Jun 7, 1999 - A new species of leptodactylid frog, genus Eleutherodactylus, is described from cloud forest of the northeastern versant of the Bolivian Andes.
Copeia, 2000(2), pp. 516–520
New Species of Eleutherodactylus (Anura: Leptodactylidae) from Cloud Forest of Bolivia JO¨RN KO¨HLER A new species of leptodactylid frog, genus Eleutherodactylus, is described from cloud forest of the northeastern versant of the Bolivian Andes. Eleutherodactylus ashkapara sp. nov. seems to be most closely related to E. pluvicanorus from which it is distinguished mainly by larger size, advertisement call, and arboreal habit. Because of many phenetic similarities, I propose that E. ashkapara, E. fraudator, and E. pluvicanorus be recognized as a species group distinct from other groups of South American Eleutherodactylus.
HE humid northeastern versants of the Andes of Bolivia, known as the Yungas, have a highly diversified anuran fauna with an extremely high degree of endemism. Approximately 68% of the species known from this area are Bolivian endemics (Ko¨hler et al., 1998a), and several of these have been described in recent years. At several sites in montane forests within the Yungas, frogs of the genus Eleutherodactylus surely are the most abundant vertebrates. Knowledge of this genus in Bolivia has increased remarkably in recent years. Six species of Eleutherodactylus were listed for the country by De la Riva (1990), and subsequently four more species were added (De la Riva, 1993, 1994). This was followed by descriptions of several new taxa (e.g., De la Riva and Lynch, 1997; Ko¨hler and Lo¨tters, 1999; Ko¨hler et al., 1998b). We are now aware of at least 18 species of Eleutherodactylus in Bolivia, but many more probably will be discovered. During fieldwork in January 1999 in the Chapare region of Bolivia, a new species of Eleutherodactylus seemingly related to E. fraudator and E. pluvicanorus was discovered. The purpose of this paper is to describe the species and to discuss its relationships.
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Notes on color in life were taken in the field, as were color slides of specimens and habitat. Measurements of specimens are in millimeters (mm) and were taken to the nearest 0.1 with dial calipers. Geographic position was obtained using a Magellan 3000 XL GPS receiver. Calls were recorded using a Sony WM-D6C tape recorder, a Sennheiser Me-80 directional microphone, and a TDK MA60 cassette. Recordings were sampled with a rate of 22.05 kHz and 16bit resolution and analyzed with the sound analysis software Cool Edit 96 (Syntrillium Software Corporation) on IBM compatible computers.
Frequency information was obtained through fast Fourier transformation (FFT, width 1024 points). Terminology and description of morphological characters follow Lynch and Duellman (1997). Morphometric abbreviations used throughout the text are as follows: E–N, eye to nostril distance; HW, greatest head width; IOD, interorbital distance; SVL, snout–vent length. Institutional abbreviations are as listed in Leviton et al. (1985) with the following additions: CBF, Coleccio´n Boliviana de Fauna (La Paz), and NKA (formerly MNK-AM), Museo de Historia Natural ‘‘Noel Kempff Mercado,’’ amphibian collection (Santa Cruz de la Sierra). Eleutherodactylus ashkapara sp. nov. Figures 1–2 Holotype.—CBF 3344; adult male, from approximately 47 km on the ‘‘old’’ road from Paractito via El Palmar to Cochabamba (17⬚07⬘58⬙S, 65⬚36⬘54⬙W), Provincia Chapare, Departamento Cochabamba, Bolivia, 2100 m above sea level; collected on 30 January 1999 by Jo¨rn Ko¨hler. Paratopotype.—ZFMK 70318; adult male, collected with the holotype. Diagnosis.—A robust, medium-sized species, distinguished from other species of Eleutherodactylus by the following combination of characters: (1) skin on dorsum shagreened, well-developed dorsolateral folds, skin of venter smooth; (2) tympanic membrane distinct, oval; tympanic annulus visible beneath skin, its diameter about half of the eye length; (3) snout rounded in dorsal view and lateral profile; canthus rostralis sharp; (4) upper eyelid bearing tubercles, narrower than IOD; (5) vomerine odontophores oval, prominent, well separated, median behind choanae; (6) males with vocal slits and large vo-
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ly by larger size, smaller upper eyelid width/ IOD ratio (maximum value in E. ashkapara 70.0%, minimum value in E. pluvicanorus 96.8%), and advertisement call (see below). Eleutherodactylus fraudator is smaller (males 23.2– 32.7 mm SVL), has a smaller vocal sac, usually exhibits a dorsal color pattern with longitudinal stripes, and a continuous dark stripe on the upper lip (irregular dark blotches in E. ashkapara).
