A new species of poison frog from the Andean mountains of Tolima, Colombia by Victor Luna

Zootaxa 1638: 59–68 (2007) www.mapress.com / zootaxa/

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)

ZOOTAXA

A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia MANUEL HERNANDO BERNAL1,2, VICTOR FABIO LUNA-MORA1,OSCAR GALLEGO1 & ALONSO QUEVEDO3 1

Laboratorio de Herpetología & Eco-Fisiología, Grupo de Investigación en Zoología, Universidad del Tolima, Ibagué, Colombia. E-mail: mhbernal@ut.edu.co; victorfl05@hotmail.com; oscargallego@yahoo.com 2 Laboratorio de anfibios, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia. 3 Fundación Proaves. Bogotá, Colombia. E-mail: aquevedo@proaves.org

Abstract We describe a new species of poison frog of the genus Ranitomeya from the Andean mountains of Tolima, Cordillera Central of Colombia. The new species can be distinguished from all other dendrobatids by its distinctive color pattern in combination with its small size and advertisement call. The maximum adult snout vent length is 17.39–18.91 mm, its dorsal surface is brown, head with a metallic yellow-bronze color, ventral surfaces overall brown dark with or without bluish green spots. This new species is syntopic with Ranitomeya dorisswansonae, but readily distinguishable by color pattern and foot morphology. Key words: Dendrobatidae, Ranitomeya tolimense sp. n., tadpole, vocalization

Introduction Poison frogs (Dendrobatoidea) are widely distributed in the Neotropics, from Nicaragua to Bolivia and from the pacific cost of South America to Martinique in the French Antilles. Grant et al. (2006) referred to 247 species in 16 genera but several more species, not yet described, are known to exist. In Colombia, there are eight genera of Dendrobatoidea. One of these, Ranitomeya (Bauer, 1988), family Dendrobatidae, is equivalent to the Silverstone’s (1975) Dendrobates minutus group with the removal of the species steyermarki and quinquevitattus sensu stricto and with the addition of several species described since 1975. Within Ranitomeya, Grant et al. (2006) recognized a monophyletic radiation equivalent to Minyobates sensu Myers (1987) minus steyermarki, which they call the minutus clade. This clade is found in Central America and Colombian Chocó, and is the sister clade of an exclusively Amazonian group, the ventrimaculatus clade (Grant et al., 2006). However, the authors have not studied in detail the Andean (Colombia, Ecuador) species allocated to Ranitomeya. Consequently, Grant et al., (2006) suggested that further studies are necessary to the placement of this group; T. Grant (pers. comm.) expects these species conform an Andes clade which may be sister to Minyobates steyermarki. These Andean species include R. abdita (Myers & Daly, 1976), the only Ecuadorian taxon, R. bombetes (Myers & Daly, 1980), R. opisthomelas (Silverstone, 1975), R. viridis (Myers & Daly, 1976), R. virolinensis (Ruiz-Carranza & Ramirez-Pinilla, 1992) and two species, which were initially placed in the genus Dendrobates, R. dorisswansonae and R. daleswansoni (Rueda et al., 2006). The purpose of this paper is to describe a new species of Ranitomeya which was found in the Andean mountains of the municipality of Falan, Tolima, eastern flank of the Cordillera Central of Colombia.

