Ranitomeya defleri, Twomey, Evan & Brown, Jason L., 2009

Twomey, Evan & Brown, Jason L., 2009, Another new species of Ranitomeya (Anura: Dendrobatidae) from Amazonian Colombia, Zootaxa 2302, pp. 48-60 : 50-58

Ranitomeya defleri sp. nov.

Figures 1–3

Dendrobates quinquevittatus (non Steindachner): Silverstone 1975 (partim) p. 20, Fig. 14, pattern F, (MCZ 28061)

Holotype. MCZ 28061, an adult male collected by I. Cabrera on 31 March 1952 at “Río Apaporis, Colombia ”.

Paratypes. All from Colombia. Vaupés: JLB 08-001, collected by J. Brown and E. Twomey, 6 August 2008, north bank of Mosiro Itájura (an oxbow lake off Río Apaporis, also known as ‘Lago Taraira’), 98 m elevation, 1° 4' 37.46" S, 69° 30' 51.34" W; approximately 0.2 km SW of Estación Biológica Caparú; JLB 08- 0 0 2, collected by J. Brown and E. Twomey, 7 August 2008, Departamento Vaupés, Colombia (same locality as JLB-001); JLB 08-003, collected by J. Brown and E. Twomey, 8 August 2008 (same locality as JLB 08- 001). Amazonas: JLB 08-004, collected by J. Brown and E. Twomey, 4 August 2008, north bank of Río Caquetá near Puerto Córdoba (a village 16.6 km NW from La Pedrera), 68 m elevation, 1° 16' 51.63" S, 69° 43' 10.36" W.

Etymology. The epithet is a patronym for Dr. Thomas Defler, an American primatologist who has worked for 32 years in Colombia. Dr. Defler founded Estación Biológica Caparú in 1983; since that time the station has served as an important outpost for biologists working in Amazonian Colombia.

Definition and diagnosis. Assigned to the genus Ranitomeya due to the combination of the following characteristics: small size (<20 mm SVL), first finger distinctly shorter than second, dorsal coloration conspicuous and bright, dorsal skin smooth, toe webbing absent, maxillary and premaxillary teeth absent, pale limb reticulation present. Ranitomeya defleri is a relatively small species of Ranitomeya , adult SVL of approximately 15–18 mm. Dorsal body and head are black with irregular yellow markings; pale yellow-green vertebral stripe present on posterior two-thirds of dorsum. Limbs and venter are black with pale to bright blue reticulation forming round black spots on the limbs and irregular spots on the venter. Underside of head has a yellow ‘hourglass’ shape. Teeth absent; finger I shorter than finger II; disc of third finger 2.2–2.6 times wider than finger width. Tadpole gray, ovoid, with irregular yellow markings present from early in development.

Ranitomeya defleri can be distinguished from all other dendrobatids by its distinctive color pattern. Other species with which it could be confused include R. flavovittata , R. vanzolinii , and R. ventrimaculata . Ranitomeya flavovittata has highly variable dorsal markings consisting of yellow dots and dashes on a black ground color, similar to R. defleri . However, R. flavovittata lacks the large yellow blotches behind the eyes as in R. defleri . Also, the legs and venter of R. flavovittata have a pale blue or gray reticulum (vs. dark blue in R. defleri ). Ranitomeya vanzolinii has a dorsum covered in small yellow spots which are sometimes fused forming dashes, but this species lacks a pale median stripe on the dorsum as found in R. defleri . Furthermore, R. vanzolinii has a yellow patch on the venter and lacks the yellow ‘hourglass’ found under the chin of R. defleri . Both R. vanzolinii and R. flavovittata share a similar call (a loud ‘trill’ similar to that of R. imitator ) which differs from the buzz call of R. defleri . Ranitomeya ventrimaculata is a fairly variable species, but the form found throughout most of Amazonian Peru and Colombia (including near La Pedrera) can be described as having a yellow dorsum with a conspicuous black “ Y ” which starts at the rump and terminates above the eyelids. This species also lacks the pale median stripe found in R. defleri and has coarser black spotting on the limbs and venter. The only other species of Ranitomeya we found occurring near R. defleri was R. ventrimaculata . In addition to differences in color pattern, these two species can be differentiated on the basis of their advertisement calls ( Table 1). Ranitomeya ventrimaculata has an advertisement call consisting of a series of buzz-like notes, each note 0.174 sec in duration, notes spaced 0.88 sec apart, notes pulsed at a rate of 143 pulses/sec. In R. defleri , notes are much longer (0.510 sec in duration), more spaced out (1.44 sec apart), and pulsed at a slower rate (98 pulses/sec).

ventrimaculata . Calls of R. ventrimaculata were chosen so there was one representative from the nearest population to R.

defleri (Yupatí, Departamento Vaupés, Colombia), one representative from the Iquitos-French Guiana clade (Iquitos,

Departamento Loreto, Peru), and one representative from the east-Andean versant clade (Shucushuyacu, Departamento

Loreto, Peru). Measurements are based on mean values in a call series from a single individual.

