Oreobates cruralis, (BOULENGER, 1902), 2008

Padial, José M., Chaparro, Juan C. & Riva, Ignacio De La, 2008, Systematics of Oreobates and the Eleutherodactylus discoidalis species group (Amphibia, Anura), based on two mitochondrial DNA genes and external morphology, Zoological Journal of the Linnean Society 152 (4), pp. 737-773 : 749-753

OREOBATES CRURALIS ( BOULENGER, 1902)

COMB. NOV.

Hylodes cruralis Boulenger (1902)

Eleutherodactylus cruralis – Stejneger (1904) ( Figs 3B–C, 6A–B )

Hylodes cruralis Boulenger, 1902: 396 . Holotype: BM 1947.2 .15.70 (formerly 1901.8.2.44). Type locality: ‘ La Paz, Bolivia, 4000 m’ ( Fig. 4 ).

Lynch (1989) redescribed this species after examining the holotype. He also studied numerous specimens from Bolivia and Peru deposited in several collections. He confronted two problems. One, the type locality of H. cruralis was La Paz, Bolivia, 4000 m a.s.l. (type collected by P. O. Simmons). Lynch considered this locality to be in error, which was subsequently supported by De la Riva (1990), De la Riva (1993), and De la Riva et al. (2000). The second problem was the great variability in the size of adults. Most of these specimens were in very poor preservation condition, and therefore many subtle morphological characters were difficult or impossible to observe or identify with confidence. Moreover, the specimens studied by Lynch came from very different altitudes and habitats. For example, the largest sample available to him was the series AMNH 6060–73, and the locality of procedence ‘Juliaca’ was also in error, as it lies in the dry altiplano of southern Peru.

De la Riva et al. (2000) previously stated that what was considered E. cruralis could be in reality a composite of more than one species. Some species described recently were similar in external appearance to E. cruralis ( O. ibischi and O. madidi ), and differences in advertisement calls were pivotal for assessing their distinctness (Reichle, Lötters, & De la Riva, 2001; Padial et al., 2005b; Padial et al., 2008). We studied 181 specimens of E. cruralis from Bolivia and Peru, collected by us as well as those deposited in various collections, including the holotype and almost all specimens studied by Lynch (1989). After recognizing O. granulosus (see below), O. ibischi , O. madidi , O. sanderi , and O. lehri , O. cruralis can be defined with confidence. The redescription of E. cruralis by Lynch (1989) is not only based on the holotype, but on a series of specimens. Furthermore, in our point of view, the series examined by him contain three different species ( O. cruralis , O. granulosus , and O. sanderi ). Hence, in order to avoid confusion we provide a thorough diagnosis of O. cruralis and a redescription based exclusively on the holotype. The study of the intraspecific variation is based on additional specimens listed in the Appendix.

Diagnosis: A small Oreobates (SVL of adults, 20.3– 33.6 mm) characterized as follows: (1) skin on dorsum coarsely shagreened without keratinized granules, texture composed of small, round, low, flat warts, regular in size, only some of them slightly enlarged; warts on flanks slightly larger than those of dorsum; a pair of incomplete dorsolateral folds composed by enlarged warts; venter smooth; posterior surfaces of limbs smooth; discoidal fold present; postrictal glands present; (2) tympanic membrane and annulus distinct, about half the eye length; supratympanic fold weak and short; (3) head large, slightly longer than wide; snout round in dorsal and lateral views; canthus rostralis sinuous in dorsal view, round in profile; (4) cranial crests absent; upper eyelid covered by small granules; (5) dentigerous process of vomers large, situated posteromedial to choanae; (6) males with vocal slits and no nuptial pads; (7) hands with long and slender fingers, first finger longer than second; subarticular tubercles large, prominent, conical; supernumerary tubercles large, prominent, round to conical, smaller than subarticular tubercles; tips of fingers III and IV truncate, slightly enlarged, lacking circumferential grooves and ungual flaps; lateral fringes and keels on fingers from moderate to absent; (8) ulnar tubercles absent; (9) no tubercles on heel and tarsus; (10) inner metatarsal tubercle ovate to round, prominent; outer metatarsal tubercle smaller, round, prominent; supernumerary tubercles conical, prominent; (11) toes long and slender (foot length 50% of SVL), lateral fringes weak or absent, webbing absent; fifth and third toes reaching midpoint of second subarticular tubercle of toe IV; tips of toes moderately enlarged, rounded, ungual flap not indented; (12) axillary gland present; (13) dorsal coloration pale brown to dark brown or greyish-brown, with W-shaped occipital and mid-dorsal X-shaped dark marks, or a pair of cream dorsolateral stripes and a short longitudinal sacral stripe; throat and chest light grey to dark brown; belly cream with brown mottling or reticulations on anterior margin.