Accepted by M. Vences: 3 Sept. 2007; published: 14 Nov. 2007

Material and methods All specimens were fixed and preserved according to the standard protocols suggested by McDiarmid (1994). They have been deposited in the herpetological collection at the Universidad del Tolima, Ibagué, Colombia (CZUT-A: Colección Zoológica, Universidad del Tolima-Anfibios) and the Instituto de Ciencias Naturales (ICN), Universidad Nacional de Colombia, Bogotá, Colombia. Coloration of species was determined from living specimens and color photographs. Morphometric terminology, as well as some diagnostic characteristics (neither osteology nor skin toxins), follow Myers & Daly (1980) and Ruiz-Carranza & Ramirez-Pinilla (1992). Only adult specimens were measured using a Scherr-Tumico caliper to the nearest 0.01 mm. Sex was determined by examination of gonads and ducts with the aid of a stereomicroscopy as well as through presence versus absence of vocal slits. Measurements taken: SVL, snout-vent length; TL, tibia length measured between heel and outer surface of flexed knee; GBW, greatest body width taken just under the axillae; HW, head width between angles of jaws; IOD, interorbital distance; HL, Head length, sagital distance from tip snout to angle of jaw; TSCN, tip of snout to center of naris; NED, distance from center naris to anterior edge of eye; IND, distance between centers of nares; EL, eye length; HDT, horizontal diameter of tympanum; MTD, distance from corner of mouth to lower edge of tympanic ring; HaL, hand length measured from the proximal edge of large medial palmar tubercle to tip of longest third finger; WTFD, width of third finger disc; WTF, width of third finger below disc; WTTD, width of third toe disc; WTT, width of third toe below disc; WFTD, Width of fourth toe disc; WFT, width of fourth toe below disc. Calls were recorded in captivity on metal cassettes with a Sony TCM -459V tape recorder and a SONY FV-5 microphone at the Laboratorio de Herpetología & Eco-Fisiología, Universidad del Tolima, between May and June 2007. Air temperature within the terrarium was about 25 ºC. Call analysis and recording parameters were performed in SYRINX-PC 2.6h, as described in Bernal et al. (2004). Oscillograms and audiospectrograms are shown, and waveforms and dominant frequencies are described. Buzz call definition follows Lötters et al. (2003).

Ranitomeya tolimense sp. nov. (Fig. 1, 2) Holotype: ICN 53372, an adult male, collected by Oscar Gallego, Victor Luna and Manuel H. Bernal on 19 May 2007 near “Finca La Lulera”, vereda el Llano, Departamento del Tolima, Municipio de Falan, Cordillera Central of Colombia, elevation 1852 m above sea level (5º01’08”N, 75º02’31”W) (Fig. 3). Paratypes: ICN 53373, adult female; CZUT-A 988-989, adult females; CZUT-A 990-991, adult males; collected along with the holotype. Etymology: The specific epithet means “from Tolima”, the department of Colombia where the new species was found. Definition and diagnosis: Ranitomeya tolimense is a dendrobatid having an adult SVL of 17.66–18.92 mm. Dorsal surfaces in life brown or dark brown, anteriorly with a moderate metallic yellow-bronze color that ends posterior to the head and gradually after the midbody. Ventral surfaces in life overall brown dark, with or without bluish green spots or speckling on belly, undersides of thighs and groins. The skin is granular on the dorsum, flanks, venter and the dorsal surface of the limbs, and comparatively less granular on the forelimbs. A brown dark stripe extends from the outer border of the eyes, crossing the tympanum, to the forelimbs insertions, which contrasts with the yellow color of the upper jaw. The proximodorsal surface of the upper arm is yellow. Fingers are webless; adpressed first finger shorter than second; third finger disc of adults about 1.5– 2.0 times wider than distal end of adjacent phalanx, discs on fingers notably expanded. Digits of feet lacking webbing or lateral fringe; toe I shorter than toe II, and unexpanded toe discs.

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Ranitomeya tolimense is considered to be related to R. abdita, R. bombetes, R. opisthomelas and R. virolinensis based on shared larval characters, proposed to represent synapomorphies by Myers & Daly (1980). The character state is the median gap that interrupts the papillae fringe on the lower edge of the oral disc. The new species can be distinguished from these four species by the dorsal color: R. abdita is unicolor dark bronzy brown with orange flash marks proximally on the arms and legs adjacent to axilla and groin; R. bombetes is black with dorsolateral stripes yellowish or orange golden; R. opisthomelas and R. virolinensis are largely red turning gray distally on limbs and dark brown after two-third of body, respectively. R. tolimense is syntopic with R. dorisswansonae, but readily distinguished by color pattern and morphology since the latter is dark brown or black with irregular red blotches, and the toes I and II are partially or totally fused (not so in the new species described herein). Measurements of holotype (mm): SVL 17.66; TL 7.98; GBW 8.13; greatest HW 5.97; IOD 2.35; HL 5.04; TSCN 1.55; NED 1.36; IND 2.52; EL 2.32; HDT 1.18; MTD 1.02; HaL 4.65; WTFD 0.80; WTF 0.40; WTTD 0.64; WTT 0.61; WFTD 0.50; WFT 0.45. Description of the type series (3 adult males, 3 adult females): Size small, with maximum SVL of 18.91 (Table 1); females slightly larger than males (Table 2). Head narrower than body; greatest HW 73 % of GBW in males, and 79 % in females. Greatest HW averaging about 30 % of SVL (Table 2). Males with defined vocal slits, but with little or not external indication of the subgular vocal sac. Snout weakly pointed to truncate in dorsal and ventral aspects. Nares situated near tip of snout and visible from front and from below but not from above. Canthus rostralis rounded, loreal region flat, inclined slightly outward to lip. Eye longer than snout length; distance from center of naris to eye 65 % of EL in males and 64 % in females (Table 2). Tympanum vertically oval, smaller than eye. TABLE 1. Measurements (in mm) for the type series of Ranitomeya tolimense, new species. ICN 53373 Adult female