Call parameters

Measurements (in mm) of holotype. The male holotype has SVL 16.9; FL 7.0; TL 7.3; KK 14.2; FoL 6.3; HaL 4.5; HL 5.0; HW 5.2; BW 5.5; UEW 1.5; IOW 1.4; IND 1.5; TD 0.74; ED 1.26; DET 0.32; L1F 1.16; L2F 1.53; W3D 0.53; W3F 0.21. For paratype measurements see Table 2.

MCZ JLB08 JLB08 JLB08 JLB08

Character 28061 0 0 1 0 0 2 0 0 3 0 0 4 Average SVL 15.0 15.4 15.5 15.3 17.7 15.8 ± 1.1 FL 7.0 7.2 7.3 6.9 8.2 7.3 ± 0.5 TL 7.3 7.6 7.2 6.7 8.4 7.4 ± 0.6 KK 14.2 14.6 14.9 13.3 16.6 14.7 ± 1.2 FoL 6.3 5.6 6.6 6.0 7.5 6.4 ± 0.7 HaL 4.5 4.1 4.1 3.9 5.1 4.3 ± 0.5 HL 5.0 5.3 5.0 5.3 7.2 5.6 ± 0.9 HW 5.2 4.9 5.0 4.9 5.5 5.1 ± 0.3 BW 5.5 4.7 5.7 4.6 5.6 5.2 ± 0.5 UEW 1.5 2.8 2.6 2.1 3.0 2.4 ± 0.6 IOW 1.4 2.8 2.8 2.5 3.6 2.6 ± 0.8 IND 1.5 2.3 2.3 2.1 2.7 2.2 ± 0.4 TD 0.74 0.97 0.87 0.86 0.96 0.88 ± 0.09 ED 1.26 2.10 2.10 2.29 2.20 1.99 ± 0.42 DET 0.32 0.39 0.53 0.41 0.51 0.43 ± 0.07 L1F 1.16 1.82 1.81 1.67 2.00 1.69 ± 0.32 L2F 1.53 2.43 2.43 2.34 2.80 2.31 ± 0.47 W 3D 0.53 0.98 0.80 0.81 0.86 0.80 ± 0.17 W 3F 0.21 0.42 0.33 0.37 0.33 0.33 ± 0.08 Description of holotype. Widest part of head is at jaw articulations. Head slightly narrower than body. Tongue ovoid; teeth absent. The holotype is notable in that its pattern is approximately symmetrical on right and left halves. In preservative, the head is black with large, pale yellow dorsolateral spots behind each eye, snout is yellow anterior from orbits. On the snout, a black “U” connects nares through loreal region; creating a yellow spot on the tip of the snout and a thin yellow stripe just anterior to the eyes which crosses the head and terminates on the upper lips. Dorsum black with two yellow dorsolateral dashes on either side; thin, irregular yellowish-gray vertebral stripe extending from vent to approximately 2/3 distance towards eyes. There is a weakly-defined pale yellow spot on the dorsal surface of the axilla, extending partially onto the anterior flank; another yellow spot is present at the corner of the mouth. The arms, legs, and toes are covered in a pale gray reticulum (presumably blue in life) over a black ground color, creating round black spots; toes are gray. Underside of head yellowish-gray with lateral black gular spots, creating appearance of a pale hourglass. Lower lip color matches color of dorsolateral dashes. Venter black with discrete gray reticulation, creating black spots, much like the limbs. Iris black.

In preservative, skin texture nearly smooth on the dorsal surfaces of the body and head; limbs and rump weakly granular. Venter weakly granular on limbs and body, ventral surface of head nearly smooth. Snout sloping and rounded in lateral profile, round or slightly blunted in dorsal profile. Nares situated at tip of snout and directed laterally; both nares visible from ventral and anterior view but not from dorsal view. Canthus rostralis rounded, loreal region flat and nearly vertical. Upper eyelid approximately equal in width to interorbital distance; internarial distance roughly equal to eye width. Tympanum round, partially concealed posterodorsally.

