Ranitomeya flavovittata Schulte 1999

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 : 66-68

Ranitomeya flavovittata Schulte 1999

Account authors: E. Twomey, J.L. Brown, P. Perez-Peña

Figs. 3 , 4 , 9 , 23 (e – i), 29

Tables 1, 4 – 6

Dendrobates flavovittatus Schulte 1999: p.80 [CRS BD 10H (holotype) from “Boca des Río Tahuayo, Nordufer, 120 m NN” = mouth of Río Tahuayo, north shore, 120 m. a.s.l, collected by Rainer Schulte];— Lötters & Vences 2000: p. 252; Brown et al. 2006: p. 46, Fig. 1; Roberts et al. 2006a: p. 378, Table 1, Figs. 2 , 4 ; Santos et al. 2009, by implication

Ranitomeya flavovittata — Grant et al. 2006: p.171; Lötters et al. 2007: p. 47, Figs. 595, 596; Twomey & Brown 2008: p. 129, Table 3, Fig. 6 , 2009: p. 50; von May et al. 2008a: p. 395, Appendix 2; Perez-Peña et al. 2010: p. 2, Figs. 7 , 8 , 13

Background information. This species was described from a single juvenile reared in the laboratory of INIBICO (Instituto de Investigación Biológica de las Cordilleras Orientales, Tarapoto, Peru). Schulte (1999) suggested that this species was closely related to Adelphobates quinquevittatus and A. castaneoticus , primarily on the basis of larval morphology. Schulte (1999) described the call as follows: “a short, harsh trill-call, this call type is unprecedented in Peru and forms a new call group” [translated from German]. Although the description was lacking in some aspects (particularly with regard to intraspecific variation), Lötters & Vences (2000), in a severe critique of Schulte (1999), nevertheless agreed on the validity of R. flavovittata . Roberts et al. (2006a) published the first genetic data for this species, supporting its validity, and found it to be nested within the vanzolinii group as the sister taxon to R. vanzolinii .

Morphologically, R. flavovittata strongly resembles R. yavaricola , although the latter lacks black markings on the legs. Each of the traits appears to be fixed within each species, respectively ( Perez-Peña et al. 2010).

Tadpole. The description is based on a single tadpole in stage 26 from Río Tahuayo, Loreto, Peru. Tadpole in stage 26. Body ovoid in dorsal view, wider near vent. Total length 17 mm; body length 7.3; tail length 9.7, 57% of total length. Body width 6.9; body depth 5.4, 78% of body width. Eye well developed; naris small; distance from naris to anterior edge of eye 1.8. 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 2.7; tail muscle width at base of tail 1.7; maximum tail height 3.9. Dorsal fin slightly higher than ventral fin.

Oral disc ventral, emarginate; transverse width 1.9, 28% 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 oral disc); P-1 on lower labium with narrow medial gap; P-3 80% width P-1; P-2 equal to width P-1.

Color in life. Head whitish, mouthparts visible from above. Abdomen whitish, mostly transparent, intestinal coils tan, heart visible. Tail musculature uniform tan, dorsal and ventral fins semi-transparent, white.

Natural history. Almost nothing has been published on the natural history of this species. Schulte (1999) mentioned that he found two white eggs in a small bromeliad ( Guzmania sp. ) 1.2 m from the ground. Based on our own observations, this species appears to have similar life-history traits as other members of the vanzolinii group. We have witnessed adults (presumably males) carrying single tadpoles in the vicinity of Guzmania bromeliads. We also encountered one courting pair in the axils of a species of palm. Near Rio Yavari-Mirin, we encountered a single tadpole within a bromeliad attached to a liana 1.5 meters above the ground. Males call regularly throughout the day. It is still unknown whether this species displays biparental care like its closest relatives R. vanzolinii and R. imitator ( Caldwell & de Oliveira 1999; Brown et al. 2010). However, anecdotal data from terrarium observations reveal that tadpoles of this species engage in “begging” behavior similar to the behavior displayed by R. imitator and R. vanzolinii when begging for food eggs (Chris Miller, pers. comm.). Therefore, this species may also have biparental care, although further study is required.

Vocalizations. The call of R. flavovittata is a stereotypical vanzolinii species group call: loud trill, notes 0.8- 1.1 sec in length, repeated at roughly 2 notes per minute ( Fig. 28 , Table 5). We disagree with Schulte’s assertion that this species has an unusual call which should be considered a new call group. At the time of this species’ description in 1999, the calls of several species of the vanzolinii species group frogs were known and the call of R. flavovittata fits into that call type.

Distribution. The type locality is described as ‘mouth of Río Tahuayo, north shore.’ Although this leaves some ambiguity as to the precise location (Río Tahuayo flows into the Amazon on a north–south axis, therefore the two ‘shores’ are better described as east or west), we can assume that the type locality is south of the Amazon. Since 2004 we have documented several other localities for this species, all of which are in the Tamshiyacu– Tahuayo region, except for two records: one from Río Yavari and another further south from nearby Genaro Herrera ( Fig. 29 , Giuseppe Gagliardi, pers. comm). Based on extensive field work within this region (mainly by P. Perez-Peña), it appears that R. flavovittata has a highly restricted range, although areas south of Río Yavari remain under-studied. Several flavovittata -like frogs have been observed in Brazil near Reserva Extrativista do Alto Juruá and Parque Nacional da Serra do Divisor; however, it remains undetermined whether these frogs represent populations of R. flavovittata or R. vanzolinii . Surveys of these populations are central to clarifying the alpha-taxonomic status of this species.

