Herpetologica, 62(2), 2006, 173–183 Ó 2006 by The Herpetologists’ League, Inc.
A NEW SPECIES OF TELMATOBIUS (ANURA: LEPTODACTYLIDAE) FROM NORTHERN CHILE J. RAMO´N FORMAS1, CE´SAR C. CUEVAS,
AND JOSE´
J. NUN˜EZ
Instituto de Zoologı´a, Universidad Austral de Chile, Casilla 567, Valdivia, Chile ABSTRACT: We describe a new species, Telmatobius chusmisensis, from Chusmisa, Iquique Province, northern Chile. The new taxon is diagnosed by characteristics of the adult morphology, osteology, larval external morphology, and chromosomes. The new species is compared with its Chilean congeners and differs from them in presenting all the carpal elements cartilaginous. The tadpole of T. chusmisensis lack intramarginal mental papillae sharing this character with other Chilean species of the genus. Key words: Amphibia; Anura; Chromosomes; Leptodactylidae; Northern Chile; Osteology; Tadpoles; Telmatobius chusmisensis sp. nov.
ANURANS of the leptodactylid genus Telmatobius are typical inhabitants of high aquatic environments (above 2000 m) in the Andes. The genus comprises about 50 species (Formas et al., 2003) scattered from the equator (T. niger) to 298 S on the eastern slopes of the Andes (T. contrerasi). In Chile, nine species (T. peruvianus, T. marmoratus, T. zapahuirensis, T. pefauri, T. fronteriensis, T. halli, T. philippii, T. dankoi, and T. vilamensis) have been described, and they are distributed from 188 119 S (T. peruvianus; Veloso et al., 1982) to 228 519 S (T. vilamensis; Formas et al., 2003). Most Chilean species (T. fronteriensis, T. vilamensis, T. halli, T. philippii, T. dankoi, T. pefauri, and T. zapahuirensis) are confined to small bodies of water within desert habitats suggesting high levels of endemism (Benavides et al., 2002). Herein, we describe a new species restricted to a small stream near the village of Chusmisa (198 419 S, 698 139 W), Iquique Province, in the region of Tarapaca´ in northern Chile. Diagnosis of the new species is based on external morphology and osteology of adults, external morphology of tadpoles, karyotype, chromosomal C-banded patterns and Ag-NOR (nucleolar organizer region) position. We provide morphological and karyological comparisons among Chilean species and include notes on the ecology of the new species. MATERIALS AND METHODS This description is based on nine adult frogs and 19 tadpoles collected at Chusmisa, 92 km 1
CORRESPONDENCE: e-mail,
[email protected] 173
NE Huara, Chile (Fig. 1). Specimens were collected by hand and with nets from below the stones and vegetation in flowing water. Notes on the habit and color in life were taken at the time of capture. Vouchers and additional specimens used in this study (see Appendix) are deposited in the following collections: Instituto de Zoologı´a, Universidad Austral de Chile (IZUA); Coleccio´n Boliviana de Fauna (CBF); Museo de Zoologı´a, Universidad de Concepcio´n (MZUC); Museo Nacional de Historia Natural, Chile (MNHN); Departamento de Biologı´a Celular y Gene´tica, Universidad de Chile (DBCUCH); Departamento Biome´dico, Universidad de Antofagasta (DBMUA); and American Museum of Natural History (AMNH). The following variables were measured with digital calipers (to the nearest 0.1 mm): snout– vent length (SVL), head length (posterior corner of jaw to tip of the snout), head width (from posterior corner of jaw), thigh length (from vent to knee), tibia length (knee to heel), foot length (proximal edge inner metatarsal tubercle to tip of third toe), eye diameter (between anterior and posterior corners of eye), interorbital distance, nostril–snout distance and internarial distance. Sexual maturity was assessed by presence of eggs in females and the degree of development of nuptial excrescences in males. Formulae for toes webbing are those of Savage and Heyer (1967), as modified by Myers and Duellman (1982). Osteological observations were made on five adult specimens (see Appendix); cleared-and-stained skeletons were prepared using the method of Song and Parenti (1995).
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between a glass slide and cover slip and dipped in liquid nitrogen. Thereafter, the cover slip was removed with a razor blade and the slides were allowed to air dry. After 3 days, chromosomes were stained for 15 min, in So¨rensen’s buffer (pH 6.8) containing 4% Giemsa solution (Formas, 1991). Chromosomes were stained to reveal C-band patterns and Ag-NOR position, following the methodologies of Sumner (1972) and Rufas et al. (1982). Centromeric positions were determined according to Levan et al. (1964).
FIG. 1.—Distribution of the species of Telmatobius in Chile. The inset shows the type locality of Telmatobius chusmisensis.
