Ranitomeya variabilis Zimmermann & Zimmermann 1988

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 : 86-90

Ranitomeya variabilis Zimmermann & Zimmermann 1988

Account authors: J.L. Brown, E. Twomey, E.H. Poelman, M. Pepper, M. Sanchez-Rodriguez, P. Perez-Peña Figures 3 , 4 , 9 , 14 , 32 (a – p), 33 (a – p), 34 (a – k), 37

Tables 1, 4 – 6, 8

Dendrobates minutus ventrimaculatus Shreve 1935 (partim): p. 213–214 [paratypes MCZ 19737, 19739 and LACM 44398 (formerly MCZ19741) collected by O.C. Felton in 1933 at “ Sarayacu, Ecuador ”; paratypes MCZ 19685 and MCZ 19689, collected by C. Spencer between January 1931 and August 1932 “along the Pastaza River from Canelos to the Maranon river , Ecuador ”]

Dendrobates quinquevittatus (non Steindachner 1864)— Crump 1971; Silverstone 1975 (partim): p. 35; Duellman 1978: p. 125, Plate 1; Lescure & Bechter 1982: p. 26; 1983; Myers 1982: p. 13, Fig. 7 ; Zimmermann & Zimmermann 1988: p. 132, Schulte 1999: p. 48, Fig. DB-050.

Dendrobates ventrimaculatus (non Shreve 1935) — Daly et al. 1987: p. 1025; Schulte 1999: p. 129; Caldwell & Myers 1990: p. 17; Summers & Amos 1997: p. 261; Fujitani et al. 1998: p. 74; Summers 1999: p. 557, Figs. 1–7; Summers & Earn 1999: p. 517; Summers & Symula 2001: p. 17; Symula et al. 2001: p. 2415, Table 1, Figs. 1–3; 2003: p. 453, Figs. 1–6;; Cisneros-Heredia 2003; Christmann 2004: p. 5, Figs. on p. 15, 42, 98, 100, 147, 151; Brown et al. 2006: p. 55, Table 2, Fig. 1; 2008a: p. 1157; 2008b: p. 2; 2009b: p. 478; Noonan & Wray 2006: p. 1008, Table 2, Figs. 4 , 5 ; Roberts et al. 2006a: p. 378, Table 1, Figs. 1, 3 , 4

Dendrobates variabilis Zimmermann & Zimmermann 1988: p. 132 [SMNS 7054 (holotype) collected by Rainer Schulte from "Departamento San Martín, Peru "; restricted to "km 27 auf der Strasse von Tarapoto nach Yurimaguas" by Henle 1992: p. 102];— Caldwell & Myers 1990: p. 17; Henle 1992: p. 102; Schulte 1999: p. 39 –46, Figs. DB-067, DB-044, DB-063, DB- 009; Summers & Earn 1999: p. 517; Symula et al. 2001: p. 2415, Table 1, Figs. 1–3, 2003: p. 453, Figs. 1–6; Lötters et al. 2003: p. 1909; Christmann 2004: p. 5, Figs. on p. 25, 121; Noonan & Wray 2006: p. 1008, Table 2, Figs. 4 , 5 ; Roberts et al. 2006a: P. 378, Table 1, Figs. 2–4 ; Brown et al. 2006: p. 55, Table 2, Fig. 1; 2008a: p. 1140, Table 1; 2008b: p.1, Table 1, Figs. 1 – 3; 2009b: p. 478, Tables 1 – 4, Fig. 3 ; 2009c: p. 148, Fig. 1; Santos et al. 2009, by implication

Ranitomeya variabilis — Grant et al. 2006: p. 171, Fig. 76, Fig. 76; Lötters et al. 2007: p. 500, Figs. 630 – 633; Brown et al. 2008c: p. 9; 2009a: p. 1877, Table 1, 2010: p. 436, Figs. 1, 2 , 4 , 5 ; Perez-Peña et al. 2010: p. 18, Fig. 13 ; Schulte et al. 2010

Ranitomeya ventrimaculata (non Shreve 1935)— Grant et al. 2006: p. 171, Fig. 76; Lötters et al. 2007: p. 504, Figs. 634, 636, 637; Brown et al. 2009a: p. 1877, Table 1; Perez-Peña et al. 2010: p. 18, Fig. 13