Fig. 1. Holotype of Eleutherodactylus ashkapara sp. nov. (CBF 3344) in life; top, dorsolateral view; bottom, ventral view.
cal sac; males with nonspinous nuptial pads; (7) first finger slightly longer than second; tips of outer two fingers truncate, with large pads, tips of inner two fingers rounded, only slightly expanded; (8) fingers with weakly defined lateral fringes; (9) no ulnar tubercles; (10) no tubercles or folds on heel and tarsus; (11) inner metatarsal tubercle oval and elevated, outer smaller, rounded, less conspicuous; supernumerary plantar tubercles absent; (12) toes with weak lateral fringes; webbing absent; fifth toe equal in length with third, not reaching distal subarticular tubercle of fourth toe (condition B, Lynch and Duellman, 1997); toe tips truncate, expanded, slightly smaller than those of outer fingers; (13) dorsum brown with darker markings; dark brown canthal and supratympanic stripe, upper lip with irregular brown blotches; venter cream with brown spots and blotches; (14) adults medium-sized, SVL of two males 44.1 and 49.8 mm, females unknown. Eleutherodactylus ashkapara is most similar to E. pluvicanorus from which it is distinguished main-
Description of holotype.—Head narrower than body, broader than long; snout rounded in dorsal view and in lateral profile; nostrils slightly protuberant, directed laterally; canthus rostralis sharp, slightly concave; loreal region concave; lips not flared; prominent tubercles on upper eyelid, forming rows; indistinct interorbital fold; cranial crests absent; supratympanic fold low, not obscuring upper edge of tympanic annulus; tympanic annulus thin; skin of tympanic membrane barely differentiated; tympanum ovoid, separated from eye by a distance of slightly more than its length; skin on head shagreened; choanae round, small, less in size than tip of first finger, not concealed by palatal shelf of maxillary arch; vomerine odontophores oval, prominent, separated medially, behind choanae, each bearing five vomerine teeth; tongue longer than wide, cordiform, posterior half not attached to floor of mouth; vocal slits moderately long, posterolateral to tongue; vocal sac large, subgular. Skin on dorsum shagreened; dorsolateral folds prominent; two distinct sigmoid folds on dorsum; skin on flanks shagreened; anal sheath absent; tubercles in cloacal region slightly enlarged; skin on throat and venter smooth; discoidal fold absent. Upper surfaces of arms shagreened; ulnar region bearing small tubercle; thenar tubercle oval, elevated; palmar tubercle round, flat; supernumerary palmar tubercles absent; subarticular tubercles round, nonconical; fingers bearing indistinct lateral fringes; first finger longer than second; discs on fingers III and IV expanded, truncate, with enlarged pads; tips of fingers I and II very slightly expanded, round; relative length of fingers II ⬍ I ⬍ IV ⬍ III; nuptial pads present, nonspinous; webbing absent. Upper surfaces of hindlimbs shagreened; heel lacking tubercle; tarsus lacking tubercles and folds; inner metatarsal tubercle oval, elevated, four times the size of round outer metatarsal tubercle; supernumerary plantar tubercles absent; subarticular tubercles nonconical, round; toes bearing weakly defined lateral fringes; webbing absent; discs on toes expanded, truncate, nearly as large as those of outer fingers; toe V equal to length of toe III,
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Fig. 2. Paratype of Eleutherodactylus ashkapara sp. nov. (ZFMK 70318) in life; frontal view; note the throat pattern.