Tadpoles (IZUA 3385) were staged according to Gosner (1960). The following measurements were taken according to Altig and McDiarmid (1999): total length (distance from the tip of the snout to the tip of the tail), body length (distance from the tip of the snout to the junction of the posterior body wall with the axis of the tail myotomes), tail length (distance from the body terminus to the absolute tail tip), maximum tail height (by measuring the greatest height of the fin above or below the tail musculature at a specified distance from the body terminus or tail tip), tail-muscle height (measured vertically from the junction of the body wall with the ventral margin of the tail muscle), tail-muscle width (measured transversely at the same place as tail-muscle height), interorbital distance (between centers of the pupils), and internarial distance (between centers of the nares). Chromosomal characteristics were recorded from one male (IZUA 3395) and one female (IZUA 3396), which were each injected with 0.1% colchicine. After 2 hours, specimens were anaesthetized with diethyl ether. A ventral incision was made under sterile conditions and the intestines were removed. Metaphase plates were obtained by macerating intestinal epithelium fragments. These were hypotonically treated with distilled water, fixed in acetic acid-methanol (1:3), and placed in 45% acetic acid. Small fragments of tissue were placed
SPECIES DESCRIPTION Telmatobius chusmisensis sp. nov. Holotype.—Instituto de Zoologı´a Universidad Austral de Chile (IZUA 3397), adult male from Chusmisa (198 419 S, 698 139 W), 92 km NE Huara, Iquique Province, I Regio´n of Tarapaca´, Chile; approximately 3650 m elevation (Fig. 1). Collected on 11 March 2002 by Jose´ Nun˜ez, Ce´sar Cuevas, and J. Ramo´n Formas. Paratypes.—IZUA 3400 (adult male), IZUA 3394 (adult female) and IZUA 3385 (a series of 5 tadpoles); five cleared-and-stained skeletons of adults specimens (IZUA 3395–96, 3398–99, 3402). All specimens collected with the holotype. Diagnosis.—Telmatobius chusmisensis can be distinguished from other members of the genus by a combination of features including: (1) SVL 50.0–63.2 mm; (2) snout short, depressed in lateral view; (3) hind limbs 159.6–179.9% of SVL; (4) in life, irregular apricot spots on dorsum and ventral surfaces of thighs; (5) dorsal surface, flanks, and limbs covered with small, spiculate granules; (6) chest and ventral surfaces of forelimbs and belly with minute, dark brown spines; (7) 8 or 9 supernumerary palmar and plantar tubercles; (8) postfemoral fold absent; (9) toes webbed; (10) tarsal fold thin; (11) outer border of Toe V fringed; (12) tongue subrectangular, almost totally attached (81.2%) to the floor of mouth, posterior border unnotched and free; (13) choanae large, subcircular; (14) all the carpal and distal tarsal elements cartilaginous; (15) pubis cartilaginous, poorly developed; (16) anterolateral process of hyoid plate with distal expansion; (17) prootic ossification limited to anteromedial part of otic capsule.
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Telmatobius chusmisensis differs from all other Chilean Telmatobius by having all the carpal and tarsal elements cartilaginous (in T. philippii the prehallux and prepollex are cartilaginous; Cuevas and Formas, 2002), and the dorsum and ventral surfaces of thighs with irregular apricot spots. Telmatobius chusmisensis is geographically and morphologically distinct from other Chilean species of Telmatobius. Its type locality, Chusmisa, is isolated from both the northern (T. peruvianus, T. marmoratus, T. zapahuirensis, T. pefauri) and southern (T. fronteriensis, T. philippii, T. halli, T. vilamensis) groups of Telmatobius (Fig. 1). Chusmisa is located approximately 292 km north of Puquios (type locality of T. fronteriensis) and 238 km south of Murmuntani (type locality of T. pefauri; Fig. 1). Among the Chilean species of Telmatobius, T. dankoi and T. vilamensis have well developed postfemoral folds; T. chusmisensis lacks postfemoral folds. Telmatobius chusmisensis (SVL 50.0–63.2 mm) is larger than T. fronteriensis (SVL 39.5–40.0 mm) and T. vilamensis (SVL 33.0–57.1 mm). In addition, T. fronteriensis occurs at 4150 m in elevation, whereas T. chusmisensis has been collected at 3650 m. Telmatobius halli (SVL 48.0–55.0 mm), like T. chusmisensis, is a moderate-sized species; however, their snouts differ in shape in dorsal aspect with the snout of T. halli being truncate and that of T. chusmisensis being rounded. The xiphisternum is unnotched in T. peruvianus (Veloso et al., 1982), whereas it is notched in T. chusmisensis. Telmatobius marmoratus has a gray dorsum with irregular black spots and the tibiotarsal joint of the adpressed limb does not reach the posterior border of the eye; in T. chusmisensis the dorsum has irregular apricot spots, and the joint reaches the anterior border of the eye. The belly color of T. chusmisensis (white or light yellow) distinguishes it from T. pefauri (white or pink; Veloso et al., 1982) and T. philippii (gilt copper). Telmatobius chusmisensis has irregular apricot spots on dorsum and ventral surfaces of thighs; this color pattern is absent in T. zapahuirensis. In addition T. chusmisensis is larger (SVL 50.0– 63.2 mm) than T. zapahuirensis (SVL 39.4– 51.2 mm; Veloso et al., 1982). Description of holotype.—Adult male (SVL 55.7 mm). Head slightly narrower than body;
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FIG. 2.—Morphological details of the male holotype (IZUA 3397) of Telmatobius chusmisensis. Lateral (A), dorsal (B) and ventral (D) views of head; plantar (C) and palmar (E) surfaces; nuptial excrescences (F). Bars indicate 5 mm.