This species occurs within Amazonian rainforests of Peru (Departments: Loreto, possibly in Ucayali) and possibly within Brazil (States: Acre, Amazonas) .

Conservation status. The IUCN Red List of Threatened Species considers this species as Data Deficient ( DD) on the basis of the unverified taxonomic status and the ambiguous type locality. This species is now known from 6 localities in the Tamshiyacu–Tahuayo region of northern Peru and its taxonomic status appears to be valid. We recommend listing this species as Least Concern ( LC), applying IUCN Red List categories and criteria ( IUCN 2010) since it is locally abundant and occurs in habitat that is largely unaffected by humans .

Taxonomic remarks. As in previous studies (e.g., Roberts et al. 2006a, Twomey & Brown 2008), our results support the arrangement of R. flavovittata as sister species to R. vanzolinii . However, our expanded dataset (which includes five R. flavovittata as opposed to a single individual in previous studies) raises some uncertainty as to the taxonomic status of this species. In our current phylogeny, R. flavovittata is paraphyletic with respect to R. vanzolinii . Still, R. vanzolinii and R. flavovittata are morphologically distinct and therefore we maintain the current taxonomy here until more data can be collected, particularly from intermediate geographical regions (as mentioned above). Regardless of the aforementioned taxonomic issues, introgressive hybridization appears to have occurred between this species and other members of the vanzolini group; we collected an individual of R. sirensis (Panguana morph from Contamana) whose mtDNA was most closely related to R. flavovittata (suggesting historic hybridization between a female R. flavovittata and a male R. sirensis , Fig. 3b ).

If R. flavovittata is determined to be a separate species from R. vanzolinii , the observed phylogenetic topology could be attributed to historic introgression between the ancestors of R. flavovittata and R. vanzolinii . However, until additional populations of R. vanzolinii are surveyed, these questions cannot be addressed. For additional information see the R. vanzolinii account.

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 6. Andinobates Plate 2. fulguritus group: A–D: Andinobates fulguritus (all from Risaralda, Colombia. photos DMV). bombetes group: E: Andinobates abditus type locality (photo W.E. Duellman). F–I: Andinobates daleswansoni and habitat (photos J. Mejía-Vargas); F & G: from type locality; H: type locality habitat; I: overview of habitat – human encroachment continues to threaten the habitat of this species. J–M: Andinobates dorisswansonae from Tolima, Colombia (photos DMV and T. Ostrowski). N–P: Andinobates tolimense from Tolima, Colombia (photos V. Mora-Luna). Q–R: Andinobates sp. aff. tolimense from Supatá, Colombia (photos G. Chaves-Portilla and T. Ostrowski).

FIGURE 7. Andinobates Plate 3. bombetes group: A–B: Andinobates sp. aff. tolimense; A: from Supatá, Colombia (Photo credits: G. Chaves-Portilla); B: Tolima, Colombia (Photo credits: Fundacion ProAves-Alonso Quevedo). C–H: Andinobates bombetes, all from Colombia (photo credits: DMV and T. Ostrowski); C: Quebrada a la Chapa, Boyacá; D-E: Valle del Cauca, T. Ostrowski; F: Yotoco, Valle del Cauca; G: Lowland habitat of A. bombetes near Quebrada a la Chapa; H: Yotoco, Valle del Cauca. I: Andinobates sp. aff. bombetes undisclosed locality in Colombia (photo credits: Dennis Nilsson and DMV). J–N: Andinobates virolinensis; Charalá, Virolin, Colombia. O–Q: Andinobates opisthomelas. O: Guatape, Antioquia, Colombia (photo credits: Dennis Nilsson and DMV); P-Q: Carmen de Atrato, Choco, Colombia.

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 23. Ranitomeya Plate 6. vanzolinii group: A & B: Ranitomeya cyanovittata: Sierra del Divisor, Ucayali, Peru (G. Knell and D. Vasquez, 1:Ω,2: 1Φ). C & D: Ranitomeya yavaricola (all from Loreto, Peru): C: Rio Blanco (G. Knell); D: Lago Preto (PPP, Ω). E– I: Ranitomeya flavovittata (all from Quebrada Blanco, Loreto, Peru (Photo credits: JLB, ET and PPP, Ω). J–K: Ranitomeya vanzolinii Atalaya, Ucayali, Peru (J. Yeager). L–V: Ranitomeya imitator (All from San Martin, Peru): L–O: Upper Canarachi Valley (‡); P– Q: Tarapoto (‡); R: Shapaja (‡); S: Chumia (‡) and T–V: Chazuta (Ω). (nΦ = number of individual in phylogeny, Ω = population sampled in phylogeny, ‡ = genetically sampled, but not included in our phylogeny).

FIGURE 28. Advertisement calls of Ranitomeya species in the vanzolinii group. A. Ranitomeya vanzolinii from Pongo de Mainique, Cuzco, Peru, recorded in captivity at 26° C; B. Ranitomeya sirensis from Ishanga near Tocache, San Martín, Peru, recorded at 25.5° C; C. Ranitomeya imitator from Varadero, Loreto, Peru, recorded at 23.5° C; D. Ranitomeya imitator from Cainarachi valley, San Martín, Peru, recorded at 22 C; E. Ranitomeya flavovittata from Rio Tahuayo, Loreto, Peru, recorded in captivity at 25° C; F. Ranitomeya yavaricola from Lago Preto, Loreto, Peru, recorded at 24° C (call courtesy Pedro Pérez-Peña).

FIGURE 29. Known distribution of Ranitomeya flavovittata, R. yavaricola and R. cyanonvittata. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).