reaching penultimate subarticular tubercle on toe IV (condition B, Lynch and Duellman, 1997); relative length of toes I ⬍ II ⬍ III ⫽ V ⬍ IV; heels overlapping when hindlimbs flexed perpendicular to axis of body. Coloration.—In preservative, dorsum brown; interorbital bar narrow, curved, dark brown, bordered anteriorly by irregular beige fleck; two symmetric, well-defined, dark blotches on scapular region, lateral to the dorsolateral folds; two symmetric, dark flecks in inguinal region, lateral to dorsolateral folds; indistinct, irregular beige flecks on dorsum; upper lip with irregular dark blotches; three dark brown blotches on each of lower eyelid; dark brown canthal stripe, reaching upper lip, interrupted in narial region; dark brown supratympanic bar, covering upper third of tympanic membrane; tympanic membrane dark brown; groin reddish brown; upper surfaces of thighs and shanks with irregular, indistinct, beige flecks, indistinctly barred; posterior side of thighs brown with white spotting and mottling; plantar surfaces dark brown; toe tips dark brown; well-defined, dark brown fleck on anterior side of each forearm, bordered with white; ventral surfaces of forearm beige with brown mottling; dark brown, elongated flecks on outer edge of forearms; palmar surfaces brown, subarticular tubercles white; finger tips brown; throat dark gray with scattered beige mottling; chest medially beige, dark gray on outer edges; venter whitish with dark brown spotting and mottling; ventral surfaces of hindlimbs yellowish with dark brown blotches and flecks laterally. There is little difference in color pattern between the preserved and living specimen, except that the brown color of all body parts is slightly darker in preservative. The red-
Fig. 3. Audiospectrogram and oscillograms of the advertisement call of Eleutherodactylus ashkapara sp. nov. Recording obtained on 30 January 1999. Air temperature was 15.9 C at time of recording.
dish color in the groin was more intense in life. In life, upper third of iris golden, lower twothirds copper brown, with black spotting, darker medially. Measurements and proportions.—Data of holotype and paratype (in parentheses): SVL, 49.8 (44.1); HW, 19.8 (18.1); head length, 18.5 (17.0); upper eyelid width, 3.8 (3.5); IOD, 6.0 (5.0); tympanum length, 2.1 (1.8); eye length, 5.4 (4.9); E–N, 5.0 (4.5); tibia length, 28.6 (26.7); foot length, 38.2 (36.1). Tibia length/SVL, 57.4% (60.5%); HW/SVL, 39.8% (41.0%); upper eyelid width/IOD, 63.3% (70.0%); tympanum length/eye length, 38.9% (36.7%); E–N/eye length, 92.6% (91.8%). Variation.—Besides the smaller size of the paratype there are only slight differences concerning coloration. The paratype exhibits a paler brown on all dorsal surfaces and two irregular dark brown flecks on each flank. The dark blotches on its venter are larger in comparison to the holotype, and the throat is dark gray with two parallel, longitudinal stripes (Fig. 2). Advertisement call.—The call (Fig. 3) consists of a short, single note and sounds like a sonorous ‘‘clack,’’ reminiscent of two hard wooden sticks beaten together. The notes have a duration of 24–43 msec (mean ⫽ 36.0 ⫾ 5.9) and are repeated at a rate of 0.93–1.23 notes/sec (mean ⫽ 1.12 ⫾ 0.11). Principal calls may be followed by a series (5–7) of fast repeated notes of identical character with a repetition rate of approximately 3.5 notes/sec. Call energy is distributed between 1150 and 1830 Hz, with a dominant