Background information. Technically, this species did not receive a formal taxonomic name until Zimmermann & Zimmermann (1988) described a morph of this species as Dendrobates variabilis . Prior to that, most members of this group were referred to as Dendrobates ventrimaculatus or Dendrobates quinquevittatus . Shortly after its description Caldwell & Myers (1990) stated “at present it is not diagnosable from all other populations of D. ventrimaculatus s.l. ” and considered Dendrobates variabilis sensu Zimmermann & Zimmermann (1988) as a junior synonym of Dendrobates ventrimaculatus Shreve 1935 . Symula et al. (2003) responded to Caldwell & Myers’ synonymy, stating “there are acoustic differences between the advertisement calls of D. variabilis and D. ventrimaculatus … Furthermore , D. variabilis is restricted to the summits of mid-level mountains, whereas D. ventrimaculatus is confined to lowland habitats”. They urged future research, particularly hybridization studies, before a conclusion on the specific status could be reached. Certainly, R. variabilis sensu Zimmermann & Zimmermann (1988) and nearby lowland populations of R. ventrimaculata sensu Schulte (1999) have diverged from each other in some regards (as is apparent in their morphology); however, unlike stated by Symula e t al (2003), we are not able to recover any consistent acoustic differences between R. variabilis sensu Zimmermann & Zimmermann (1988) and nearby populations of R. ventrimaculata sensu Schulte (1999) ; (see R. amazonica account for discussion of acoustic differences between R. variabilis and R. amazonica ).

Interestingly, we have found evidence of four independent origins of “spotted highland” populations (i.e., morphologically similar to variabilis sensu Zimmermann & Zimmermann 1988 ) in our molecular phylogenetic analyses. To reconcile the monophyly of either species ( R. ventrimaculata sensu Schulte (1999) and R. variabilis sensu Zimmermann & Zimmermann (1988) —using only the type populations), so that each is a distinct species, several additional populations would have to be elevated to specific status. Based on the lack of phylogenetic and acoustic data and consistent morphological or ecological differences, we consider R. variabilis sensu Zimmermann & Zimmermann (1988) to be synonymous with R. ventrimaculata sensu Schulte (1999) . Because members of this group were erroneously considered R. ventrimaculata (see R. ventrimaculata acount), the name R. variabilis gains precedence.

The evolution of spots seems to coincide with the transition to montane forests from lowland ancestors. The exact cause of this trend is unclear and not all montane populations are spotted; however, generally speaking the trend is prevalent. Additionally, we do not have molecular data for several populations of R. variabilis sensu Zimmermann & Zimmermann (1988) . To further complicate the situation, it is common within populations of spotted frogs to observe transitional morphs or an entirely lowland morph. This phenomenon gets to the heart of the problems scientists face when trying to clarify the taxonomy of this group. Under any species criterion, no taxonomy can portray the diversity scientists perceive with complete satisfaction. This species is highly nomadic and appears to be tolerant of suboptimal habitats (in terms of geology, climate and reproductive resources) and is often found in areas unoccupied by any other Ranitomeya (e.g., seasonally flooded forests). This behavior likely reduces the possibility of isolation for periods long enough to result in speciation. Thus, like R. sirensis (sensu this paper), these groups appear to be widely dispersed species with the propensity for local adaptation– though not enough to result in complete speciation.

Definition and diagnosis. Assigned to the genus Ranitomeya due to the combination of the following characters: adult SVL <18.0 mm, dorsal coloration conspicuous, dorsolateral stripes present (in lowland populations), stripes complete when present, 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. Adults use arboreal phytotelmata for reproduction and deposit eggs above or in water. Two main morphs of this species are currently known: (i) the Highland morph ( R. variabilis sensu Zimmermann & Zimmermann 1988 , Fig. 32a – p ) and (ii) the Lowland morph ( R. ventrimaculata sensu Schulte 1999 , Figs. 33a – p , 34a – k ). All morphs possess a large black spot on the snout, anterior to orbits:

(i) The Highland morph possesses regular yellow-green reticulation, creating ovoid and large black spots on dorsum. The dorsal coloration often transitions from yellow-green anteriorly to blue-green posteriorly. Venter and limbs are green to blue and typically are evenly stippled with medium to large black spots. The throat is yellow and gular spots are commonly present. This morph is known to occur within rainforests in Ecuador (Province Morona- Santiago) and Peru (Department Amazonas, San Martín, Pasco).

(ii) The Lowland morph has thin yellow dorsolateral, middorsal and oblique lateral stripes. The ventrolateral and dorsolateral stripes are typically complete; however, the middorsal stripe typically terminates around the axilla and creates a distinctive black ‘Y’ on the dorsum ( Fig. 2 g-i). In some populations, dorsal coloration is orange (e.g., near Varadero, Department Loreto, Peru); middorsal stripe is largely complete (e.g., populations near Shamboyacu, Department San Martín, Peru); or dorsolateral and oblique lateral stripes fuse near the axilla (e.g., populations near Pongo de Cainarachi, Department San Martín, Peru; Quebrada Blanco, Department Loreto, Peru; Puyo, Province Morona-Santiago, Ecuador). The ventral and limb coloration is typically blue-green to light gray to blue. The limbs and venter are finely reticulated. This morph occurs predominantly though the lowland forests adjacent to eastern Andean versant, though some populations also occur far from mountains (e.g., those in La Pedrera, Department Vaupés, Colombia; Rio Tahuayo , and Contamana, Department Loreto, Peru). This morph is known from the rainforests of Brazil (State Amazonas), Colombia (Departments Amazonas, Caquetá, Putumayo (tentative), Vaupés), Ecuador (Provinces Napo, Orellana, Pastaza, Sucumbíos) and Peru (Departments Amazonas, Loreto, San Martín, Ucayali) .

