Ranitomeya ventrimaculata Shreve 1935

Brown, Jason L., Twomey, Evan, Amézquita, Adolfo, Souza, Moisés Barbosa De, Caldwell, Jana- Lee P., Lötters, Stefan, May, Rudolf Von, Melo-Sampaio, Paulo Roberto, Mejía-Vargas, Daniel, Perez-Peña, Pedro, Pepper, Mark, Poelman, Erik H., Sanchez-Rodriguez, Manuel & Summers, Kyle, 2011, A taxonomic revision of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae) 3083, Zootaxa 3083 (1), pp. 1-120 : 59-61

Ranitomeya ventrimaculata Shreve 1935

Account authors: J.L. Brown, E. Twomey, E.H. Poelman

Figs. 3 , 4 , 9 , 16 (h – n), 18, 21

Tables 1, 4 – 6

Dendrobates minutus ventrimaculatus Shreve 1935: p. 213 [MCZ 19734 (holotype) collected by O. C. Felton from “Sarayacu, Ecuador ” 1933]

Dendrobates quinquevittatus (non Steindachner 1864)—Silverstone 1975 (partim): p. 33; Almendariz 1987 (partim): p. 77; Lötters 1987 (partim) p. 72, Fig. 1

Dendrobates ventrimaculatus — Daly et al. 1987 (partim): p. 1025; Rodriguez & Duellman 1994 (partim): p. 17, Plate 2d; Caldwell & Myers 1990 (partim): p. 1; Santos et al. 2009, by implication

Dendrobates duellmani Schulte, 1999: p. 69 [NHMK 231832 (holotype, wrongly given as NHMK 221832 in the original description and corrected by Lötters & Vences 2000: p. 252), unspecified collector from “San Jacinto, 2 km, nahe der ekuadadorianischen Grenze, Loreto, Peru,” restricted to “Südöstliche Umgebung vom Ölcamp San Jacinto (bei 2°18’42.8“ S, 75°51’57.9“ W), circa 180 m NN, östlich des Rio Tigre, Departamento Loreto, Peru ” by Lötters & Vences 2000: p. 252];— Lötters & Vences 2000: p. 252; Santos et al. 2003: p. 12794, Fig. 1; Cisneros-Heredia 2003; Christmann 2004: p. 8, Figs. on p. 16, 103, 104; Darst & Cannatella 2005: p. 60, Fig. 1; Brown et al. 2006: p. 45, Table 2, Figs. 1, 2 ; Roberts et al. 2006a (partim): p. 377, Table 1, Figs. 1, 4 ; Santos et al. 2009, by implication

Dendrobates sp. G — Santos et al. 2003: p. 12794, Fig. 1; Darst & Cannatella 2005: p. 60, Fig. 1

Ranitomeya aff. uakarii — Lötters et al. 2007: p. 496, Fig. 626

Ranitomeya duellmani — Grant et al. 2006: p. 171; Lötters et al. 2007: p. 470, Fig. 587: Venegas & von May 2010: p. 282; von May & Mueses-Cisneros 2011: p. 306.

Background information. This species was originally described by Shreve (1935) as a subspecies of Dendrobates minutus . Silverstone (1975) considered it a junior synonym of Dendrobates quinquevittatus . In 1982, Myers wrote that “New material, as well as closer attention to morphological details and evidence of sympatry, convinces me that Dendrobates quinquevittatus Steindachner , sensu Silverstone is a composite of five or more species of distinctively colored frogs.” Interestingly, almost a decade later Caldwell & Myers (1990) would point out that none of those species were in fact D. quinquevittatus sensu stricto.

In 1999, Schulte described Dendrobates duellmani from northern Peru. Its description promptly sparked criticism from Lötters & Vences (2000), primarily because most of the description was based on a photograph of a single live frog (from Rodriguez & Duellman 1994), which is traceable as NMHK 231832, and the use of other unorthodox “specimens” including a postal stamp issued by the Ecuadorian government. Nevertheless, due to unique morphology, Lötters & Vences (2000) agreed that duellmani was a valid species. In 2006, Grant et al. placed this species in the genus Ranitomeya within the ventrimaculata group. That same year, Roberts et al. (2006a) demonstrated that duellmani was polyphyletic, with one individual (the population closest to the type locality) nested within a clade of reticulatus and another individual that was sister to a species referred to as ventrimaculatus (the latter now considered to be Ranitomeya uakarii , see account in this paper).