CZUT-A 988 Adult female

CZUT-A 989 Adult female

ICN 53372 Adult male

CZUT-A 990 Adult male

CZUT-A 991 Adult male

SVL

18.91

17.82

18.11

17.66

17.95

18.02

7.94

7.14

7.53

7.98

7.22

7.73

GBW

8.16

6.93

7.08

8.13

7.35

6.52

5.86

5.42

5.64

5.97

5.81

5.35

IOD

2.27

2.25

2.36

2.35

2.16

2.19

5.65

4.97

5.14

5.04

5.08

5.46

TSCN

1.74

1.31

1.57

1.55

1.38

1.89

NED

1.52

1.44

1.35

1.36

1.65

1.38

IND

2.40

2.22

2.34

2.52

2.33

2.19

2.23

2.19

2.24

2.32

2.20

HDT

1.44

1.13

1.27

1.18

1.10

1.33

MTD

0.85

0.64

0.87

1.02

0.91

0.94

HaL

4.57

4.30

4.22

4.65

4.52

4.10

WTFD

0.73

0.64

0.65

0.80

0.75

0.78

WTF

0.48

0.40

0.39

0.40

0.46

0.40

WTTD

0.60

0.58

0.56

0.64

0.60

0.71

WTT

0.55

0.50

0.44

0.61

0.54

WFTD

0.64

0.48

0.46

0.50

0.44

0.38

WFT

0.48

0.42

0.36

0.45

0.40

0.32

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Zootaxa 1638 漏 2007 Magnolia Press 路

FIGURE 1. Ranitomeya tolimense, new species. Lateral view showing color pattern. CZUT-A 989 adult female, SVL 17.94 mm. Photo: Manuel H. Bernal.

Hand (Fig. 4A) moderately large, its length (proximal edge of metacarpal tubercle to tip of longest finger) about 23.5–26.7 % of SVL. Relative length of adpressed fingers III > IV > II > I; adpressed finger I shorter than finger II and its tip just reaching disc of second. Discs slightly expanded on finger I, but notably expanded on fingers II, III and IV; third finger disc in females and males averaging 1.59–1.86 times wider than distal end of adjacent phalanx. A large circular outer metacarpal tubercle on median base of palm, an smaller inner metacarpal tubercle on base of finger I, and one tubercle on base of fingers I and II, and two tubercles on fingers III and IV. Hind limbs relatively long; tibia 40–45 % of SVL. Relative lengths of adpressed toes IV > III >V >II > I; toe I short (Fig. 4B), reaching bottom of subarticular tubercle of toe II, and with unexpanded disc. Other toe discs slightly expanded. One to three nonprotuberant subarticular tubercles, one on toes I, II, two on toes III and V, and three on toe IV. Small outer and moderately-sized inner metatarsal tubercles. Feet lacking webbing or lateral fringes. Coloration: In life (Fig. 1), head yellow-bronze, upper jaw and anteroproximal part of the upper arm bright yellow; venter, throat, chest, sides of the body, hind limbs and hands brown or black brown. A dark stripe extends from the eyes to the arm insertion. Throat and venter with or without small bluish green blotches; flanks, groin and thighs (anterior and ventral) with or without a few bluish spots. Iris dark brown. In 70 % alcohol the dark or dark brown surfaces of the body maintain their color, as well as the bluish green of blotches or spots of ventral surfaces. However, the bronze color of head become dark whereas the yellow color of the upper arm and jaw change to a pale white and later to a dark gray.

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FIGURE 2. Male nurse frog (CZUT-A 990) with a tadpole over his back at the type locality. Photo: Victor Luna.