Hands relatively large, length 28.1 % of SVL. Relative length of appressed fingers III> IV> II> I; first finger 75.8 % length of second; finger discs moderately expanded, width of disc on finger III 2.5 times width of adjacent phalanx. An unpigmented median metacarpal tubercle is present on base of palm; inner metacarpal tubercle present near base of finger I; unpigmented proximal subarticular tubercles present on base of each digit, except on finger I, where tubercle is part-way up the digit; distal subarticular tubercle visible only on fingers III and IV. All tubercles raised above level of hands; scutes present on dorsal surface of fingers.

Hind limbs moderate length, with heel of appressed hind limbs reaching level of eye. Femur and tibia roughly equal in length, tibia 1.04 times length of femur; knee-knee distance 88.8 % of SVL. Relative lengths of appressed toes IV> III> V> II> I; first toe short with unexpanded disc; second toe with slightly expanded disc, discs on toes III–V moderately expanded. Two unpigmented metatarsal tubercles present on base of foot, one situated medially near base of toe I, the other situated laterally at the base of the fifth metatarsal. Proximal subarticular tubercles present at base of each toe but most notable on toes I and II due to their lack of pigmentation. Toes III and V with two subarticular tubercles, toe IV with three subarticular tubercles. A tarsal keel is present starting below the ankle and turning into the medial metatarsal tubercle at the foot. Tarsal tubercle absent; feet and hands lacking webbing and lateral fringing.

Variation. Adult males range from 15.3–17.7 mm SVL, females unknown. Head width 87–104 % of body width; head width 31–33 % of SVL. Tibia can be longer or shorter than femur; TL/FL ranges from 0.97 to 1.05. Knee-knee distance 87–96 % of SVL.

The type series ( Fig. 2 ) displays substantial variation in color pattern and most individuals are not as symmetrical as the holotype. For example, JLB08-004 has a vertebral stripe which connects to the right eyespot (vs. terminating mid-dorsum in the holotype), has only one elongate dorsolateral dash on either side (vs. two dashes in the holotype), and has whitish axillary spots (vs. yellow in the holotype). JLB08-001 lacks a defined “U” on the snout as in the holotype; rather, it has an irregular yellow blotch on the right side of the head which connects with the right eye spot. JLB08-003 also lacks a “U” on the snout, possesses irregular spots on the flanks (vs. regular and symmetrical dashes in the holotype), and has a vertebral stripe with small lateral branches (vs. branches absent in the holotype). We should note that the sketch of the holotype presented in Silverstone 1975 (p. 20, Fig. 14, pattern F) is drawn inaccurately; this was also mentioned by Myers (1982): “the Colombian frog [= MCZ 28061] is inaccurately drawn. The artist unfortunately omitted a pale vertebral line which was still conspicuous on the specimen when I saw it in 1980.” This pale vertebral line was still visible as of 2009.

Tadpole: A stage 29 tadpole was used for the description. This tadpole was collected on 4 August 2008 from the bromeliad in which one of the paratypes (JLB08-004) was calling. Total length 19.6 mm, body length 7.1 mm, body width 4.4 mm. Snout rounded when viewed from above; body ovoid in dorsal view. Eyes black and conspicuous, dorsal, angled anterolaterally, pupils white in preservative. Nares not forming tube, situated half-way between eye and tip of snout, directed anterolaterally. Spiracle sinistral; vent dextral. Maximal tail height 2.9 mm measured half-way along tail length. Ventral tail fin begins at tail base, dorsal tail fin begins just posterior to plane of vent opening, ventral and dorsal fins relatively uniform in thickness throughout tail, tapering towards tip. Maximum musculature height 1.7 mm measured at tail base; height uniform throughout, tapering towards tip.

The mouth ( Fig. 3 ) is directed anteroventrally. Oral disc emarginate, anterior and posterior labia forming flaps free from body wall, 1.5 mm in width. Marginal papillae absent on anterior labium except for lateralmost portion (4-6 papillae present), present on posterior labium in one row but with a distinct medial gap. Papillae white, conical; submarginal papillae absent. Jaw sheaths deep in longitudinal width, serrate, posterior sheath has a curved medial indentation. Lateral processes short, extending slightly past lower jaw. Labial tooth row formula is 2(2)/3(1). A-1 complete, A-2 with broad medial gap, same width as A-1. P-1 with small medial gap, P-2, and P-3 complete; P-1 and P-2 equal width, P-3 slightly shorter.

