Ranitomeya vanzolinii Myers 1982

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 : 75-78

Ranitomeya vanzolinii Myers 1982

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

Figs. 3 , 4 , 9 , 23 (j, k), 28, 31

Tables 1, 4 – 6

Dendrobates quinquevittatus (non Steindachner, 1864)—Silverstone 1975 (partim): p. 33, Fig. 12 (drawing), pattern D and 14 (drawing), pattern E

Dendrobates vanzolinii Myers 1982: p. 9 , Fig. 4 , Table 1 [MZUSP 51597 collected by Paulo E. Vanzolini and Miguel Petrere at Pórto Walter on Rio Juruá, Acre, Brazil];— Vanzolini 1986; Caldwell & Myers 1990: p. 4; Caldwell 1997: p. 211, Fig. 1; Moreira et al. 1997; Caldwell & de Oliveira 1999: p. 565, Table 1 – 2, Figs. 1 – 3; Schulte 1999: p. 110, Fig. DB-032, DB-38; Symula et al. 2003: p. 452, Table 1, Figs. 1, 3 – 6 ; Christmann 2004: p. 6, Figs. on p. 36. 158; Pröhl 2005: p. 358, Table 1; Roberts et al. 2006a: p. 379, Table 1, Figs. 1, 4 ; Santos et al. 2009, by implication

Ranitomeya vanzolinii — Bauer 1988: p. 1; Grant et al. 2006: p. 171, Fig. 76; Lötters et al. 2007: p. 497, Figs. 498 – 629; von May et al. 2008a: p. 396, Appendix 2; Souza 2009: p. 31.

Background information. A population of R. vanzolinii from near Porto Walter, State of Acre, Brazil was the focus of intensive behavioral study ( Caldwell 1997; Caldwell & de Oliveira 1999) and included in several phylogenetic studies ( Symula et al. 2003; Grant et al. 2006). Little information has been published on other populations of this species. Some confusion exists regarding the taxonomic status of R. flavovittata , the sister species to R. vanzolinii (see R. flavovittata account for more details).

Tadpole. A total of seven tadpoles of Ranitomeya vanzolinii were collected from Porto Walter , Acre, Brazil, from 4–17 April 1996. A tadpole in Stage 38 ( OMNH 36057 ) was chosen for a complete description. All seven tadpoles were used to examine variation. These tadpoles ranged from stages 26 to 40, although not all stages were represented in the sample .

Description of OMNH 36057. Total length 27.8; body length 8.9; tail length 18.9, tail length 67.9% total length. Body depressed, maximum width 6.1, maximum depth 4.4. Snout broadly rounded in dorsal view, rounded in lateral view. Nares small, directed anterolaterally, 0.9 from tip of snout; internarial distance 1.6, interorbital distance 1.5. Distance from naris to anterior edge of eye 1.0, eye width, 1.4. Eyes dorsal, directed dorsolaterally.

Spiracle sinistral, short, 1.0, forming small tube free only on outer margin, opening directed posterodorsally 5.7 from tip of snout. Spiracle located 63.8% of body length from tip of snout, just below horizontal midline of body. Vent tube dextral, 0.5 in length.

Caudal musculature depth at body–tail junction 3.0; depth of musculature nearly uniform until it begins tapering at posterior one-third of tail. Upper fin originates 1.1 behind tail–body junction, upper fin at midtail 1.0, slightly deeper than lower fin at midtail, 0.8. Tail tip rounded, notochord ends 0.8 from end tail.

Oral disc emarginate, located ventrally, not visible from above. Transverse width oral disc 2.4, 38.9% of body width. Lower labium free from body wall. Short, conical papillae present on entire margin of posterior labium and laterally on anterior labium; most of anterior labium free of papillae. Papillae mostly in single row, double in few places. Lower jaw sheath broadly V-shaped, deeper than upper jaw sheath. Transverse width upper jaw sheath 1.1, 44.5% transverse width oral disc. Both upper and lower jaw sheaths with finely serrated cutting edges, serrations becoming smaller on proximal lateral processes of upper sheath, absent on ends of lateral processes.

Labial tooth row formula 2(2)/3(1). Labial tooth row A-1 complete, 1.5; A-2 with medial gap, 0.9, right half A- 2 length, 0.3, 20.0% of A-1. P-1 with medial gap, 0.1; right half P-1 length, 0.5, 44.6% of P-2; P-2 and P-3 equal in length, 1.1.

Variation. The two smallest tadpoles, stages 26 and 27, averaged 15.1 ± 1.2 total length. Four tadpoles in stages 34 to 38 averaged 24.8 ± 1.2 total length (range, 22.1–27.8). The single tadpole in early metamorphosis at stage 40 was 24.7; in this specimen tooth rows were becoming irregular, the spiracle opening is beginning to close, and the vent tube is partially absorbed.