head length 31.8% of SVL; head broader than long (head width/SVL 5 0.34; head length/ head width 5 0.92). Snout rounded in dorsal view (Fig. 2B); margin of upper jaw flared; snout short, depressed in lateral profile (Fig. 2A); loreal region flat, granular, with scarce, minute, dark brown spines; nostrils slightly prominent, oriented anterodorsolaterally; internarial distance 19.6% of head width; internarial region slightly convex; nostrils closer to the anterior border of the eye than to terminus of snout; in dorsal view, canthus rostralis distinct. Eye 31.5% of head length, oriented anterodorsolaterally; tympanum absent; supratympanic fold moderately developed, extending from posterior corner of eyelid, terminating dorsal to forelimb; lips thick; maxillary and premaxillary teeth present and embedded within labial mucosa, so that only tips are noticeable; three vomerine teeth (2 on the left and 1 on right), horizontally located between the choanae (paratype IZUA 3400); choanae large (52% of internarial distance; IZUA 3399) and subcircular; tongue subrectangular; longer
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TABLE 1.—Measurements (mm) of adult males and females of T. chusmisensis. Means, standard deviations, and ranges (parentheses). Holotype
Paratypes
Character
IZUA 3397 male
IZUA 3400 male
IZUA 3394 female
Males n52
Females n54
Snout–vent length Head length Head width Thigh length Tibia length Foot length Eye diameter Interorbital distance Nostril-snout distance Internarial distance
55.7 17.7 17.4 27.6 26.2 41.6 6.3 6.7 4.5 4.9
51.8 19.7 18.8 25.2 26.3 41.7 4.8 6.8 4.1 4.8
54.8 19.4 18.4 25.9 24.1 37.9 6.2 6.2 4.5 4.9
51.3 (50.0–52.6) 17.9 (17.3–18.5) 17.2 (16.8–17.5) 24.7 (24.3–25.0) 24.9 (24.7–25.0) 39.1 (38.5–39.7) 5.7 (5.3–6.0) 7.3 (7.1–7.5) 4.1 (4.0–4.2) 5.3 (5.1–5.5)
58.6 6 3.4 (55.6–63.2) 21.9 6 2.3 (19.0–24.0) 19.5 6 1.4 (19.0–24.0) 28.0 6 0.6 (27.2–28.4) 27.2 6 0.9 (26.2–28.5) 43.6 6 2.2 (40.5–45.1) 5.8 6 0.2 (5.5–6.0) 7.1 6 1.0 (5.9–7.5) 5.1 6 0.4 (4.7–5.5) 4.4 6 0.6 (3.7–5.0)
(11.3 mm) than wide (8.2 mm), attached approximately 81.2% of its length anteriorly (IZUA 3399); posterior border unnotched; vocal slits absent. Forelimbs moderately robust, with dermal antebrachial fold; dorsal and ventral surfaces granular, with scarce, minute, dark brown spines. Relative lengths of fingers: III . IV . II 5 I; lateral fringes present along inner margins of Fingers II and III; tips of fingers spherical, approximately equal in size; inner palmar tubercle large, depressed, and fusiform; outer palmar tubercle large, rounded, and protruding; subarticular tubercles large, simple, rounded, protruding; two subarticular tubercles on Fingers III and IV, one on Fingers I and II; supernumerary tubercles absent (Fig. 2E); 8 or 9 supernumerary palmar tubercles; nuptial spines on dorsal, ventral and lateral surface of thumb, moderately small, conical, keratinized black in color (Fig. 2F). Hind limbs long (approximately 171.2% of SVL) and slender; toes long, thin; relative lengths of toes: IV . III . V . II . I; webbing formula: I 13 4 – 23 4 II 11 2 –3 III 21 4 –31 2 IV 31 3 –2 V; webbing diminishing distally from wide fringes along lateral margins of toes (Fig. 2C); outer border of Toe V fringed, extending approximately to the distal subarticular tubercle; tarsal fold thin, extending 67% of length of tarsus, confluent distally with the fringe along inner margin of Toe I; tips of toes rounded; inner metatarsal tubercle flat, narrow, subrectangular; external tubercle conical, small, one-fourth of length of inner metatarsal tubercle; subarticular tubercles rounded, smaller than the tips of toes, distributed on toes as follows: I (1), II (1), III (2), IV (3), V (2); supernumerary subarticular tubercles distally distributed on toes as
follows: II (3), III (6), IV (10), V (5–6); ventral surface of tarsus with minute, spiculate tubercles (approximately 30); postfemoral fold absent. Skin of head smooth; dorsal surface, flanks and limbs covered with small, spiculate granules; ventral surfaces of hind limbs smooth; chest, ventral surfaces of forelimbs and belly with minute, dark brown spines (Fig. 2D); jaws with a few spines; ‘‘bagginess’’ absent; cloacal opening directed posteriorly at dorsal level of thighs; cloacal opening round, unornamented, covered by a fold of skin. Variability (measurements in mm) of the holotype, paratypes, and six adult specimens are shown in Table 1. Color in preservative.—Dorsal surfaces of head, body, upper arms and legs dark gray; head and dorsal surface of the body profusely covered with minute, black spots; a few small, white spots irregularly distributed on dorsum and legs; throat and chest cream, belly and ventral surfaces of upper arms and legs light brown; ventral surfaces of thighs with irregular, yellowish spots. Color in life.—Dorsal ground color light brown or greenish brown, profusely spotted with minute, black spots; skin of belly white or light yellow; ventral surfaces of thighs light brown; irregular spots on dorsum and ventral surfaces of thighs apricot. Osteology.—Prootic ossification limited to anteromedial part of otic capsule and mediumsized ossifications associated with the anterior margins of the otic eminences; occipital condyles ossified. Dorsum of braincase with an elongated frontoparietal fontanelle; the fontanelle is about half of braincase length and
=
=
=
=
=
=
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about a third to a quarter of medial skull length (Fig. 3A). Rostral cartilages nearly entirely exposed, with a pair of small, approximately rectangular nasals medially separated, and not in contact with the sphenethmoid and pars facialis of maxilla; premaxilla and maxilla not in contact but united by cartilage, as are the premaxillas; alary process of premaxilla rectangular, dorsolateral corners acuminate, sloping posteriorly; pars palatina moderately well developed; vomers consist of remnants of the anterior ramus and short pre and postchoanal rami in form; neopalatines present as long, slender, nearly straight bone, reaching the sphenethmoid medially and not in contact with the maxilla. Frontoparietals well developed, acuminate anteriorly and overlying dorsolateral braincase from anterior part of orbit posteriorly to angle of epiotic eminence; frontoparietals broadly separated anteriorly, narrowly separated posteriorly; frontoparietals fused posteromedially, investing medial margins of prootics and having a distinct articulation with the exoccipitals. Parasphenoid cruciform, cultriform process not reaching the level of neopalatines; alae long, broad and associated with prootic anteriorly and with exoccipitals posteriorly; posteromedial process truncate; cultriform process underlying most of orbital region of braincase and forming ventral margin of prootic foramen (Fig. 3B). Occipital condyles with wide medial separation. Maxillary arcade composed of robust premaxillae; pars dentales equally well developed on premaxillae and maxillae; maxillae slender with low pars facialis and lacking preorbital processes; quadratojugals short, not articulating with maxillae; 6–7 (n 5 5) premaxillary teeth; 19–21 (n 5 5) teeth in each maxilla. Pterygoids robust, with flanges; anterior ramus nearly in contact with neopalatines; posterior ramus investing medial surface of massive palatoquadrate cartilage; medial ramus short, terminating on anteroventral margin of otic capsule and not in contact with prootic or parasphenoids. Squamosal Tshaped in lateral view (Fig. 3C), with slender and acuminate zygomatic ramus as long as two times the otic ramus; otic ramus broad; ventral ramus distinctly curved (posteriorly concave), investing lateral surface of palatoquadrate cartilage and posterior surface of quadratojugal (Fig. 3C). Jaw articulation lying posterior to
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FIG. 3.—Skull of Telmatobius chusmisensis, (IZUA 3402); in dorsal (A), ventral (B), and lateral (C) views. Pectoral girdle (D) and hyoid plate (E) of T. chusmisensis. Bar indicates 5 mm.