The highland morph is similar in appearance to the local R. imitator and in some populations is involved in a mimicry complex, however, populations of R. imitator that are similar in appearance possess paired nose spots (versus a single nose spot in R. variabilis ). For a detailed list of characters see Brown et al. (2008b). The lowland morph is similar in appearance to R. amazonica , R. toraro sp. nov. and some populations of R. imitator , R. ventrimaculata and R. sirensis . Ranitomeya variabilis lacks a large belly spot (present in R. sirensis ) and bears a conspicuous black ‘Y’ on the dorsum (versus stripes parallel and extending to vent in R. toraro , R. imitator , R. sirensis and R. uakarii ). Distinguishing the lowland morph of R. variabilis and R. amazonica can be difficult if nothing is known about the origin of the individual. Where the species co-exist near Iquitos, R. variabilis typically has thin-yellow dorsal stripes and R. amazonica has broad bright red or orange dorsal stripes (though they can also be yellow). Individuals of R. amazonica from the Guiana Shield are almost identical in appearance to some R. variabilis individuals from Pongo de Cainarachi or Quebrada Blanco in Peru, possessing thin-yellow dorsolateral stripes that fuse with the ventrolateral stripe near the axilla. To confidently identify these populations, genetic or locality data must be used.

Ranitomeya (sensu Grant et 13 100/2.41 98/100 100/42/* Med-High (86) al. 2006)

Tadpole. The description is based on a tadpole from the Cainarachi Valley , San Martín, Peru. Mouthparts were verified in three individuals from same locality .

Tadpole in stage 28; no external gills; feeding on detritus. Body ovoid in dorsal view, wider near mouth. Total length 18.1; body length 8.6; tail length 9.5, 52% of total length. Body width 5.2; body depth 3.1, 60% of body width. Eyes well developed; naris small; distance from naris to anterior edge of eye 1.6. Eye positioned dorsally on head, directed dorsolaterally. Spiracle well developed, sinistral; vent tube dextral.

Tip of tail bluntly rounded. Tail muscle height at base of tail 1.8; tail muscle width at base of tail 1.3; maximum tail height 2.0. Dorsal and ventral fins approximately same height.

Oral disc ventral, emarginated, transverse width 1.9, 37% 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 (1/3 total width of A-1); P-1 on lower labium with narrow medial gap; P-2 width equal to P- 1; P-3 75% width of P-1.

Color in life. Head and body gray, mouthparts visible from above. Abdomen mostly transparent; intestinal coils black. Tail musculature uniform gray, dorsal and ventral fins opaque gray.

Natural history. Zimmermann & Zimmermann (1984) reported that captive specimens of R. variabilis exhibited biparental care. In contrast, observations in the field indicate that this species has a promiscuous mating system: unrelated tadpoles are commonly deposited within the same phytotelm and females do not return to pools to perform egg-feeding. Oviposition usually takes place at the edge of the water within phytotelmata; clutches contain 3 – 6 eggs. After 10 – 15 days, the male transports tadpoles to separate small phytotelmata, where they are deposited individually and thereafter abandoned (Summers 1999; Summers & Amos 1999; Lötters et al. 2007; Brown et al. 2008b). Alternatively, within the same population, clutches can be abandoned shortly after reproduction and all the tadpoles fall into the pool below, often resulting in cannibalism of all but one tadpole ( Brown et al. 2008b). The degree of embryo cannibalism varies between populations. Near Tarapoto, Peru, tadpoles were never observed cannibalizing embryos that were deposited in their pools ( Brown et al. 2008a, 2009c), whereas in populations from Sucumbíos Province, Ecuador, tadpoles were frequently observed cannibalizing embryos (Summers 1999, Summers & Amos 1999). In both populations, the tadpoles would frequently consume other congeneric tadpoles.

This species occupies primary and secondary forests where bromeliads are abundant. It commonly breeds in Guzmania spp. and Aechmia spp. Occasionally this species has been observed breeding in tree holes and in the axils of Heliconia , Dieffenbachia and Xanthosoma plants. Most individuals are transient and in mark-and-recapture studies they demonstrate little site fidelity (Summers & Amos 1999, Brown et al. 2009b).