¨ HLER—NEW BOLIVIAN ELEUTHERODACTYLUS KO frequency peak at 1470 Hz. Notes lack pulses and harmonics. Air temperature was 15.9 C during time of recording; 43 calls of two individuals were analyzed. In contrast to the short clack of E. ashkapara, the advertisement call of E. pluvicanorus is a moderately long, soft whistle with a mean duration of 339.5 msec (De la Riva and Lynch, 1997; unpubl. data). Both species were calling concomitantly when the new species was discovered, E. ashkapara from the canopy and E. pluvicanorus from the ground. Natural history.—The type locality is in evergreen tropical montane rain forest, part of the Yungas de Cochabamba. Precipitation in that region is the highest in Bolivia and can be expected to be 3500 mm to more than 5000 mm annually (Ibisch, 1996). The region is characterized by extremely steep slopes. The forest of the slopes is rich in epiphytes, tree ferns, and mosses. Eleutherodactylus ashkapara is an arboreal species, in contrast to the terrestrial E. fraudator and E. pluvicanorus. Calls were heard from the canopy at approximately 5–10 m height. The holotype called from a branch approximately 2.5 m high and was completely covered by moss while calling. Calling activity in December and January was most intensive at night but also occurred in the late evening when there was rain or heavy fog. Calls were usually emitted within choruses of several individuals. Other species of Eleutherodactylus found in sympatry with E. ashkapara include E. fraudator, E. llojsintuta, E. platydactylus, E. pluvicanorus, and E. rhabdolaemus. Distribution.—Eleutherodactylus ashkapara is known only from the type locality, but calls of this species were heard at all localities between 1800 m and 2150 m a.s.l. along the old road from Paractito to Cochabamba. Etymology.—The specific name is a noun in apposition and derived from the Quechuan ashka, meaning a lot, and para, meaning rain. It refers to the type locality which can be expected to be among the regions in Bolivia with the highest amount of precipitation. DISCUSSION As is obvious from the description, E. ashkapara is phenetically similar to the species E. fraudator and E. pluvicanorus. I consider all three species to be closely related. When Lynch and McDiarmid (1987) described E. fraudator, they tentatively assigned the species to the E. conspicillatus group. Subsequently, De la Riva and
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Lynch (1997) provided additional data on E. fraudator and described the closely related E. pluvicanorus. Both species were then tentatively assigned to the subgenus Craugastor which mainly is distributed in Middle America (Lynch, 1986). This tentative assignment was based on the presence of the ‘‘E’’ condition of the trigeminal nerve (mandibular ramus medial to the most superficial adductor muscle; Lynch, 1986). Dissection of the paratype of E. ashkapara also revealed the ‘‘E’’ condition of the trigeminal nerve. In addition, E. ashkapara seems to exhibit a frontoparietal fontanelle which seemingly is apparent in a radiograph taken of the type specimens. This character also is present in E. fraudator and E. pluvicanorus, as well as in another Bolivian species, E. mercedesae (Lynch and McDiarmid, 1987; De la Riva and Lynch, 1997). Because of the consistent morphological characters present in E. ashkapara, E. fraudator, and E. pluvicanorus, I consider them to be a lineage distinct from other groups of South American Eleutherodactylus (and probably also distinct from the Middle American subgenus Craugastor). I propose to regard the three species mentioned above as the Eleutherodactylus fraudator species group, defined by the following combination of characters: moderate to medium-sized frogs (SVL in males 23–50 mm) with narrow heads and short snouts; sexually dimorphic in size; cranial crests absent; body robust; limbs moderately long; skin of venter smooth; dorsolateral folds present; vomerine odontophores oval; males with vocal slits and large vocal sac; ‘‘E’’ condition of the trigeminal nerve (sensu Lynch, 1986); tympanic membrane present; canthus rostralis sharp; discs on fingers and toes broad; finger I slightly longer than finger II; toe V slightly shorter or equal the length of toe III, not reaching distal subarticular tubercle of toe IV (condition B sensu Lynch and Duellman, 1997); no