In preservative, pigmentation on the head and dorsum is mottled brown with a white ground color. This mottling is most dense on the vertebral region and head, less dense around the sides. Ventral coloration is almost entirely white, although small black melanophores are visible under a dissecting microscope. These melanophores cover the venter uniformly, with the exception of the mouthparts and vent tube, which lack any dark markings. The gut appears pale brown and is visible through the skin. Tail musculature pale brown, fins translucent white. The entire tail is covered with a faint reticulation of pale brown that is more dense around the musculature and less dense around the fins and the distal region of the tail. The tadpole had conspicuous dorsal markings in life, although these have faded in preservative. These markings were yellow in life; dorsal ground color in life was gray.

Vocalizations. On 6 August 2008 in Caparú we heard “a call that sounded like a ventrimaculata but quieter and longer with notes more spaced-out” (ET, field notes). This frog was collected and later designated a paratype. Although this individual ceased calling before we could obtain a recording, two days later we recorded another individual calling from the exact same spot. We were unable to capture this individual, but the call sounded similar to the call of the paratype. Furthermore, we are confident this call belongs to R. defleri (rather than R. ventrimaculata ) because we witnessed the paratype from Puerto Córdoba making a similar call immediately prior to collection, and because we never found R. ventrimaculata in Caparú. The following call description is thus based on a recording of a single (uncollected) male; sample sizes refer to the number of individual notes (or spaces between notes) used for the analysis. Call data is reported as means, where n is the number of notes used to calculate the mean.

The advertisement call of R. defleri is a series of buzz-like notes ( Fig. 4 A) with the following parameters: mean note length 0.510 sec (n = 19); note spacing 1.44 sec (n = 15); dominant frequency 5357 Hz (n = 6); pulses per note 52.8 (n = 6); pulse rate 99.2 pulses/sec (n = 6). This species appears to call in weakly defined ‘bouts’ which consist of 3–8 regularly-spaced notes; pauses between bouts were typically 3 sec or more. Mean notes per bout 4.7 (n = 10 bouts); mean bout duration 8.31 sec (n = 10 bouts). Within a bout, notes are repeated at a mean rate of 1 note per 1.77 sec.

The call of R. defleri sounds similar to the call of R. ventrimaculata , but the latter species clearly differs in that notes are much shorter and more closely spaced. On 5 August 2008, we recorded a R. ventrimaculata from Cerro Yupatí, a 405 meter-high hill on the north bank of Río Caquetá just across the river from La Pedrera. This call is also a series of buzz-like notes ( Fig. 4 B); mean note length 0.174 sec (n = 23); note spacing 0.88 sec (n = 12); dominant frequency 5368 Hz (n = 9); pulses per note 25.7 (n = 9); pulse rate 143.5 pulses/sec (n = 9). This species also appears to call in weakly defined bouts consisting of 3–13 regularlyspaced notes; pauses between bouts are usually 6 sec or more. Mean notes per bout 7 (n = 6); mean bout duration 6.62 sec (n = 6). Within a bout, notes are repeated at a mean rate of 1 note per 0.95 sec. We have analyzed the calls of an additional 21 R. ventrimaculata individuals from throughout most of its range, and the overall mean note length for this species is 0.27 sec, roughly half the length of R. defleri notes.

Distribution and natural history. Ranitomeya defleri occurs in southeastern Colombia, where it is known from only two localities ( Fig. 5 ) 32 km apart (Euclidean distance). This species likely occurs more widely throughout the Apaporis-Caquetá drainage (including in Brazil), although further sampling is needed to determine the extent of its distribution. Since much of the forest in the Apaporis region is seasonally flooded, this species may be absent from low-lying areas such as igapó forests. When we visited this region in August of 2008, nearly all of the forest south of the Caquetá was flooded several kilometers inland. It is possible that these large expanses of flooded forest may impose a southern limit to the distribution of this species, as we were unable to find R. defleri in La Pedrera (located on the south side of Caquetá) or in the forests around Leticia and Puerto Nariño. It does appear, however, that R. defleri occurs in very low-lying forests, as the Puerto Córdoba locality was just a few meters above the flood zone.