Vocalizations. The call of R. variabilis is a series of short buzz notes, note range 0.14 – 0.44 sec in length, repeated at 34 – 62 notes per minute.

Distribution. This species occurs in Amazonian rainforests of Brazil (States: Amazonas), Colombia (Departments: Amazonas, Caquetá, Putumayo (tentative), Vaupés), Ecuador (Provinces: Morona-Santiago, Napo, Orellana, Pastaza, Sucumbíos) and Peru (Departments: Amazonas, Loreto, San Martín, Ucayali), Fig. 37 .

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

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 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 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 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 14. Advertisement calls of Ranitomeya species in the variabilis group and defleri group. A. Ranitomeya amazonica from 23 km S Iquitos, Loreto, Peru (type locality), recorded at 26° C; B. Ranitomeya amazonica from French Guiana, unknown temperature (call courtesy Erik Poelman); C. Ranitomeya variabilis from Cainarachi valley, San Martín, Peru, recorded at 22° C. D. Ranitomeya variabilis from Cerro Yupatí, Amazonas, Colombia, recorded at 27° C; E. Ranitomeya variabilis from Saposoa, San Martín, Peru, recorded at 24.5 C; F. Ranitomeya defleri from Rio Apaporis, Vaupés, Colombia, recorded at 26° C.

FIGURE 32. Ranitomeya Plate 11. variabilis group. A–P: Ranitomeya variabilis (Highland morph): A: Chazuta, San Martin, Peru; B–G: Upper Cainarachi Valley, San Martin, Peru (Ω); H & I: Borja, Loreto, Peru (24, 46Φ); J: Parque Nacional Ichigkat Muja, Amazonas (D. Rodriquez-Mercado); K: Saposoa, San Martin, Peru (Ω); L: Comparision between Saposoa and upper Cainarachi Valley populations (respectively); M: Xanthosoma sp. that was being used by R. variabilis for tadpole and egg deposition near Saposoa, San Martin, Peru; N: Saposoa, San Martin, Peru (Ω); O: Tocache, San Martin, Peru (C. Torres); P: Macas, Morona Santiago, Ecuador (J. Verkade, Ω). (nΦ = number of individual in phylogeny, Ω = population sampled in phylogeny).

FIGURE 33. Ranitomeya Plate 12. variabilis group: A–P: Ranitomeya variabilis (Lowland morph): A: Contamana, Loreto, Peru (42Φ); B: Shamboyacu, San Martin, Peru (41Φ); C: Lower Huallaga Canyon, San Martin, Peru (‡); D: Callanayacu, San Martin, Peru(‡); E: Barranquita, San Martin, Peru (‡); F: Pongo de Cainarachi, San Martin, Peru (7,8,11Φ); G & H: Bonilla, San Martin, Peru (1,3, 9 Φ); I & J: Varadero, Loreto, Peru (27Φ); K: Quebrada Blanco, Loreto, Peru (Ω); L: Rio Boncuya, Loreto, Peru (G. Gagliardi); M: Upper Rio Nanay, Loreto, Peru; N: Middle Rio Nanay, Loreto, Peru; O & P: Archidona, Napo, Ecuador (EHP and J. Verkade). (nΦ = number of individual in phylogeny, Ω = population sampled in phylogeny).

FIGURE 34. Ranitomeya Plate 13. variabilis group: A–K: Ranitomeya variabilis: A: Archidona, Napo, Ecuador (J. Verkade); B– D: Macuma, Morona-Santiago, Ecuador (J. Verkade and EHP); E &F: Puyo, Pastaza, Ecuador (j. Verkade) G: Yupati, Vaupés, Colombia (14 Φ); H: Embryos, Archidona, Napo, Ecuador (J. Verkade); I: Breeding pair of R. variabilis, Archidona, Napo, Ecuador (J. Verkade); J & K: Yupati, Vaupés, Colombia (14-16 Φ). L–Q: Ranitomeya amazonica: L: Km 41 Iquitos, Loreto, Peru (ET, 26Φ); M: Km 31 Iquitos, Loreto, Peru (PPP); N & O; Km 26 Iquitos, Loreto, Peru (ET, 25, 27Φ); P: Upper Rio Mazan-Pintuyacu, Loreto, Peru (J. J. Lopez-Rojas); Q: Lower Rio Mazan, Loreto, Peru (J. J. Lopez-Rojas). (nΦ = number of individual in phylogeny).

FIGURE 37. Known distribution of Ranitomeya variabilis. The inset map displays the geographic extent of distributions (black circles = all other Ranitomeya).