Sexual dimorphism: The most remarkable external characteristics to differentiate adult males and females are the presence of vocal slits. Also, a wider disc on finger III and a smaller SVL was found in males (Table 2); however, there are a few data to be confident with this sexual difference. Testes and eggs are dark brown. Distribution and natural history: So far, R. tolimense is known only from the type locality on the eastern flank of the Cordillera Central, Municipio de Falan, Departamento de Tolima, Colombia. Specimens were collected at an elevation of about 1852 m above sea level. They were found during day and the onset of night time in May 2007 on the forest floor. On 19 May 2007, at 18:00 h (relative humidity: 75 %, air temperature: 20.4 ºC), we found a male nurse frog carrying a tadpole on his back on the ground near bromeliads and heliconias. When captured the frog expelled a milky secretion over his body (Fig. 2). The type locality of R. tolimense is a small patch of a secondary forest dominated by trees with a maximum height of 4 to 6 m, covered by epiphytic plant, mainly of the families Araceae, Bromeliaceae and Orchidaceae. The canopy is dense allowing for little penetration of light. Humidity in the area is maintained by the constant cloud cover and frequent rainfall. The forest floor is covered by leaf litter, fallen tree branches and

A NEW SPECIES OF POISON FROG

trunks, house to fungi, mosses and lichens. There are also smaller trees, palms and tree ferns. The mean temperature is about 19 ºC and the annual precipitation is between 2500–3000 mm per year (Gallego, 2003). The general area is dominated by farms with coffee plantations, most likely not suitable habitat for R. tolimense. We recommend further studies to assess the distribution of this species and its conservation status. TABLE 2. Size and proportions of adult Ranitomeya tolimense, New species sensu Myers & Daly (1980). Measurements

Mean (+/- S.E.)

Stand dev.

C.V. (%)

Range

SVL

3 males 3 females

17.87 (0.11) 18.28 (0.22)

0.190 0.564

1.06 3.06

17.66–18.02 17.82–18.91

TL/SVL

3 males 3 females

0.42 (0.02) 0.41 (0.01)

0.010 0.005

4.76 2.42

0.45–0.40 0.40–0.41

HL/SVL

3 males 3 females

0.30 (0.00) 0.30 (0.01)

0.011 0.002

3.66 0.66

0.28–0.32 0.30–0.31

NED/EL

3 males 3 females

0.65 (0.04) 0.64 (0.02)

0.0.8 0.04

12.30 6.25

0.58–0.75 0.60–0.68

WTFD/WTF

3 males 3 females

1.86 (0.11) 1.59 (0.04)

0.20 0.07

10.75 4.40

1.63–2.00 1.52–1.66

FIGURE 3. Map of Colombia showing (arrow) the type locality of Ranitomeya tolimense.

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FIGURE 4. Ventral view of hand and foot of Ranitomeya tolimense (CZUT-A 989). Scale = 1mm.

Tadpole: The following description is based on a larva (CZUT-A: 991) obtained from the back of a nurse frog male (Figs. 2, 5). The larva is in stage 25 sensu Gosner (1960). Measurements in millimeters are: head-body length 4.4; total length 13.1; tail length 8.7; greatest depth from upper edge dorsal fin to lower edge ventral fin 1.3. The tadpole has a globular shape when viewed from above, with maximum body width of 61 % of head body length. The head and body are depressed, width much greater than depth; eyes and nostrils are dorsal, directed dorsolaterally; the spiracle is sinistral and low and the anus dextral (Fig. 5A). The tail is 64 % of the total length and its maximum tail height is only 9.9 % of total length. The tip of the tail is rounded (Fig. 5A). The mouth is directed anteroventrally. There are two upper and three lower tooth rows, with the second upper row being broadly broken above the beak (Fig. 5B). The other rows are complete, although the third posterior one row is weakly pronounced, probably due to an ontogenetic difference with respect to other tadpoles found in the locality. The beak is massive, with serrate cutting edges. The oral disc is laterally indented and its posterior edge has a broad median gap (Fig. 5B). This gap is shared with other related species of the genus Ranitomeya as mentioned above and perhaps represents a synapomorphy (Myers & Daly, 1980), although R. bombetes has a somewhat broader median gap and larger and fewer labial papillae than R. abdita, R. opisthomelas (Myers & Daly, 1980), R. virolinensis (Ruiz-Carranza & Ramirez-Pinilla, 1992) and R. tolimense. Furthermore, R. tolimense shares with R. virolinensis one to two rows of labial papillae (Figure 5B), whereas the illustrations of the other species shown apparently just one. Life coloration was brown to dark brown, lighter on ventral side, turning clear towards the tail tip. In 10 % formalin, the body and tail are pale brown, uniformly pigmented, including fins. The tail tip is somewhat transparent and the venter translucent. Vocalization: The advertisement call of R. tolimense (Fig. 6) is a series of short buzzes of 0.84–0.99 seconds (N = 6). The call is pulsed throughout its length with a dominant frequency of about 4.73–5.22 kHz. The

