tubercle-like. (16) Toe discs moderately expanded. (17) Toe webbing reduced. (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 but indistinct on males, absent on females. (21) Dermal collar absent. (22) Male throat coloration grey with profusion of melanophores; female throat coloration dirty white with a profusion of melanophores. (23) Male abdomen color immaculate white. (24) Female abdomen color dirty white. (25) Iris coloration bronze with black reticulation; pupil ring bronze. (26) Large intestine unpigmented. (27) Testes white. (28) Median lingual process absent. (29) Tympanum distinct in its inferior half, tympanic annulus absent. (30) Vocal sac distinct. (31) Teeth present on the maxillary arch. (32) Size small, males (n = 3) 22–23.1 mm, mean 22.6 ± 0.6; females (n = 3) 22.9–26.9, mean 25.5 ± 2.3.

Varitation in the referred series. Rivero (1978) described variation within A. saltuensis by confronting the type specimen against a subadult (UPRM 5593) also collected from the type locality. However, the description provided in Rivero (1978) does not allow us to unambiguously evaluate the variation among our referred series. Therefore, we provide a description of the variation only based on our referred series. Males have a SVL range of 22–23.1 mm, and females SVL range of 22.9–26.9 based on three adult specimens of each sex. Body is slender, round to quadrangular in cross-section. Dorsal skin, including dorsal surfaces of hind limbs is smooth, shagreen to finely granular, without tubercles on the posterior part of the body in preservative. Ventral skin is smooth. Head is longer than wide, HeL = 35.8–37.9 % SVL; HW = 32.8–36.3 % SVL. On males, snout is truncated to pointed in profile. On females, snout is rounded to slightly pointed. Nares are situated laterally to the tip of snout; narial openings are barely visible when viewing the head from the front, not visible when viewing dorsally; and they are visible when viewing from a ventral perspective. Canthus rostralis is angular, the loreal region is almost flat; interorbital region is little wider than the upper eyelid. Snout is longer than ED. Only half of the tympanum is distinct and it is visible at its anteroventral portion but concealed posterodorsally by a low supratympanic bulge formed by the superficial slip of m. depressor mandibulae. The tympanum is positioned closely behind eye and close to the angle of jaws. Teeth are present on maxillary arch. Vocal slits are short to long, arched from mid-level of tongue to the anterior angle of the jaws. The tongue is short, oval to triangular; it is half free posteriorly.

Hand is of moderate size (25–28.2 % SVL); relative lengths of adpressed fingers are III> I> II> IV; discs of all fingers are weakly expanded, horizontally oval to round; FIII is barely wider than distal end of adjacent phalanx, at its maximum point is 1.3 wider; the base of palm has a large, palmar tubercle, rounded, quadrangular to heartshaped; and on the base of FI there is a smaller (approximately 1/3 of the palmar tubercle), oval to elongate thenar tubercle; one or two subarticular tubercles on fingers (one each on FI and FII, two each on FIII and FIV); and all tubercles are flat to round or oval; without supernumerary tubercles. Fringes on fingers are mainly absent, but on some males and females can be present, they are low and indistinct on FII and FIII.

Hind limbs are of moderate length, SL = 47.5–52.9 % SVL; relative lengths of adpressed toes are IV> III> V> II> I; TI is short, the tip never reaching the mid-subarticular tubercle of TII; toe discs are round to oval, moderately expanded, TIV is about 1.8 times wider than distal end of adjacent phalanx; feet is moderately webbed; formula is I2-2 ½ II2-3 ½ III3-4 IV and basal between TIV and TV; fringes on all toes are notable, short but flap-like with a folding around the toes; one to three non-protuberant, subarticular tubercles are present but small (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 rounded outer, and a slightly larger oval inner tarsal tubercle; mid-tarsal tubercles are seldom seen; tarsal keel is well-defined, thick, straight, transverse across tarsus, from proximal edge of inner metatarsal tubercle to mid-tarsus, with an ending tubercle-like structure; cloacal opening is located at the upper level of thighs, with short tube flap or anal sheath.

Comparison with the original description. When compared with the original description ( Rivero 1978), we found a few additional details that should be noted. First, Rivero (1978) does not note a supratympanic bulge, but this characteristic varies depending on the preservation method. Second, Rivero also mention the presence of basal webbing between FII-III-IV, which is absent on the referred specimens examined (another character that can vary in preserved specimens). All the remaining characteristics described for the holotype are among the variation seen in the new specimens collected.