Recently, the plea of Caldwell & Myers (1990) that taxonomists proceed with caution when dealing with the systematics of this group was further justified. After reading Shreve’s description of Dendrobates minutus ventrimaculata and examining the type material, J.L. Brown was surprised to learn that most of the specimens, including the holotype, were actually identical to R. duellmani . It is not clear exactly when the “unofficial” definition of R. ventrimaculata changed to R. variabilis sensu this paper; however, shortly after the description of R. duellmani , this “definition” became absolute in the scientific literature. One cause for this change was likely due to the presumption that Schulte (1999) considered the type specimens of R. ventrimaculata when describing duellmani . The situation was further exacerbated by an abundance of observations of the more widely distributed species: variabilis and amazonica sensu this paper, which at that time were also being called ventrimaculata . Due to the clarity of Shreve’s definition (see excerpt below) and morphology of the type specimens, we herein formally consider Ranitomeya ventrimaculata to be senior synonym of the junior synonym Ranitomeya duellmani . For classification of species considered to be R. ventrimaculata from 1987 to 2010, see the R. variabilis and R. amazonica accounts.

Black above, three prominent, longitudinal, grayish lines extending from the head almost the entire length of the back, the outermost starting about the posterior border of the upper eyelid, the median about on a level with the anterior border of the upper eyelid (in the paratypes [and type] these dorsal lines are often rather pinkish). Fifteen of the paratypes have substantially the same dorsal markings as the type; ten [now considered to be R. variabilis ] show an alternative set of dorsal markings. In these the median dorsal line is much shortened and sends out a pair of branches on the head (sometimes one of the pair is missing)… [and] the outermost lines [i.e., the oblique and dorsolateral lines] are often joined by a transverse line at their posterior ends [commonly observed in R. variabilis but not R. ventrimaculata sensu stricto]…

B. Shreve 1935, p. 214

Definition and diagnosis. Assigned to the genus Ranitomeya due to the combination of the following characters: adults small, SVL <18.0 mm, dorsal coloration conspicuous, dorsolateral stripes extending to top of thigh, brightly colored throat, distinctive pale reticulation on limbs and venter, dorsal skin smooth, finger I greatly reduced and shorter than finger II, finger discs II – IV greatly expanded, disc of finger two times wider than finger width, thenar tubercle conspicuous, toe discs III – V moderately expanded, toe webbing absent, larval vent tube dextral, maxillary and premaxillary teeth absent.

This species possesses thin pink to reddish-pink middorsal and dorsolateral stripes. Dorsolateral stripes typically extend from the groin, pass through the eyes and fuse at the tip of the snout. Middorsal stripe starts between the eyes and typically terminates above the vent. Ventrolateral and oblique lateral stripes absent. In most populations, both the dorsolateral and middorsal stripes blend with the limb and flank reticulation in the middle of the dorsum (between the axilla and groin, gradually changing from red to blue). The black space between the dorsolateral and middorsal stripe typically creates the appearance of a black ‘U’ with the bottom near the snout (occasionally this ‘U’ is broken and the red nose spot fuses with red medial stripe). Labial stripe, identically colored as dorsal stripes, terminates at the upper surface of the forearms. Venter, flanks and limbs are finely reticulated in blue-gray to gray on black; the throat coloration varies from being entirely pinkish to pinkish only at the tip (with the remaining throat being predominantly black). Some populations near Río Nanay, ca. 40 km west of Iquitos, Loreto, and on Río Momón near Iquitos lack a middorsal stripe and possess pinkish to plum dorsolateral stripes.

This species is similar in appearance to Ranitomeya amazonica , R. uakarii and some morphs of R. reticulata . Ranitomeya amazonica typically possesses a conspicuous black ‘Y’ that starts mid-dorsum and terminates at the snout (some morphs of R. ventrimaculata appear similar to this, possessing a broken ‘U,’ giving the appearance of black ‘Y;’ however, they typically have a complete to largely complete middorsal stripe). Ranitomeya uakarii individuals with red dorsolateral stripes typically have yellow oblique lateral stripes (typically absent in R. ventrimaculata , or, if present, they are the same coloration as ventral and limb reticulation). Some preserved specimens lose their red dorsal coloration, and can appear identical to some morphs R. uakarii . The latter generally possess distinct gular spots that do not connect, giving the appearance of an hourglass on the throat (versus fused gular spots, possessing light coloration- in life pinkish- only at the anterior edge of the throat in R. ventrimaculata ). Certain morphs of R. reticulata (and almost all juveniles of this taxon) possess a similar black ‘U,’ although it is typically broken rather than a complete stripe. The middorsal stripe is broad, blending with incomplete dorsolateral stripes that terminate near the mid-dorsum ( Fig. 16a, f ). The Río Nanay/Río Momón populations are distinct; no other Ranitomeya lacks a middorsal stripe while possessing pinkish dorsolateral stripes ( Fig. 16k ).