level of fenestra ovalis. Stapes present (IZUA 3395), reduced (IZUA 3399, 3402) or absent (IZUA 3398); tympanic annulus reduced. Hyoid corpus broad, about 65% broader than length at midline; hyoglossal sinus broad, U-shaped, as deep as wide. Anterior processes of hyalia developed; anterolateral processes of hyoid long slender, straight, tips expanded, directed anterolaterally; posterolateral processes slender, straight, approximately as long as the anterolateral processes directed posterolaterally, with acuminate tip; posteromedial processes ossified, stout, broadly separated from one another anteriorly, terminating in cartilage posteriorly (Fig. 3E). Pectoral girdle arciferal and robust (Fig. 3D). Clavicles stocky, arcuate and robust. Coracoids short, stocky; sternal and glenoid ends expanded, about equal in width; width of glenoid head about 50% greater than midshaft width of coracoid. Pectoral fenestra shallow, 1.6 times as broad as long, anterior and medial margins cartilaginous, posterior margin formed by coracoid. Epicoracoid cartilages well developed, anterior termini posterior to medial end of clavicles and broadly separating these bones. Omosternum well developed, with cartilaginous manubrium, end expanded. Sternum
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FIG. 4.—Vertebral column of Telmatobius chusmisensis (IZUA 3402) in dorsal (A) and ventral (B) views. Dorsal views of the hand (C) and foot (D) of Telmatobius chusmisensis (IZUA 3395). Bar indicates 5 mm.
short and broad, poorly mineralized, with cartilaginous margins. Scapula short, robust, only slightly longer than the coracoid, distinctly bicapitate; partes acromialis and glenoidalis about equal in size. Suprascapula expanded; anterior border ossified as cleithrum; posterior and lateral margins cartilaginous. Vertebral column composed of eight procoelus, non-imbricated, independent presacral vertebrae (Fig. 4A,B); centrum width approximately equal to centrum length. Presacral I (atlas) wide, shallow cervical cotyles widely separated, presacrals I–V bearing low neural spines; relative lengths of transverse processes and sacrum: III , sacrum , II 5 IV , VI– VIII; distal ends of transverse processes of presacrals III and IV slightly expanded; transverse processes of presacral II slightly expanded, oriented anterolaterally; transverse processes of presacrals V and VI not expanded, oriented posteriorly; transverse processes of presacrals VII and VIII not expanded, oriented perpendicular to longitudinal axis. Sacral diapophysis round, not dilated, oriented posterolaterally; sacrum with bicondylar articulation with urostyle. Urostyle robust, bearing a dorsal crest that is best developed anteriorly, flanked by lateral flanges of bone that diminish in size posteriorly; two foramina located anterolaterally. Overall length of pelvic girdle approximately equal to length of sacrum plus presacral vertebral column. Ilial shaft robust, bearing
FIG. 5.—Tadpole of Telmatobius chusmisensis (Stage 30). Lateral (A), dorsal (B) and ventral (D) views; oral disc (C). Bar indicates 5 mm.