The sites where we found R. defleri were generally undisturbed, primary forests. These forests are located in the “Caquetá Moist Forest” ( Millikin 2008), one of the world’s eco-regions as defined by the World Wildlife Fund. Caparú has a mean annual temperature of 25.1° C ( Defler 1996), with a mean annual rainfall of 3836 mm ( Defler and Defler 1996). There is little seasonal variation in rainfall, with the driest month (September) receiving 258 mm rainfall on average, compared to an average monthly precipitation of 319 mm ( Defler and Defler 1996). Forests along Río Apaporis and near La Pedrera appear to have had little or no impact from humans. Caparú is one of the most pristine examples of lowland rainforest we have seen, with many large trees and a relatively sparse understory with little light penetration ( Fig. 6 ). The canopy in the sites where the frogs were found is dominated by trees of the families Fabaceae (legumes), Moraceae (figs), Euphorbiaceae (spurges), and Arecaceae (palms) ( Defler and Defler 1996). The understory consists mostly of large palms and tree saplings, and the ground is covered by a thick, wet leaf litter. Most woody surfaces in the understory are covered with moss, yet very few bromeliads can be found despite these wet conditions. The most common bromeliads are a slender, spiny species which grow on the sides of trees, forming small clumps of 2–4 plants. These bromeliads are small, approximately 8 inches tall by 6 inches in diameter, but contain a substantial volume of water in their central axil (mean = 32 ml, range = 20–42 ml, n = 4). In Caparú, we were unable to find tadpoles of R. defleri , but we did find an R. defleri tadpole in Puerto Córdoba in one of these bromeliads. Additionally, we found tadpoles in a site at the western foot of Yupatí (Angosturas in Fig. 5 ), which may belong to R. defleri based on color pattern. These tadpoles were found in the central axil of a similarly-shaped bromeliad which was growing terrestrially. Small egg clutches (2– 4 eggs) were also found in these bromeliads, although we do not know whether these belonged to R. defleri or R. ventrimaculata . Adults were found at different heights in the forest. Two of the specimens from Caparú were found at the base of trees, while the third was found amidst low-growing shrubs growing on a stream-bank. The single specimen from Puerto Córdoba was found in a bromeliad at roughly 3 meters from the ground, where it was courting a female. We heard males calling in the morning (9 h) and evening (18 h), although the call is faint and easily missed. Population densities of R. defleri appear to be low in the areas we searched. In Caparú, we were able to find only three individuals in three full days of searching, and only found one during three days around La Pedrera. In Caparú, we met two Colombian biologists that had been conducting a herpetological survey for the past month, consisting of daily surveys, and found only a single R. defleri .

Conservation status. Following the IUCN Red List criteria (IUCN 2001), we suggest this species be listed as Least Concern (LC). Although the area of occupancy for this species is unknown, the Apaporis region has experienced minimal habitat loss due to deforestation. Few people live in this area, and those that do rely primarily on fishing rather than agriculture for subsistence. As such, there is little risk of significant habitat loss in the near future.

Figures

FIGURE 1. Ranitomeya defleri sp. nov. Male paratype (JLB 08 - 004) in life from Puerto Córdoba, Amazonas, Colombia.

FIGURE 2. Paratypes of Ranitomeya defleri with corresponding ventral photos. Left to right, JLB 08 - 001 – JLB 08 - 004.

FIGURE 3. Drawing of the mouthparts of the tadpole of R. defleri, stage 29.

FIGURE 4. Advertisement calls of (A) R. defleri from type locality, recorded 8 August 2008 at 26 ° C. (B) Advertisement call of R. ventrimaculata from Cerro Yupatí, recorded 5 August 2008 at 27 ° C.

FIGURE 5. Map of study area. All localities in Colombia: (1) Puerto Córdoba, Departamento Amazonas, 1 ° 16 ' 51.63 " S, 69 ° 43 ' 10.36 " W, (R. defleri); (2) Angosturas, Departamento Amazonas, 1 ° 17 ' 47.84 " S, 69 ° 37 ' 38.77 " W, (R. ventrimaculata and putative R. defleri tadpoles); (3) Cerro Yupatí, Departamento Amazonas, 1 ° 18 ' 15.59 " S, 69 ° 36 ' 30.28 " W, (R. ventrimaculata); (4) Caparú, Departamento Vaupés, 1 ° 4 ' 37.46 " S, 69 ° 30 ' 51.34 " W (R. defleri). Two other dendrobatids were found in this region (Ameerega trivittata in Puerto Córdoba and Caparú, and A. hahneli in Puerto Córdoba).

FIGURE 6. Forest near Estación Biológica Caparú (6 August 2008).