Color. The referred specimens in life have dorsa with pale to dark brown coloration, patternless or presenting irregular spotting; the dorsolateral stripes can be very distinct ( Fig. 10 A) to ill-defined ( Fig. 10 C), pale orange to dark brown. The flanks can have a narrow dark brown longitudinal band below the dorsolateral stripe or they can be completely dark brown to the ventral area. The oblique lateral stripe can be solid, diffuse, or almost absent (consisting in a few, irregular and indistinct dirty white spots in the inguinal zone, even not forming a real stripe). Upper lips are patternless. Arms and hind limbs can be pale orange or brown to dark brown, with darker well-defined to ill-defined crossbars. Ventrally, males are pale grey on the throat and chest, white on the belly, with some opaque yellow on the hind limbs ( Fig. 10 B). Females are plain grey on the throat, dirty white on the belly ( Fig. 10 D). Iris is bronze with black reticulation; iris ring is also bronze.

Preserved specimens have a minimal dichromatism slightly apparent ventrally on males, as they have darker throats (pale to dark grey), consisting of a profusion of melanophores under magnification. Females are all white (with a few melanophores under magnification). The rest of the body coloration is not dichromatic in both sexes, varying in being paler or darker, with well or ill-defined crossbars on hind limbs.

Natural history. We found all Aromobates saltuensis associated to a slow flowing creeks surrounded by pastures (type locality), primary, and secondary forests (Rio Frio, Tamá). Several males were calling from exposed and concealed sites in the creek, such as on the top of rocks or behind small waterfalls. Some females were seen moving along the creek as well. All individuals were active during daytime.

Vocalization. The analyzed call is a section of a trill that lasted several minutes. The call was recorded at 22.5ºC (water temperature) at early afternoon on the June 9th, 2007 near the type locality (see referred specimens). The analyzed section of the call has four duplets of notes ( Fig. 11 ), lasting 2 sec. One to two duplets of notes are produced per second. The dominant frequency of the first pulse is slightly lower than the second. The first pulse has a dominant frequency range of 3437.0–3862.7 Hz. The second pulse has a dominant frequency range of 3511.0 –3862.0 Hz. Four consecutive duplets were chosen at random from the spectrogram to determine temporal variables. Duplet duration 0.15 ± 0.01 (0.14–0.16) seconds, and inter-duplet interval 0.46 ± 0.17 (0.34–0.65) seconds. Note and inter-note duration with their mean, SD and range in seconds are indicated as follows (1) note duration, first note 0.04 ± 0.01 (0.03–0.04); second note 0.05 ± 0.01 (0.04–0.05); and (2) inter-note, 0.07 ± 0.01 (0.06–0.07). Both, the waveform is shown by Fig. 11 A and the spectrogram by Fig. 11 B.

Distribution. Aromobates saltuensis is known from the southwestern extreme of the Cordillera de Mérida and northeastern Cordillera Oriental, and has been reported in northeastern Colombia by Grant et al. (2006) and Anganoy-Criollo (2012) from Departamentos of Norte de Santander, Boyacá and Cesar, respectively ( Fig. 3 ). However, A. saltuensis is likely to be a Venezuelan endemic and the Colombian specimens might represent other species and closer to A. cannatellai sp. nov. as supported by our phylogeny ( Figs. 1 and 2 , see next section). For this reason, we revised the specimen information associated to A. saltuensis specimens provided by Grant et al. (2006) and we found it to be problematic. The information provided of the specimens ICN 42512-16 and 33587 is inaccurate as they are from two distinct and geographically distant localities on the western slopes of the Northern Andes of Colombia. Moreover, it is not justified why all specimens are assigned to a single population from Bacar[a]sica (the name is misspelled as ‘Bucarsica’ in the original paper, Grant et al. 2006: 242). First, the locality information for the specimens ICN 42512-16 corresponds to Corregimiento Pueblo Nuevo, Sitio El Reposo, 4.8 km on the road of Ocaña to Pueblo Nuevo (8.2304 N, 73.3890 W at ~ 1560 m). This locality is 61 km WNW of the Bacar[a]sica site provided by Grant et al. (2006). Second, the data provided for the specimen ICN 33587 corresponds only to the municipality and the following information is more accurate: 25.3 km by road from Sardinata at 1040 m, municipio Bacarasica, Norte de Santander. The approximate coordinates of ICN 33587 are 8.1326 N and 72.8960 W with an uncertainty of at least 3 km.