dorsolateral crest; interilial profile a narrow U-shape, width of U at base about half the distance between anterior ends of ilia; ilium forming anterior margin of round acetabulum; preacetabulum forming approximately a 908 angle to ilial shaft; ilia articulating with one another medially, forming posterior margin of acetabulum; ventral margin of acetabulum formed by cartilaginous pubis. Humerus longer, more robust than radioulna; crista medialis present, well developed; phalangeal formula of manus: 2-2-3-3; terminal phalanges pointed; carpal elements and prepollex cartilaginous (Fig. 4C); femur and tibia similar in length; tibiale and fibulare ossified, distal tarsal elements cartilaginous (Fig. 4D); phalangeal formula of foot: 2-2-3-4-3. Description of tadpoles.—Larvae (Stages 28–39) large (total length 38.0–99.0 mm; body length 15.0–37.0 mm), and robust; tail relatively short (1.3–1.7 times body length) and slightly thick; head and body fusiform in lateral view (Fig. 5A); lateral profile of snout gently rounded; nostrils rounded, not protuberant, situated dorsally, with a thin cutaneous fringe (Fig. 5B); interocular distance 156–266% of internarial distance; distance between the anterior border of the nostril and terminus of
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TABLE 2.—Measurements (mm) of the tadpoles of Telmatobius chusmisensis. Means, standard deviations, and ranges (in parenthesis). Character
Stage 28 n52
Stage 30 n52
Stage 31 n53
Stage 36 n52
Stage 39 n 5 10
Total length Body length Tail length Maximum tail height Tail muscle height Tail muscle width Interorbital distance Internarial distance
39.8 (38.0–41.5) 16.0 (15.0–17.0) 23.7 (23.0–24.5) 9.1 (9.2–9.3) 4.8 (4.7–5.0) 3.7 (3.5–4.0) 4.6 (4.5–4.8) 2.9 (2.8–3.0)
55.0 (54.0–56.0) 23.0 (22.0–24.0) 32.0 (32.0–32.0) 11.4 (11.3–11.5) 7.9 (7.7–8.2) 5.7 (5.7–5.7) 5.6 (5.5–5.6) 3.4 (3.3–3.5)
62.7 6 2.5 (60.0–65.0) 23.7 6 1.2 (23.0–25.0) 39.0 6 1.7 (37.0–40.0) 13.3 6 1.4 (12.2–14.8) 8.5 6 0.5 (8.0–8.8) 6.6 6 0.6 (6.0–7.2) 6.2 6 0.6 (5.8–7.0) 3.8 6 0.2 (3.7–4.0)
77.0 (74.0–80.0) 31.0 (30.0–32.0) 46.0 (44.0–48.0) 15.1 (15.0–15.2) 9.6 (9.2–10.0) 8.9 (8.7–9.2) 7.5 (7.2–7.8) 4.2 (4.2–4.3)
89.1 6 5.8 (81.0–99.0) 34.2 6 1.7 (32.0–37.0) 54.9 6 4.1 (49.0–62.0) 17.1 6 1.4 (15.7–17.8) 10.7 6 0.8 (10.0–12.5) 10.3 6 0.8 (9.0–11.7) 8.0 6 0.4. (7.5–8.7) 3.7 6 0.5 (3.0–4.2)
snout two times the distance between the anterior border of eye and posterior border of nostril; eyes anterolaterally situated, diameter equal to internarial distance; width of oral disc 103–119% of interocular distance; oral disc anteroventral, not emarginate; broad rostral gap; mental gap absent (Fig. 5C); transparent, conical marginal papillae in single row on anterior labium, in double row on posterior labium; intramarginal lateral papillae in supraangular and infrangular regions; intramarginal mental papillae absent; upper jaw sheath wider than tall, well keratinized; jaw sheath with incipient serrations and dark-brown pigmentation; labial tooth formula [(1) (1-1)/(1-1) (2)]. Spiracular tube sinistral, two times internarial distance; aperture oval, diameter 38–57% of eye diameter; proctodeal tube conical, opaque (in 10% formalin), wide; vent opening dextral, not visible in ventral position; distal end ovoid (Fig. 5D). Dorsal fin not extending onto body; ventral fin starting at the end of proctodeal tube; tail tip rounded; maximum width of dorsal and ventral fins slightly posterior midlength of tail; fin depth slightly exceeding body depth; dorsal surface of body with numerous black minute spots; ventral surface transparent, internal organs visible; posterior third of tail with black spots and blotches; minute black spots near the body; hind limbs with minute melanophores. Measurements of the tadpoles are given in Table 2. Chromosomes.—The examination of 19 metaphases from one male and one female of T. chusmisensis revealed a diploid number of 2N 5 26. All chromosomes are bi-armed and the fundamental number (NF) is 52 (Fig. 6A). Pairs 1, 8, 9, 10, 11 and 12 are metacentric, Pairs 2, 4, 6, and 7 are submetacentric, and Pairs 3 and 5 are subtelocentric (Table 3). Pair
6 shows a remarkable secondary constriction in the small arm. Sexual dimorphism was not detected. Heterochromatic C-bands (Fig. 6B) were revealed in centromeric areas of all chromosomes in the karyotype, being those located on Pairs 1, 5, and 9 stained more conspicuous. Telomeric C-bands were not revealed, except in subtelocentric Pair 5, which has a remarkable telomeric C-band on long arm. Interstitial C-bands and sexual dimorphism were not revealed in the Cbanded karyopype of T. chusmisensis. The AgNORs were revealed in the smaller arms of Pair 6 (Fig. 6C). Distribution and ecology.—This species is known only from the type locality. Chusmisa is located in the tropical marginal region which
FIG. 6.—Chromosomes of Telmatobius chusmisensis. Standard (A) and C-banded karyotype (B); Ag-NOR (C).
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TABLE 3.—Relative length, arm ratio (mean and standard deviation), and type of chromosomes of Telmatobius chusmisensis sp. nov. * Chromosomes with secondary constriction. Pair
RL1
r2
Type3
1 2 3 4 5 6* 7 8 9 10 11 12 13
168.69 6 13.32 137.01 6 1.82 126.42 6 5.49 113.44 6 5.75 100.79 6 11.19 57.68 6 1.41 51.57 6 1.63 48.50 6 1.87 46.91 6 1.85 42.05 6 2.27 39.03 6 4.91 34.25 6 4.16 32.48 6 3.40
1.31 6 0.25 1.82 6 0.36 3.99 6 0.53 2.09 6 1.27 3.09 6 1.17 1.90 6 0.36 1.72 6 0.11 1.52 6 0.23 1.63 6 0.26 1.63 6 0.24 1.11 6 0.19 1.27 6 0.25 1.73 6 0.87
M Sm St Sm St Sm Sm M M M M M Sm
1 2 3
Relative length according to Bogart (1970). r 5 long arm/short arm. m 5 metacentric, sm 5 submetacentric, st 5 subtelocentric.
