Ranitomeya uakarii Brown, Schulte & Summers 2006

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 : 57-58

Ranitomeya uakarii Brown, Schulte & Summers 2006

Account authors: J.L. Brown, E. Twomey, R. von May, J.P. Caldwell, P.R. Melo-Sampaio, M.B. Souza

Figs. 3 , 4 , 9 , 16 (o, p), 17(a – h), 18, 22

Tables 1, 4 – 6

Dendrobates quinquevittatus (non Steindachner 1864)—Silverstone 1975 (partim): p. 33

Dendrobates ventrimaculatus (non Shreve 1935)— Rodriguez & Knell 2003 (partim): p. 148; Christmann 2004 (partim): p. 19, Figs. on p. 19, 97, 154; Brown et al. 2006 (partim): p. 45, Table 2, Figs. 1, 4 ; Roberts et al. 2006a (partim): p. 382, Table 1, Fig. 4

Dendrobates duellmani (non Schulte 1999)— Roberts et al. 2006a (partim): p. 377, Table 1, Figs. 1, 4 .

Dendrobates uakarii Brown, Schulte & Summers 2006: p.47 , Figs. 1–4, Table 1, 2 [MUSM 23246 (holotype) collected by Mario Callegari upstream Quebrada Blanco near the Tamshiyacu–Tahuayo Reserve, Department Loreto, Peru, 2004];— Santos et al. 2009, by implication

Ranitomeya uakarii — Grant et al. 2006, by implication; Lötters et al. 2007: p. 494, Fig. 624; von May et al. 2008a: p. 396, Appendix 2; Perez-Peña et al. 2010: p. 2, Figs. 8 , 13

Ranitomeya cf. reticulata (non Boulenger, 1884 “1883”)— Lötters et al. 2007: p. 493, Fig. 623.

Ranitomeya cf. uakarii — Lötters et al. 2007: p. 495, Fig. 625

Ranitomeya ventrimaculata (non Shreve 1935)— Perez-Peña et al. 2010 (partim): p. 18, Fig. 13

Background information. Prior to the formal description of this species as R. uakarii , it was considered a morph of R. ventrimaculata sensu this paper (see below). The type series consists of five individuals collected from just outside Tamshiyacu–Tahuayo reserve. Since this description, we have learned of additional populations of uakarii - like frogs from numerous localities throughout the Amazon basin. Molecular phylogenetic analyses indicate that these populations represent several morphs not discussed in the original description, making it necessary to redefine R. uakarii .

Definition and diagnosis. Assigned to the genus Ranitomeya due to the combination of the following characters: Size small (adults <17.5 mm SVL), dorsal coloration conspicuous, dorsolateral stripes extend to top of thigh, ventrolateral stripes present, 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 2 – 2.5 times wider than finger width, thenar tubercle conspicuous, toe disc III – V moderately expanded, toe webbing absent, larval vent tube dextral, adults use arboreal phytotelmata for reproduction and deposit eggs above the waterline in phytotelm, maxillary and premaxillary teeth absent. Tadpole gray, ovoid, with irregular markings present from early in development. Three morphs of this species are currently known: (i) the Nominotypical morph ( Figs. 16o – p , 17a – c, h ), (ii) the Toraro morph ( Fig. 17e, f ) and (iii) the Tri-Country morph ( Fig. 17g ). The limbs and venters of all morphs are reticulated in blue to greenish blue on black, forming black spots.

(i) The Nominotypical morph has a dorsum with paired red or reddish-orange dorsolateral stripes (thin or thick) that extend from the tip of the snout, where they form a U-shape, to the groin. A single middorsal stripe starts on the top of the head and terminates above the vent. This stripe may occasionally form a ‘Y’ on the head, connecting with the dorsolateral stripes to create a black spot on top of snout. A yellow labial stripe continues to form a spot on the upper forearm. A yellow, irregular ventrolateral stripe is present. Venter is reticulated blue or greenish blue on black. Chin is yellow with paired black spots. This morph occurs throughout the lowlands east of Río Ucayali and southeast of Río Amazonas in Peru (Loreto and possibly Ucayali Departments) and has been observed in central Peru along Río Pachitea (Huánuco Department). A population of frogs similar in appearance has been discovered in Guyana (District: Potaro-Siparuni, Fig. 17h ). Due to the seemingly widespread distribution of R. uakarii , we provisionally consider the Guyana population as R. uakarii .

(ii) The Toraro morph is so named because of its strong resemblance to R. toraro sp. nov. (in fact, these two species were long thought to be conspecific and may in fact be Müllerian mimics, see mimicry section). It has thin yellow dorsolateral and oblique lateral stripes. A similar middorsal stripe begins at the top of the head and terminates above the vent. The stripe typically divides into a ‘Y’ on the head (between the orbits) connecting with both dorsolateral stripes. The ventrolateral stripes often form irregular connections to the dorsolateral stripes. This morph is infrequently encountered, though it can be locally abundant (e.g., near Porto Walter, Brazil). This morph occurs within the lowland forests of southwestern Brazil (States: Acre, Amazonas), in southeastern Peru (Department: Madre de Dios) and possibly into northwestern Bolivia (Department: Pando).

(iii) In the Tri-Country morph, 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 the red middorsal stripe). The upper lip has a short yellow stripe that terminates on the upper surface of the forearms. This morph lacks a distinct oblique lateral stripe. This morph has not been genetically sampled, thus its classification should be considered provisional. This rare morph is known to occur in southeastern Colombia (Departments: Amazonas and Caquetá) near the three-country corner shared between Peru, Colombia and Brazil. Thus, we would not be surprised if this morph were discovered in nearby Brazil or Peru.