Tail length as a percentage of total length averaged 62.8 ± 0.01 (range, 60.7–67.9). In the two smallest tadpoles, the upper fin originated at the tail–body junction, whereas in the five largest tadpoles, the fin was low at the tail–body junction, but began to increase in height at an average of 1.4 ± 0.2 (range, 1.0–1.8) behind the tail–body junction. Height of the upper and lower fins was nearly equal in the two smaller tadpoles (upper, 0.40 and 0.45; lower, 0.70 in both individuals). Height of the upper fin was slightly greater in the five larger tadpoles (upper, 1.12 ± 0.10, range 0.90–1.46; lower, 1.01 ± 0.10, range, 0.80–1.38). Tail musculature depth at the tail–body junction was 2.5 ± 0.2 (range, 2.1–2.9) in the five largest tadpoles.

Transverse width as a percentage of body width in the seven tadpoles averaged 39.4 ± 0.01 (range, 35.7–45.6). Transverse width of the upper jaw sheath as a percentage of the transverse width of the oral disc averaged 49.7 ± 0.01 (range, 44.5–55.6). A-2 gap is larger than the P-1 gap. Average percentage of the width of the A-2 gap compared to the total width of A-2 is 49.4 ± 0.04 (range, 37.1–60.5). Average percentage of the width of the P-1 gap compared to the total width of P-1 is 17.8 ± 0.04 (range, 8.3–33.6). P-2 and P-3 are nearly identical in length in 5 tadpoles in which both were normal and well-developed. In the smallest tadpole, P-3 was shorter than P-2 but may not have been fully developed. P-3 was deformed in one other tadpole; the ends of P-3 curved upward and fused with P-2.

Color in life (based on tadpole observed in a small treehole, later transferred to open-air laboratory). Body dark gray, tail musculature lighter gray, fins opaque light gray. Eye black. First observed 3 March, tadpole nearing metamorphosis by 21 March and had developed small light yellow spots on dorsum.

Color in preservative. Dorsum of body grayish brown. Venter opaque, intestinal coils dark grayish brown, some organs seen through venter light yellow. Tail musculature light yellow-brown. Back legs grayish brown. Fins translucent. Eyes black.

Natural history. Ranitomeya vanzolinii exhibits biparental care and likely, as observed in R. imitator , a monogamous mating system ( Caldwell & de Oliveira 1999). After one to two embryos hatch, the male carries the tadpoles on its back and deposits each individually in a phytotelm. Paired males and females remain together in small territories. Males call sporadically each day, and, on average, the female mate responds to his calls every 4.8 days. The male guides the female to their tadpole, they undergo some courtship behavior, and the female deposits two (usually) unfertilized trophic eggs, which the tadpole immediately consumes. The tadpoles are continually fed until metamorphosis. For a more detailed discussion of these behaviors and their evolution see Caldwell (1997) and Caldwell & de Oliveira (1999).

In the Reserva Extrativista do Alto Juruá (REAJ) and Parque Nacional da Serra do Divisor (PNSD) of Brazil, this species is frequently observed in primary forests during the rainy season, mainly in areas abundant in bamboo ( Guadua sp. ), bromeliads, and other phytotelmata (i.e. tree holes; Souza 2009). Adults frequently climb and jump on leaves, stems, and trunks of herbaceous vegetation up to 4 meters in height. In REAJ and PNSD this species uses bamboo internodes, the leaf axils of bromeliads, and other phytotelmata for tadpole deposition ( Souza 2009). In forests near Porto Walter, this species uses primarily cavities in small saplings and woody vines for tadpole deposition ( Caldwell & de Oliveira 1999).

Vocalizations. Like other members of this species group, the call of R. vanzolinii is a loud trill ( Fig. 28 ). Vocalization of Ranitomeya vanzolinii was studied at Porto Walter, Acre, Brazil, using two methods: recordings of males analyzed with Raven 1.3 (Cornell Laboratory of Ornithology, Ithaca, New York), and timing of vocalizations recorded during focal observations of males engaged in distinct behaviors. Focal observations were also made of vocalizing frogs defending territories.

Vocalizations of 9 individuals of R. vanzolinii were recorded with a Sony WMD-6 tape recorder. Temperatures at the time of recording ranged from 24.0–27.2 C. The number of calls analyzed from these recordings per individual varied from 2 to 10 (mean 6.8 calls/individual); calls were averaged within each individual, then across individuals to obtain means for each call variable. The call of R. vanzolinii is a short trill audible from> 5m. Mean number of calls per minute and call duration varied depending on the individual’s behavior (see below; Caldwell & de Oliveira, 1999). Mean number of pulses per call was 16.8 ± 1.7 (range, 8.6–23.8), and number of pulses per second was 31.3 ± 0.8 (range, 27.9–33.6). Dominant frequency ranged from 5162–5412 Hz (n = 7). Some calls revealed four harmonics; the lowest ranged from 2444–2745 Hz (n = 5).