Natural history. Individuals of this species were found in undisturbed primary forest with deep leaf litter and low to moderately dense understory vegetation. In Napo province, Ecuador, we observed 1 to 3 individuals per day, suggesting that these frogs occur in low densities. Most frogs were observed foraging on leaf litter, occasionally climbing on tree trunks up to a meter above the forest floor. At localities where they were observed, bromeliads were not abundant on the forest floor (in many cases absent), but large bromeliads were present in the canopy. On several occasions we found vocalizing males, and males carrying 2 or 3 tadpoles on the forest floor. These observations suggest that the species has male parental care and egg clutches may be deposited in the leaf litter. However, to date, we have not been able to locate egg clutches or where males deposit their tadpoles.

Ranitomeya variabilis , R. reticulata , R. uakarii , Allobates zaparo , Ameerega bilinguis and A. parvula co-occur with R. ventrimaculata .

Vocalizations. The call of this species consists of a rapid buzz, notes 0.32 – 0.38 sec in length, repeated at approximately 124 notes per minute. Interestingly, in both R. ventrimaculata and its sister species R. reticulata , pulse rates are remarkably high compared to other members in their species group. Within a note, we found that individual ‘pulses’ are actually composed of triplets or quadruplets, a character that was not found in other members of the reticulata species group. This difference may be related to the quality of the recording (being able to detect such fine note structure in high quality recordings) rather than physiological differences in call production between species.

Distribution. This species occurs in Amazonian rainforests of Colombia (Amazonas Department), Ecuador (Provinces: Napo, Orellana, Pastaza, Sucumbíos) and Peru (Loreto Department), Fig. 21 .

Conservation status. Following the IUCN Red List categories and criteria ( IUCN 2010), we tentatively suggest listing this species as Least Concern (LC).

Taxonomic remarks. Over the past decade, mostly unpublished discussion has questioned the legitimacy of this species. Some have suggested that R. ventrimaculata is a morph of R. reticulata with the retention of juvenile coloration (paedomorphy; Roberts et al. 2006a). We remain skeptical of classifying these species as distinct because the potential distributions of both R. reticulata and R. ventrimaculata overlap considerably, something that is rare among closely related species. Further, in some areas it is impossible to distinguish them from each other, e.g., an individual from Kapawi, Ecuador is genetically classified as R. ventrimaculata , however is identical in coloration and pattern to some populations R. reticulata (possessing broad-bright red dorsal stripes versus thin-pinkish dorsal stripes observed in all other R. ventrimaculata ). However, because our phylogenetic results support two reciprocally monophyletic clades ( Fig. 3b ) that are mostly consistent with the morphological differences ascribed to each species, we suggest they remain distinct until more data are available.

Figures

FIGURE 2. Illustrated guide to morphological terminology. A. Finger and hand morphology: i. Finger I (far left) <Finger II, thenar tubercle (= inner metacarpal tubercle) present (depicted by arrow), and greatly expanded finger discs in Fingers II-IV. Inset depicts Finger I and a thenar tubercle which is clearly visible. Note that in some Ranitomeya this is trait reduced and difficult to view (as in main picture) (Ranitomeya variabilis pictured, inset of R. benedicta). ii. Finger I ≈ Finger II, thenar tubercle absent. (Adelphobates quinquevittatus pictured) iii. Weakly expanded finger discs in Fingers II-IV (Excidobates captivus pictured). B. Stripes: i. Middorsal (follows vertebral column), dorsolateral (extends from eye to either upper thigh, as pictured, or to vent), ventrolateral (running from groin to axilla) and labial stripe (stripe that extends from shoulder around upper lip)(R. sirensis pictured). ii.. Oblique lateral stripe (extends from groin to eye, as in picture stripe is incomplete anteriorly). Unlabeled arrow depicts a dorsolateral stripe that does not reach thigh, a characteristic of certain species of Andinobates (type ‘A’ in Grant et al. 2006). (Andinobates claudiae pictured). C. Limb patterns: i. Distinct limb reticulation/spotting (characteristic of most species of Ranitomeya) (R. variabilis pictured). ii. Wavy stripes (not classified as distinct limb reticulation) (R. summersi pictured). iii. Patternless. Typical of most Andinobates species (R. sirensis pictured). D. Diagnostic head patterns: i. Large black “oval” on head (R. imitator pictured). ii. Large black “pentagon” or “five-point star” on head (R. summersi pictured). iii. Black band across head entirely covering eyes (known only in a single population of this species near the Pongo de Manseriche, Peru) (R. fantastica pictured). E. Nose spots. i. Two nose spots (R. imitator pictured). ii. Single nose spot. (R. variabilis pictured). iii. Frontward-turned “U” on the tip of snout. (R. toraro pictured). F. Geographical distribution. West: distribution within Andes, west of Andes, or in Central America. East: distribution east of Andes (including Guiana Shield) or in east-Andean versant. G. Dorsal patterns: i.“Y-shape”. Space between stripes create black pattern which forms a black Y on the back. (R. variabilis pictured). ii. Merging of the obliquelateral and dorsolateral stripes (R. variabilis pictured). iii. Broken dorsolateral stripes (R. flavovittata pictured). iv. Spotting (R. imitator pictured). H. Key ventral characters: i. Distinctive throat coloration and ventral reticulation (also shown in H-ii & H-iii) (R. reticulata pictured). ii. Belly patch (R. sirensis pictured). iii. Gular spots (single or paired dark spots at corner of mouth) (R. amazonica pictured). iv. Marbled pattern (not classified as reticulation) (Andinobates virolinensis pictured).