The Nominotypical morph is similar in appearance to Ranitomeya amazonica , R. ventrimaculata (sensu this paper) and some morphs of R. reticulata . Ranitomeya amazonica typically possesses a conspicuous black ‘Y’ which 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 a black ‘Y’, but they typically have complete to largely complete middorsal stripes). Individuals of R. uakarii with red dorsolateral stripes typically have yellow ventrolateral stripes (versus typically absent in R. ventrimaculata and R. reticulata , or, if present, the ventral and limb reticulation are the same color).

The Toraro morph can be distinguished from its apparent mimic, R. toraro , by the following characters: presence of a large black spot on the rostrum (typically absent in R. toraro ), presence of a complete labial stripe (absent in R. toraro ), non-fused black nostril spots (nostril spots fused in R. toraro , creating the appearance of a upside down ‘U’ on the tip of the snout), typically two smaller pairs of black gular spots (single pair of large spots in R. toraro ), and a middorsal stripe that is constant width (middorsal stripe two times wider on the head compared to the sacral region in R. toraro ). Often the ventrolateral and dorsolateral stripes are connected by small irregular stripes, middorsally.

The Tri-Country morph is similar in appearance to R. reticulata and R. ventrimaculata sensu this paper but possesses a yellow labial stripe (versus red in R. reticulata and pinkish-red in R. ventrimaculata ).

Tadpole. The description is based on a single live tadpole from Río Tahuayo , Loreto, Peru. Mouthparts were verified in two other tadpoles of R. uakarii from Quebrada Blanco, Loreto and Tournavista, Huánuco. The tadpole was feeding on detritus .

Tadpole in stage 29, no external gills. Body ovoid in dorsal view, wider near vent. Total length 16.5; body length 6.3; tail length 10.2, 62% of total length. Body width 4.6; body depth 3.7, 80% of body width. Eyes well developed; naris small, distance from naris to anterior edge of eye 0.6. Eye positioned dorsally on head, directed dorsolaterally. Spiracle well developed; vent tube dextral.

Tip of tail bluntly rounded. Tail muscle height at base of tail 1.8; tail muscle width at base of tail 1.6; maximum tail height 2.5. Dorsal fin slightly higher than ventral fin.

Oral disc ventral, emarginate; transverse width 1.6, 35 % of body width. Single row of small papillae present laterally and ventrally; dorsal gap where papillae absent. LTRF 2(2)/3(1) with A-1 developed on upper labium, A-2 with wide medial gap (one-third total width of tooth row); P-1 on lower labium with narrow medial gap; P-2 equal width of P-1; P-3, 75% width of P-1.

Color in life. Head gray, mouthparts visible from above. Body gray, color evenly distributed; abdomen mostly transparent, intestinal coils black, heart visible. Tail musculature uniform gray, dorsal and ventral fins opaque gray.

Distribution. This species occurs in Amazonian rainforests of Brazil (States: Acre, Amazonas), possibly into Bolivia (Department: Pando), Colombia (Departments: Amazonas, Caquetá), Guyana (Potaro-Siparuni) and Peru (Departments: Huánuco, Loreto, Madre de Dios and possibly Ucayali), Figure 22 .

Conservation status. Following the IUCN Red List categories and criteria ( IUCN 2010), we suggest listing this species as Least Concern (LC). It exhibits a large geographical range and occurs within several protected areas.

Taxonomic remarks. This species warrants further study and could possibly represent a species complex given the geographically distinct morphs. Under the current phylogeny we find little support for this arrangement and the nominotypical and Toraro morph are not reciprocally monophyletic.

Figures

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 8. Advertisement calls for species of Andinobates. A. Andinobates bombetes from Bosque Yotoco, Valle del Cauca, Colombia (type locality), recorded at 18-20° C; B. Andinobates claudiae from Isla Colón, Panama, recorded at 25° C (call courtesy Thomas Ostrowski); C. Andinobates fulguritus from Itauri, Colombia, unknown temperature; D. Andinobates fulguritus from Kuna Yala, Panama, recorded in captivity at 24° C (call courtesy T. Ostrowski); E. Andinobates dorisswansonae from “El Estadero”, Caldas, Colombia (type locality), recorded at 19-20° C; F. Andinobates minutus, unknown locality or temperature; G. Andinobates opisthomelas from Guatapé, Antioquia, Colombia, unknown temperature.

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 13. Known distribution of the defleri group. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).

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 17. Ranitomeya Plate 5. reticulata group: A–I: Ranitomeya uakarii: A: Central Rio Yavari, Loreto, Peru (PPP); B: Quebrada Blanco, Loreto, Peru (PPP, Ω); C: Rio Boncuya, Loreto, Peru (G. Gagliardi); D: Tournavista, Huánuco (A. Toebe); E: Porto Walter, Acre, Brazil (JPC); F: Rio Los Amigos, Madre de Dios, Peru (RVM); G: R. uakarii sp. aff. Caquetá, Colombia (J. M. Rengifo); H: R. uakarii sp. aff. Iwokrama, Guyana (unknown photographer); I: Guzmania bromeliad with R. uakarii embryos near Tamshiyacu village, Loreto, Peru. (Ω = population sampled in phylogeny).

FIGURE 22. Known distribution of Ranitomeya uakarii. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).