has an annual mean temperature 12.5 C, and in the austral summer the rainfall ranges between 50–100 mm (Di Castri, 1968). The type locality is a semi-desertic area with scarce vegetation (Browningia candelaris, Verbena gynobaris, Adesmia spinusissima and Balbisia stitchkinii; Gajardo, 1994). Adults (males and females) were collected by hand below stones on the bottom of a slow moving stream (1 m wide, 12 C) covered with aquatic plants during the austral summer (11 March 2002). Tadpoles (Stages 28–39) were collected with a net below aquatic plants on the banks of the stream. Male specimens have nuptial asperities and a female (IZUA 3394) has about 515 immature oocites (1.1–1.3 mm in diameter); the animal pole is dark brown and the vegetative pole is creamywhite. One tadpole is near metamorphosis (Stage 42, SVL 5 33.2 mm). One unidentified tadpole was collected with the larvae of T. chusmisensis. Etymology.—The name chusmisensis is a Latin adjective and refers to the type locality, Chusmisa. DISCUSSION Cei (1986), Trueb (1979) and Wiens (1993) showed that the species of Telmatobius are characterized by a remarkable amount of inter- and intraspecific morphological variation precluding an appropiate generic definition. Trueb (1979) indicated that the fanglike teeth embedded in the labial mucosa may be
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a characteristic of Telmatobius. Wiens (1993) suggested that the following presumptive synapomorphies may support the genus: (1) frontoparietals fused posteriorly and (2) nuptial excrescences on Finger I only. The new species (T. chusmisensis) is considered to be a member of Telmatobius because it has each of the three aforementioned characters; in addition, its distribution argues for the species’ inclusion in Telmatobius. Telmatobius chusmisensis is the tenth species of the genus described from Chile; its nine Chilean congeners are: T. halli, T. peruvianus, T. marmoratus, T. pefauri, T. zapahuirensis, T. dankoi, T. fronteriensis, T. vilamensis, and T. philippii. Although the taxonomic status of these taxa are reasonably well established, two taxonomic problems remain. These involve the identities of T. halli edentatus described by Capurro (1955) from El Tatio (228 259 S, 678 599 W; Antofagasta Province) and T. marmoratus pustulosus from Cancosa (198 519 S, 688 369 W; Tarapaca´ Province; Capurro, 1954). J. Carlos Ortiz (personal communication) indicated that the systematic status of some Chilean populations of T. marmoratus should be reviewed. The Chilean species of Telmatobius extend from 188 119 S (T. peruvianus) to 228 519 S (T. vilamensis) and their altitudinal distribution ranges from 2200 m (T. dankoi; Formas et al., 1999) to 4270 m (T. marmoratus;Veloso et al., 1982). Most of these species are restricted to their type localities; however, T. peruvianus and T. marmoratus have been reported in different localities of the northern Chilean Andes (Veloso et al., 1982). The geographic isolation of the Chilean Telmatobius species, except T. peruvianus y T. marmoratus, which are restricted to small streams or permanent springs in subdesertic conditions characterized by stressful environments, and the low allozyme diversity (T. vilamensis Ho 5 0.0058, and T. fronteriensis Ho 5 0.00; Benavides et al., 2002) suggest that could be associated to the species diversity and high degree of differentiation. Although the phylogenetic relationships of the Chilean species of Telmatobius have not been resolved, the pattern of speciation of this group of species is likely to be related to the uplift of the Andes and the progressive desiccation of this part of the Chilean territory (Benavides et al., 2002). Formas et al. (2003)
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demonstrated that the Chilean Telmatobius species can be arranged into geographical species groups: the northern (T. peruvianus, T. marmoratus, T. pefauri and T. zapahuirensis) and southern groups (T. halli, T. fronteriensis, T. dankoi, and T. vilamensis), which are separated by a large geographical gap (approximately 572 km) with a semiarid environment. The presence of a new species (T. chusmisensis) between these species groups shows that this geographical discontinuity is not genuine and it reflects the inadequate herpetological knowledge of this part of the Chilean Andes. The same reasoning may explain the apparent absence of Telmatobius species southward of 228; in Argentina Telmatobius reach 298 S (T. contrerasi; Cei, 1977). On a comparative basis, the standard karyotype of Telmatobius species (2N 5 26; NF 5 52) is uniform (Cuevas and Formas, 2002), but the C-band karyotypes reveal some specific differences (Formas et al., 2003). The C-banded karyotype of T. chusmisensis is remarkable in having only one chromosomic pair (N8 5) with telocentric bands in the long arms; all the other species (T. arequipensis, T. dankoi, T. philippii, and T. vilamensis) have numerous telocentric bands in both long and short arms (Cordova et al., 1987; Formas et al., 1999; Cuevas and Formas, 2002; Formas et al., 2003). Despite the fact that the C-band karyotypes are useful in identifying Telmatobius, their utility in phylogenetic studies is limited. The tadpole of T. chusmisensis is generalized (Orton, 1953), having characters associated with anuran larvae inhabiting lotic and benthic habitats (depressed body, anteroventral oral disc, robust caudal musculature, dorsolateral eyes, and low fins). The tadpoles of T. chusmisensis, like those of T. dankoi, T. philippii, and T. vilamensis (Formas et al., 1999; Cuevas and Formas, 2002; Formas et al., 2003) lack intramarginal mental papillae in contrast to the Argentinean species group (meridional group; e.g., T. atacamensis, T. ceiorum, T. laticeps) in which these oral structures are present (Lavilla, 1985). Among frogs of the genus Telmatobius, cartilaginous distal tarsal elements, particularly the prehallux, have been reported in T. cirrhacelis, T. vellardi and T. niger (Trueb, 1979) from Ecuador, T. platy-
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cephalus, T. hypselocephalus and T. pinguiculus (Lavilla and Laurent, 1988a,b) from northern Argentina, T. huayra (Lavilla and Ergueta, 1995), T. yuracare (De la Riva, 1994), T. ifornoi (Lavilla and Ergueta, 1999), T. simonsi, T. sibiricus (De la Riva and Harvey, 2003) from Bolivia, T. breviceps, T. ignavus, T. thompsoni, T. degener, T. latirostris, T. necopinus and T. truebae (Wiens, 1993) from northern Peru, and T. philippii from northern Chile (Cuevas and Formas, 2002); however, the situation is different in T. chusmisensis because all the distal tarsal elements are cartilaginous. Cartilaginous carpal elements, particularly the prepollex, have been described in T. cirrhacelis, T. vellardi and T. niger (Trueb, 1979), T. pinguiculus, T. platycephalus (Lavilla and Laurent, 1988a,b), T. huayra (Lavilla and Ergueta, 1999), T. yuracare (De la Riva, 1994), T. breviceps, T. ignavus, T. thompsoni, T. degener, T. latirostris, T. necopinus and T. truebae (Wiens, 1993), and T. philippii (Cuevas and Fornas, 2002). Telmatobius chusmisensis differs from the species above cited in possesing all the carpal elements cartilaginous; this character has been also reported in Insuetophrynus acarpicus, a leptodactylid frog endemic of the temperate Nothofagus forests of southern Chile (Barrio, 1970). Lynch (1978), Lavilla (1985) and Wiens (1993) assumed that Telmatobius and Alsodes are sister taxa. Molecular data (12S and 16S mitochondrial DNA sequences) presented by Darst and Cannatella (2004) support this hypothesis. Lynch (1978) considered Insuetophrynus and Atelognathus to be sister taxa. The existence of carpal elements totally cartilaginous in T. chusmisensis and I. acarpicus is assumed herein to be an homoplastic character to both taxa. RESUMEN Describimos una nueva especie, Telmatobius chusmisensis de la localidad de Chusmisa, 3650 m de altura, 92 km al NE del poblado de Huara, Provincia de Iquique, norte de Chile. El nuevo taxo´n se caracteriza por poseer manchas irregulares de color anaranjado, tanto en el dorso como la superficie ventral de los muslos, y todos los elementos carpales y tarsales cartilaginosos. La nueva especie es comparada con otros taxa chilenos congene´ricos.