FIGURE 3. A consensus Bayesian phylogeny based on 1011 base pairs of aligned mitochondrial DNA sequences of the 12S (12s rRNA), 16S (16s rRNA) and cytb (cytochrome-b gene) regions. Thickened branches represent nodes with posterior probabilities 90 and greater, other values are shown on nodes. Taxon labels depict current specific epithet, number in tree, the epithet being used prior to this revision (contained in parentheses), and the collection locality. A. Top segment. B. Middle segment. C. Bottom segment of phylogeny.

FIGURE 4. Putative species tree for Andinobates, Excidobates, and Ranitomeya. Placement of species where molecular data were lacking (A. altobueyensis, A. viridis, A. abditus, A. daleswansoni and R. opisthomelas) was based on morphology. Andinobates altobueyensis and A. viridis were placed as sister taxa due to the absence of dark pigmentation on dorsal body and limbs and overall similar dorsal coloration and patterning. These species were placed as sister to A. fulguritus (sequenced) on the basis of similar dorsal coloration (bright green to greenish-yellow). Andinobates opisthomelas was placed in the bombetes group in a polytomy with A. bombetes and A. virolinensis (both sequenced) due to their similar advertisement calls and morphology, particularly their red dorsal pattern and marbled venter. Andinobates daleswansoni was placed as sister to A. dorisswansonae due to the absence of a well-defined first toe in both species. Andinobates abditus was placed in the bombetes group based on a larval synapomorphy which appears to be diagnostic of that group (wide medial gap in the papillae on the posterior labium). However, A. abditus was placed as the sister species to all other members of the bombetes group due to the absence of bright dorsal coloration and isolated geographic distribution. Andinobates abditus is currently the only species of its genus known to occur in the east-Andean versant, thus its placement remains speculative until molecular data become available. Photo credits: Thomas Ostrowski, Karl-Heinz Jungfer, Victor Luna-Mora, Giovanni Chaves-Portilla.

FIGURE 9. Known elevation distributions of Ranitomeya. Dotted line is mean for all samples. Dark boxes display the total elevation range of each species, within each contains a corresponding box plot.

FIGURE 16. Ranitomeya Plate 4. reticulata group: A–G: Ranitomeya reticulata (all from Loreto, Peru); A: Lower Rio Itaya (Ω); B–D: Upper Itaya Drainage; E-F: Rio Sucusari (KS); G: 30 km west of Pevas (MSR). H–M: Ranitomeya ventrimaculata: H: Kapawi, Pastaza, EC (L. Coloma, 7Φ); I: Upper Curaray Drainage, Loreto, PE (PPP); J: Yasuní, Orellana, EC (A. Blasco Z., Ω); K: central Rio Nanay (M. Callegari, 6Φ); L: Holotype at MCZ, Sarayacu, Pastaza, Ecuador; M: Yasuní, Orellana, EC (J. Yeager, Ω); N: Yasuní, Orellana, EC (S. Ron, Ω). O & P: Ranitomeya uakarii (all from Loreto, Peru): O: Tamshiyacu village (8Φ) P: Quebrada Blanco (12Φ). (nΦ = number of individual in phylogeny;Ω = population sampled in phylogeny).

FIGURE 21. Known distribution of Ranitomeya reticulata and R. ventrimaculata. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).