Oreobates cruralis can be distinguished from other Oreobates (characters of other species in parentheses) as follows: from O. choristolemma by lacking keratinized granules on dorsum, smaller size (SVL of the single known adult female, 46.4 mm) ( Table 3), and lacking indented ungual flap on finger discs; from O. discoidalis by having warty dorsal skin (finely shagreened with few enlarged warts in some specimens); moderately enlarged and truncate tips on fingers III and IV (enlarged and ovate); dentigerous process of vomers posteromedial to choanae (between choanae); canthus rostralis sinuous in dorsal view and round in lateral profile (straight and sharp); differences in advertisement call and habitat ( Padial et al., 2008). From O. granulosus by having slightly enlarged and truncate tips on fingers III and IV (rounded, not enlarged); dorsal skin coarsely shagreened, composed of round low warts, without keratinized granules on dorsum (dorsal skin with low, round, nonpungent keratinized granules and warts); smaller SVL of adult females, 24.9–33.6 mm (SVL, 34.4–39.5 mm), and head longer than wide (equal) ( Table 3); by having numerous, conical, and prominent supernumerary tubercles on feet (supernumerary tubercles low, few, round). From O. heterodactylus by having coarsely shagreened dorsal skin with enlarged warts (smooth); slightly enlarged and truncate tips of fingers III and IV (very enlarged and ovate); numerous, conical, and prominent supernumerary tubercles on feet (supernumerary tubercles low, few, round); advertisement call, and habitat ( Padial et al., 2008). From O. ibischi by having tympanum length half or less than half of eye length (more than half of eye length); coarsely shagreened dorsal skin with enlarged warts (smooth to finely shagreened with some enlarged warts); slightly enlarged and truncate tips on fingers III and IV (enlarged and ovate, finger tips two times wider than the digit); numerous, conical, and prominent supernumerary tubercles on feet (supernumerary tubercles low, scarce, round); head longer than wide (wider than long); differences in advertisement call and habitat ( Padial et al., 2008). From O. lehri by having slightly enlarged and truncate tips on fingers III and IV (finger tips not expanded); first finger longer than second (finger I equal to finger II); smaller size of adult males and females (SVL, 31.0– 39.9 mm) ( Table 3); shorter feet, FL/SVL = 50% (60%); numerous conical and prominent supernumerary tubercles on feet (supernumerary tubercles low, few, round). From O. madidi by having dorsal skin with small, round, uniform warts, with sparse enlarged warts (homogeneously warty, larger warts), slightly enlarged and truncate tips on fingers III and IV (rounded finger tips), and advertisement call ( Padial et al., 2005b, 2008). From O. quixensis by smaller size, mean SVL of males and females, 24.8 and 29.3 mm, respectively (mean SVL of adult males, 39.0 mm, N = 9; mean SVL of adult females, 50.4 mm, N = 14) ( Table 3); coarsely shagreened dorsal skin with enlarged warts (dorsal skin coarsely tuberculate, with enlarged and prominent warts and granules, some of them keratinized); slightly enlarged and truncate tips on fingers III and IV (rounded finger tips). From O. sanctaecrucis by smaller size, mean SVL of males and females, 24.8 and 29.3 mm, respectively (mean SVL of adult males, 35.2 mm, N = 3; mean SVL of adult females, 46.0 mm, N = 3) ( Table 3); coarsely shagreened dorsal skin with enlarged warts (dorsal skin coarsely tuberculate, with enlarged and prominent warts and granules, some of them keratinized); slightly enlarged and truncate disc on fingers III and IV (rounded finger tips). From O. sanderi it differs by smaller size (mean SVL of adult males, 29.2 mm, N = 6; mean SVL of adult females, 36.5 mm, N = 4) ( Table 3); head longer than wide (wider than long); coarsely shagreened dorsal skin with enlarged warts (dorsal skin covered by sparse keratinized granules and some warts); slightly enlarged and truncate tips on fingers III and IV (rounded finger tips). From O. saxatilis by smaller size, mean SVL of females, 29.3 mm (49.0 and 43.7 mm, holotype and paratype, respectively) ( Table 3); coarsely shagreened dorsal skin with enlarged warts (dorsal skin coarsely tuberculate, with enlarged and prominent warts and granules, some of them keratinized); slightly enlarged and truncate disc on fingers III and IV (rounded finger tips). From O. simmonsi by having coarsely shagreened dorsal skin with enlarged warts (densely granular with round, pungent, keratinized granules); slightly enlarged and truncate tips on fingers III and IV (rounded finger tips); ulnar tubercles absent (abundant, round, small). From E. zongoensis by having coarsely shagreened dorsal skin with enlarged warts (densely granular with round, pungent, keratinized granules); slightly enlarged and truncate tips on fingers III and IV (rounded finger tips); head longer than wide (wider than long).