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Acknowledgments.—Our special thanks to Dr. L. Trueb who made useful suggestions that greatly improved the manuscript. The comments of Dr. U. Sinsch and the anonymous reviewers are also appreciated. Drawings were made by M. Navarro. The final version of the manuscript was reviewed by Lila Brieva. This study was supported by Proyect Fondecyt (Fondo Nacional de Ciencia y Tecnologı´a) N8 1000426 to J. R. Formas.
LITERATURE CITED ALTIG, R., AND R. MCDIARMID. 1999. Body plan: development and morphology. Pp. 24–51. In R. McDiarmid and R. Altig (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago, Illinois, U.S.A. BARRIO, A. 1970. Insuetophrynus acarpicus un nuevo leptodactı´lido firmisternio sudamericano (Amphibia, Anura). Physis 30:331–341. BENAVIDES, E., J. C. ORTIZ, AND J. W. SITES, JR. 2002. Species boundaries among the Telmatobius (Anura: Leptodactylidae) of the Lake Titicaca Basin: allozyme and morphological evidence. Herpetologica 58:31–55. BOGART, J. P. 1970. Systematic problems in the amphibian family Leptodactylidae (Anura) as indicated by karyotypic analisis. Cytogenetics 9:369–383. CAPURRO, L. F. 1954. El ge´nero Telmatobius en Chile. Revista Chilena de Historia Natural 54:31–40. ———. 1955. Telmatobius halli edentatus, nueva subespecie para la fauna anfibia de Chile. Investigaciones Zoolo´gicas Chilenas 2:150–152. CEI, J. M. 1977. A new species of Telmatobius from the northern mountains of San Juan, Argentina (Anura: Leptodactylidae). Journal of Herpetology 11:359–361. ———. 1986. Speciation and radiation in the Andean Telmatobius frogs. Pp. 374–386. In F. Vuilleumier and M. Monasterio (Eds.), High Altitude Tropical Biology. Oxford University Press, Oxford, U.K. CO´RDOVA, J., H. J. DESCAILLEAUX, AND W. MANYA. 1987. Descripcio´n del cariotipo de Telmatobius arequipensis (Anura:Leptodactylidae) y relaciones citogene´ticas con otras especies del ge´nero. Revista Latinoamericana de Gene´tica 1:44–53. CUEVAS, C. C., AND J. R. FORMAS. 2002. Telmatobius philippii, una nueva especie de rana acua´tica de Ollagu¨e, norte de Chile (Leptodactylidae). Revista Chilena de Historia Natural 75:245–258. DARST, R. C., AND D. CANNATELLA. 2004. Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 31:462–475. DE LA RIVA, I. 1994. A new aquatic frog of the genus Telmatobius (Anura: Leptodactylidae) from Bolivian cloud forests. Herpetologica 50:38–45. DE LA RIVA, I., AND M. B. HARVEY. 2003. A new species of Telmatobius from Bolivia and a redescription of T. simonsi Parker, 1940 (Amphibia: Anura: Leptodactylidae). Herpetologica 59:127–142. DI CASTRI, F. 1968. Esquisse e´cologique du Chili. Pp. 7– 52. In C. L. Delamare Debouttteville and E. Rapoport (Eds.), Biologie de l’Ame´rique Australe Editions du Centre National de la Recherche Scientifique, Paris, France. FORMAS, J. R. 1991. The karyotypes of the Chilean frogs Eupsophus emiliopugini and E. vertebralis (Amphibia:
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Anura: Leptodactylidae). Proceedings of the Biological Society of Washington 104:7–11. FORMAS, J. R., E. BENAVIDES, AND C. CUEVAS. 2003. A new species of Telmatobius (Anura: Leptodactylidae) from Rı´o Vilama, northern Chile, and the redescription of T. halli Noble. Herpetologica 59:253–270. FORMAS, J. R., I. NORTHLAND, J. CAPETILLO, J. J. NUN˜EZ, C. C. CUEVAS, AND L. M. BRIEVA. 1999. Telmatobius dankoi, una nueva especie de rana acua´tica del norte de Chile. Revista Chilena de Historia Natural 72:427–445. GAJARDO, R. 1994. La Vegetacio´n Natural de Chile. Clasificacio´n y Distribucio´n Geogra´fica. Editorial Universitaria, Santiago, Chile. GOSNER, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190. LAVILLA, E. O. 1985. Diagnosis gene´rica de las especies de Telmatobius (Anura: Leptodactylidae) en base a caracteres larvales. Physis 43:63–67. LAVILLA, E. O., AND P. ERGUETA. 1995. Una nueva especie de Telmatobius (Anura: Leptodactylidae) del sudoeste de Bolivia. Ecologı´a en Bolivia 24:91–101. ———. 1999. A new Bolivian species of the genus Telmatobius (Anura: Leptodactylidae) with a humeral spine. Amphibia-Reptilia 20:55–64. LAVILLA, E. O., AND R. F. LAURENT. 