webbing on toes; no tubercles or folds on heel or tarsus. A fourth undescribed species of the group, most similar to E. fraudator, has been discovered in the Yungas de La Paz region (M. Harvey, unpubl.). Eleutherodactylus mercedesae Lynch and McDiarmid, 1987, shares some characters with the E. fraudator group but is quite different in its general appearance. Further investigations are needed to throw light on the relationships of this rare Bolivian species. ACKNOWLEDGMENTS I am indebted to J. Aparicio of the Coleccio´n Boliviana de Fauna, La Paz, for his cooperation. Fundacio´n Amigos de la Naturaleza, Santa Cruz
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de la Sierra, provided working space and facilities. K. Busse kindly helped with the radiograph. C. Nowicki, T. Beilenhoff-Nowicki, B. Kunitz, and I. and O. Mersch accompanied and kindly helped me on the trip to the Chapare region. Fieldwork in Bolivia was funded by grants of the German Academic Exchange Service (DAAD) and the ‘‘Graduiertenfo¨rderung des Landes Nordrhein-Westfalen.’’ LITERATURE CITED DE LA RIVA, I. 1990. Lista preliminar comentada de los anfibios de Bolivia con datos sobre su distribucio´n. Boll. Mus. Reg. Sci. Nat. Torino 8:261–319. . 1993. Sinopsis del ge´nero Eleutherodactylus (Amphibia, Anura, Leptodactylidae) en Bolivia y adicio´n de tres especies nuevas para el paı´s. Rev. Esp. Herpetol. 7:97–105. . 1994. Geographic distribution: Eleutherodactylus peruvianus. Herpetol. Rev. 25:159. , AND J. D. LYNCH. 1997. New species of Eleutherodactylus from Boliva (Amphibia: Leptodactylidae). Copeia 1997:151–157. IBISCH, P. L. 1996. Neotropische Epiphytendiversita¨t—das Beispiel Bolivien. Arch. naturwiss. Diss., Galunder Verlag 1:1–356. KO¨HLER, J., AND S. LO¨TTERS. 1999. New species of the Eleutherodactylus unistrigatus group (Amphibia: Anura: Leptodactylidae) from montane rain forest of Bolivia. Copeia 1999:422–427. , S. LO¨TTERS, AND S. REICHLE. 1998a. Amphibian species diversity in Bolivia, p. 329–335. In: Biodiversity—a challenge for development research and policy. W. Barthlott and M. Winiger (eds.). Springer Verlag, Berlin, Germany. , V. MORALES, S. LO¨TTERS, S. REICHLE, AND J. APARICIO. 1998b. A new green species of frog, genus Eleutherodactylus, from Bolivia and Peru´ (Amphibia, Anura, Leptodactylidae). Stud. Neotrop. Faun. Environ. 33:93–99. LEVITON, A. E., R. H. GIBBS JR., E. HEAL, AND C. E. DAWSON. 1985. Standards in herpetology and ich-
thyology: Part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia 1985:802–821. LYNCH, J. D. 1986. The definition of the Middle American clade of Eleutherodactylus based on jaw musculature (Amphibia: Leptodactylidae). Herpetologica 42:248–258. , AND W. E. DUELLMAN. 1997. Frogs of the genus Eleutherodactylus in western Ecuador. Spec. Publ. Nat. Hist. Mus. Univ. Kans. 23:1–236. , AND R. W. MCDIARMID. 1987. Two new species of Eleutherodactylus (Amphibia: Anura: Leptodactylidae) from Bolivia. Proc. Biol. Soc. Wash. 100: 337–346.
ZOOLOGISCHES FORSCHUNGSINSTITUT UND MUSEUM ALEXANDER KOENIG, DEPARTMENT OF HERPETOLOGY, ADENAUERALLEE 160, 53113 BONN, GERMANY. E-mail: uzs13b@uni-bonn. de. Submitted: 7 June 1999. Accepted: 30 July 1999. Section editor: A. H. Price. APPENDIX ADDITIONAL SPECIMENS EXAMINED JKSL refers to Jo¨rn Ko¨hler and Stefan Lo¨tters field numbers of not yet cataloged specimens. Total number of specimens examined given in parentheses. Eleutherodactylus fraudator (16): Bolivia: Cochabamba: Carrasco: Sehuencas, ZFMK 60244–54; La Siberia, JKSL 593–95; Santa Cruz: Caballero: Empalme, JKSL 569–70. Eleutherodactylus pluvicanorus (22): Bolivia: Cochabamba: Chapare: Incachaca, ZFMK 66938; km 49 on old road Paracti to Cochabamba, JKSL 647, 755; Carrasco: Sehuencas, ZFMK 60186–91, 60203 (paratypes); Rı´o Chua Kocha, NKA 1100 (holotype), NKA 1101–04 (paratypes); Santa Cruz: Florida: La Yunga, ZFMK 66872–75; Caballero: Empalme, JKSL 571–73.