During focal observations of males engaging in three behaviors, time of vocalization (to the second) was recorded using a stopwatch. The number of calls per minute as a measure of call rate was obtained during the following behaviors: 1) calling when no female was present; 2) calling when guiding a female to a tadpole rearing chamber; and 3) calling when inside a tadpole rearing chamber with a female. At times when calling from inside a tadpole rearing chamber (i.e., tiny vinehole or treehole), the calls given were much shorter and had only a few pulses, giving the call a drawn-out “creeking” sound. When calling alone, males vocalized at a rate of 3.41 ± 0.25 calls per minute (range, 0–11; n = 6). When calling while guiding a female, males called at a rate of 8.05 ± 0.32 (range, 0–17; n = 8), and when calling while inside a rearing chamber with a female, males vocalized at a rate of 3.13 ± 0.23 (range, 0–16; n = 7). Thus, males called more intensely when guiding a female to a rearing chamber than when calling alone (Mann-Whitney U-test, p <0.001), or when they were undergoing courtship behavior with a female inside a cavity (Mann-Whitney U-test, p <0.001). Call rate did not differ when males were alone compared to being in a rearing chamber with a female (Mann-Whitney U-test, p = 0.11). Call duration also varied depending on the male’s behavior. When alone, call duration averaged 0.721 ± 0.08 sec (range, 0.642 –0.799; n = 2), when guiding a female 0.378 ± 0.12 (range, 0.256 –0.500; n = 2), and when in a tadpole rearing chamber with a female 0.566 ± 0.09 (range, 0.291 –0.844; n = 5). Thus, when guiding a female, shorter calls were given at a faster rate.

Territories were maintained using vocal bouts in which two resident males in adjacent territories established posts about 2 m apart and alternated calls ( Caldwell and de Oliveira, 1999). In one such encounter in which the timing of vocalizations was recorded for 5 minutes, the bout (defined as number of sequential call given by a male before the other male called was 1.23 ± 0.63 calls (range, 1–5 calls). Calls were alternated between the two frogs 74 times during the 5-minute observation period.

Distribution. Ranitomeya vanzolinii is a widespread species occurring from premontane cloud forest (approximately 1300 m elevation) in southern Peru, eastward to lowland rainforests in Brazil. This species is frequently observed on the east versant of Cordillera El Sira (where it has been subjected to frequent collection from smugglers for the pet trade) and in western Brazil in the vicinity of Porto Walter, Acre state. The distribution of this species appears to overlap with other members of the vanzolinii group, i.e., R. sirensis in the south of Peru and possibly R. cyanovittata in far eastern central Peru. However to date, there are no localities where two species within the vanzolinii group have been registered. This species occurs in Amazonian rainforests of Brazil (States: Acre and possibly Amazonas) and Peru (Departments: Cusco, Pasco, Ucayali), Fig. 31 .

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 5. Andinobates Plate 1. minutus group: A–G: Andinobates claudiae and habitat (all from Bocas del Toro, Panama. Photos T. Ostrowski); A & B: Buena Esperanza; C–F: Isla Colon; G: Cerro Brujo; H: tadpole in phytotelm; I: habitat in Bocas del Toro, Panama. J–M: Andinobates minutus (all from Colombia. Photos DMV unless noted): J & K: Buenaventura, Valle del Cauca; L: Quibdó, Chocó; M: Baudó, Chocó (photo J. Mejía-Vargas). fulguritus group: N–V: Andinobates fulguritus (all from Colombia, photos DMV unless noted): N: Baudó, Chocó (photo J. Mejía-Vargas); O: Playa de Oro, Chocó (type locality); P–R: Uraba, Chocó. S–V: Anchicayá, Valle del Cauca. (nΦ = number of individual in phylogeny, Ω = population sampled in phylogeny).

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 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 12. Ranitomeya toraro sp. nov. type series. All specimens from two localities in Brazil: Amazonas state, municipality of Castanho, at km 12 on road to Autazes (ca. 40 km south of Manaus) or Scheffer Madeireira on Rio Ituxi, ca. 170 km southwest of Lábrea (labeled with ‡). Top row, from the collections of MPEG (L-R): 13839, 13838 (holotype), 13841, 13840, 13842 and 13037(‡). Bottom row, from the collections of OMNH (L-R): 37441, 37440, 36666 (‡), 37442, 37439, 36667(‡), 37438. Black bar = 20 mm (5 mm increments). Sequenced individuals (number in phylogeny): OMNH 36666 (7), OMNH 37440 (5), OMNH 36667 (6), MPEG 13841 (4)

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 31. Known distribution of Ranitomeya sirensis and R. vanzolinii. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).