1988a. Deux nouvelles espe`ces du genre Telmatobius (Anura: Leptodactylidae) en provenance de El Moreno (Province de Jujuy, Argentine). Alytes 7(3):77–89. ———. 1988b. A new species of Telmatobius (Anura: Leptodactylidae) from Catamarca (Argentina). Alytes 7(3):90–96. LEVAN, A., K. FREDGA, AND A. SANDBERG. 1964. Nomenclature for centromeric positions on chromosomes. Hereditas 52:201–22. LYNCH, J. 1978. A re-assessment of the Telmatobiine leptodactylid frogs of Patagonia. Occasional Papers of the Museum of Natural History, The University of Kansas 72:1–57. MYERS, C., AND W. E. DUELLMAN. 1982. A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama´. American Museum of Natural History 2752:1–32. ORTON, G. L. 1953. The systematics of vertebrate larvae. Systematic Zoology 2:63–75. RUFAS, J. S., P. ITURRA, W. DE SOUZA, AND P. SPONDA. 1982. Simple silver staining procedures for the location of nucleolus and nucleolar organizer under light and electron microscopy. Archives of Biology 93:267–274. SAVAGE, J. M., AND W. R. HEYER. 1967. Variation and distribution in the tree frog genus Phyllomedusa in Costa Rica, Central America. Beitra¨ge fu¨r Neotropischen Fauna 2:111–131. SONG, J., AND L. R. PARENTI. 1995. Clearing and staining whole fish specimens for simultaneous demonstration of bone, cartilage and nerves. Copeia 1995:114–118. SUMNER, A. T. 1972. A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research 75:304–306. TRUEB, L. 1979. Leptodactylid frogs of the genus Telmatobius in Ecuador with the description of a new species. Copeia 1979:714–733. VELOSO, A., M. SALLABERRY, J. NAVARRO, P. ITURRA, J. VALENCIA, M. PENNA, AND N. DI´AZ. 1982. Contribucio´n
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sistema´tica al conocimiento de la herpetofauna del extremo norte de Chile. Pp.135–268. In A. Veloso and E. Bustos (Eds.), La Vegetacio´n y los Vertebrados Ectote´rmicos del Transecto Arica-Lago Chungara´. Volumen de Sı´ntesis. Proyecto MAB-6, UNESCO. Santiago de Chile. WIENS, J. J. 1993. Systematics of the leptodactylid frog genus Telmatobius in the Andes of northern Peru´. Occasional Papers of the Museum of Natural History, University of Kansas 162:1–76. Accepted: 24 October 2005 Associate Editor: Maureen Kearney
APPENDIX Specimens Examined Telmatobius dankoi.—CHILE: Provincia El Loa: Las Cascadas, 2260 m, MNHN 3006, IZUA 2108–10, 2112 (two cleared-and-stained adults), 2113 (9 specimens), 2106 (2 tadpoles), 2107 (5 tadpoles), DBMUA 45, 46, 53, 57. Telmatobius halli.—CHILE: Provincia El Loa: Ollagu¨e, 3050 m, AMNH A-44753–54, A-44758. Telmatobius marmoratus.—CHILE: Provincia Parinacota: Lago Chungara´, 4270 m, MZUC 24520, 24524, 24526. BOLIVIA: Provincia Murillo: Valle de La Paz, CBF 03244–56, CBF 1009-11, CBF 468–70.
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Telmatobius pefauri.—CHILE: Provincia Parinacota: Quebrada de Zapahuira, 3270 m, DBCUCH 629, 632–634, 641, 652. Telmatobius peruvianus.—CHILE: Provincia Parinacota: Putre, 3200 m, MZUC 24642–43. Telmatobius vilamensis.—CHILE: Provincia El Loa: Rı´o Vilama, 3110 m, IZUA 3080-81, IZUA 3224 (clearedand stained adult), IZUA (cleared-and-stained adult), 3146 (two cleared-and-stained adults), IZUA 3225–3226, IZUA 3132 (five tadpoles); CBF 3760–62; MZUC 24104–06, MZUC 25725–38. Telmatobius zapahuirensis.—CHILE: Provincia Parinacota: Quebrada de Zapahuira, 3270 m, DBCUCH 630, 639. Telmatobius philippii.—CHILE: Provincia El Loa: Quebrada de Amincha, 3700 m, IZUA 3093, 3087; Provincia El Loa: Quebrada del Inca, 3700 m, IZUA 3088–92, 3193–95 (three cleared-and-stained specimens, chromosomes), 3094 (seven tadpoles), 3196–97 (chromosomes). Telmatobius fronteriensis.—CHILE: Provincia El Loa: Puquios, 4150 m, MZUC 25094, 25095–103, 25261–78, 25095, and 25103 (cleared-and-stained adults). Telmatobius chusmisensis.—CHILE: Provincia Iquique: Chusmisa, 3650 m, IZUA 3386–87, 3393–94, 3397, 3400–01, 3403–05; 3385 (five tadpoles), IZUA 3395–96, 3398–99, 3402 (five cleared and stained skeletons of adults specimens).