Grant et al. (2006) provided information of a third population that most likely is based on molecular data (no information is provided about specimen morphological identification). The voucher specimen is MUJ 3726 (Museo de Historia Natural, Universidad Javeriana, Bogotá, Colombia) from Cubará, Fátima, Quebrada Gralanday in Boyacá on the eastern slopes of the Northern Andes of Colombia, which is closer in our analysis to A. cannatellai than to A. saltuensis , although both species are nested in a “ saltuensis ” clade. The approximate coordinates for the MUJ 3726 specimen are 6.8790 N and 72.1879 W. The distance from the Cubará population to the two other northern populations in Norte de Santader is 160–200 km in straight line. Moreover, all localities of the A. saltuensis specimens from Grant et al. (2006) are at least 61 kms of distance from the approximate type locality of A. saltuensis provided by Rivero’s description near Michelena (7.9676 N and 72.2612 W) on the Mérida Andes. Specifically, Sardinata is at least 61 km W, Pueblo Nuevo is at least 128 km WNW, and Cubará is at least 122 km S from Michelena. Anganoy-Criollo (2012) reported further extension in the distribution of A. cf. saltuensis from two new localities in the southernmost edge and western versant of the Sierra de Perijá at ~ 133 km northwest from Michelena type locality. These two new localities are very close within the Departamento de Cesar, namely, El Gitano (near Rio de Oro at approximately 8.3166 N, 73.4167 W) and San Cayetano (near Gonzales at approximately 8.3931 N, 73.3844 W). La Marca (2005), on the other hand, has suggested that Aromobates species most likely show restricted distributions with no more than 60–70 km 2. Therefore, it is unclear to us if all these specimens correspond to a single species or even less if they are conspecific with A. saltuensis or even with A. tokuko (see phylogenetic relationships below). Thus, we consider the presence of A. saltuensis in Colombia as highly unlikely, but closely related allies might be present.

Our referred specimens are less than 13 km from the type locality near Michelena. The original description A. saltuensis ( Rivero 1978) indicates a collection site at an elevation of 830 m on the road from La Fria (elevation 119 m) to Michelena (elevation 1230 m) in Estado Táchira ( Venezuela); this road is 25 km long. The locality of the CVULA 8315– 20 specimens are from the same road described by Rivero (1978), and about 12.5 km from the georeferenced type locality. In consequence, we consider the CVULA 8315–20 series to be topotypic. The series CVULA 8321–24 from ‘Rio Frío, Tamá’ is about 44 km from type locality. Therefore, according to our data, we consider Aromobates saltuensis to be endemic to Venezuela. However, we suggest a careful comparison of all Grant et al. (2006) and our specimens with the type UPRM 5147 (University of Puerto Rico) to further confirm our insights.

Phylogenetic relationships. We found Aromobates saltuensis to be well-nested in Aromobates ( Fig. 1 ). This suggests a relative recent extension and radiation of the saltuensis clade into Eastern Cordillera of Colombia. Grant et al. (2006) provided nuclear and mitochondrial sequences from a specimen identified as A. saltuensis with the voucher number MUJ 3726 from Cubará ( Colombia: Boyacá). However, it is unclear if these authors actually identified the specimen as A. saltuensis as discussed on previous section. We found MUJ 3726 to be closely related to A. cannatellai based on the 12S-16S rRNA segment. At the moment, we suggest recognizing MUJ 3726 as voucher from a different species and we restrict A. saltuensis only to the Venezuelan localities.

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 10. Aromobates saltuensis from the road from San Felix to San Juan de Colón, Estado Táchira, near type locality. (A) Adult male CVULA 8317. (B) Ventral view of the same specimen. (C) Adult female CVULA 8320. (D) Ventral view of the same specimen. Photos by CBA.

FIGURE 11. (A) Waveform and (B) spectrogram of a 2.6 seconds sequence of the call of Aromobates saltuensis sp. nov., showing four duplets. Indistinct harmonics can be seen at around 8000 Hz. Background noise from runing water has been reduced and frequencies below below 100 – 500 Hz were filtered from the spectrogram.