A NEW SPECIES OF POISON FROG

call is heard as a short, soft cricket-like buzz and sounds similar to the syntopic Ranitomeya dorisswansonae, although not as loud as it. The buzz call (sensu the defined of Lötters et al., 2003) as described herein for R. tolimense is similar to buzz calls described to species considered sharing larval characters with the new species, i.e. R. bombetes, R. opisthomelas (Myers & Daly, 1980), R. virolinensis (Amézquita, 1995), and likely R. adbita (Myers & Daly, 1980). We will not rule out but can’t claim here that similarities in advertisement calls are due to close phylogenetic relationships. First, buzz calls have been reported in other dendrobatid frog species (see Lötters et al., 2003), and second, anuran vocalizations are considered highly adaptive traits. Remarks: According to the possible larval synapomorphy suggested by Myers & Daly (1980) and perhaps morphological and vocalization characters, R. tolimense is expected to be a member of an Andean monophyletic dendrobatid clade including R. abdita, R. bombetes, R. opisthomelas and R. virolinensis. Larvae of other Ranitomeya lack a median gap in the papillae fringe on the lower edge of the oral disc (e.g. R. minuta, R. fulgurita, R. altobuyensis) or remain unknown (R. viridis, R. daleswansoni, R. dorisswansonae).

FIGURE 5. Tadpole of Ranitomeya tolimense (CZUT-A 991). (A) Lateral view, stage 25 (Gosner, 1960). Scale equals 5 mm. (B) Mouth parts. Scale equals 1mm.

Acknowledgments We are grateful to Stefan Lötters for his constructive comments on earlier manuscript versions and J.D. Lynch and J.J. Mueses for help us to confirm the sex identification of specimens. MHB thanks to Instituto Colombiano para el Desarrollo de la Ciencia y la Tecnología, COLCIENCIAS, and The Universidad del Tolima for the financial help to his PhD studies. Also thanks to Maritza Beatriz Mendoza, Ramiro Uribe Kafure, Antonio Guio, Pilar Roa and Deicy Pava for their valuable help at the Universidad del Tolima. Collection permit was approved by CORTOLIMA (resolution 983 from 7 September 2006). All work was partially supported by Fondo de Investigaciones de la Universidad del Tolima (project number 310105).

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FIGURE 6. Advertisement call of Ranitomeya tolimense. A. Audiospectrogram of a call with three notes. B. Oscillogram of the three notes showing the pulses.

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McDiarmid, R.W. (1994) Preparing amphibians as scientific specimens. In: Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L-A.C. & Foster, M.S. (eds.). Measuring and monitoring biological diversity: Standard methods for amphibians. Smithsonian Institution Press. Washington, pp. 289–297. Myers, C.W. & Daly J. (1976) A new species of poison frog (Dendrobates) from Andean Ecuador, including an analysis of its skin toxins. Occasional Papers of the Museum of Natural History The University of Kansas Lawrence, Kansas, 59, 1–12. Myers, C.W. & Daly J. (1980) Taxonomy and ecology of Dendrobates bombetes, a new Andean poison frog with new skin toxins. American Museum Novitates, New York, 2694, 1–23. Myers, C.W. (1987) New generic names for some Neotropical poison frogs (Dendrobatidae). Papèis Avulsos de Zoología. Museu de Zoología da Universidade de Sao Paulo 36, 301–306. Rueda-Almonacid, J.V., Rada, M., Sanchez, S., Velásquez-Alvarez, A. & Quevedo, A. (2006) Two new and exceptional poison dart frogs of the genus Dendrobates (Anura: Dendrobatidae) from the Northeastern Flank of the Cordillera Central of Colombia. Zootaxa, 1259, 39–54. Ruiz-Carranza, P & Ramírez-Pinilla M.P. (1992) Una nueva especie de Minyobates (Anura: Dendrobatidae) de Colombia, Lozania, 61, 1–16. Silverstone, P.A. (1975) A revision of the poison-arrow frogs of the genus Dendrobates Wagler. Natural History Museum of Los Angeles County Science Bulletin, 21, 55 pp.

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