Description of the holotype: An adult female (small ovarian eggs) with head slightly longer than wide; snout round in dorsal view, and round to subacuminate in lateral profile; nostrils slightly protuberant, orientated dorsolaterally; canthus rostralis straight in dorsal view, round in frontal profile; loreal region slightly concave, sloping gradually to the lips; lips not flared; upper eyelid without tubercles, but covered by small warts; no cranial crests. Supratympanic fold distinct, thin, short; tympanic membrane and its annulus, distinct; tympanic membrane slightly ovate vertically, its length about two-fifths of eye length; two postrictal glands. Choanae not concealed by palatal shelf of the maxillary arch when roof of mouth is viewed from below; choanae large, round, lateral, separated by distance equal to four times the diameter of a choana; the specimen has one discernible vomerine odontophore, situated posteromedial to and far from the choanae. Skin texture of dorsal surfaces and posterior parts of hind limbs composed of small, low, round warts; ventral surfaces smooth; a W-shaped occipital fold; no dorsolateral folds; discoidal fold evident.

Ulnar tubercles absent; palmar tubercle bifid, flat, prominent; thenar tubercle ovate, prominent, twothirds of the size of the palmar tubercle; supernumerary tubercles large, round, prominent, smaller than subarticular tubercles; subarticular tubercles large, prominent, subconical; tips of fingers I and II round, not enlarged, and those of fingers III and IV moderately enlarged, truncate; basal lateral fringes on fingers I–III; relative length of fingers: II <I ³ IV <III.

Toes long and slender (foot length 50% of SVL); heel and tarsus lacking tubercles or folds; inner metatarsal tubercle round, prominent, slightly larger than outer metatarsal tubercle; outer metatarsal tubercle round, conical; six supernumerary tubercles, small, round to elongate; subarticular tubercles prominent, subconical to conical; toes with basal lateral fringes; toes I and II with tips rounded, not expanded, toes III–V with slightly enlarged and truncate tips; ungual flap not indented; relative length of toes, I <II <V <III <IV; toes III and V reaching penultimate subarticular tubercle of toe IV.

Dorsal surfaces reddish brown, with darker marks including a W-shaped occipital dark brown mark, an interocular bar, two subocular dark brown stripes, and a supratympanic stripe. Arms and hindlimbs light brown with transverse brown stripes; concealed surfaces of hindlimbs brown; flanks beige with dark brown spots that merge in an oblique wide band posterior to the arm insertion; ventrally cream with fine grey mottling on throat, chest, and anterior margin of belly.

Measurements of the holotype: SVL, 27.4 mm; HL, 8.9 mm; HW, 9.2 mm; EL, 4.1 mm; EN, 3.2 mm; IND, 2.4 mm; EE, 4.4 mm; TYH, 1.7 mm; TYL, 1.4 mm; FA, 5.6 mm; TL, 14.6 mm; TH, 14.1 mm; FL, 14.0 mm.

Variation: The most variable characters of O. cruralis are the size of adults and the coloration. These two characters can lead to confusion with other species. Although we have removed several taxa (with different adult sizes) from what was thought to be ‘ O. cruralis ’ (see remarks section below and on O. granulosus ), the variation in size of this species is still considerably high compared with other members of this genus. However, this is the species for which the largest data set has been analysed, and hence such observed variability may be influenced by sample size. Adult males of O. cruralis range from 20.3 to 30.2 mm, and females from 24.9 to 33.6 mm. The sizes of males and females overlap broadly. Another very relevant character is skin texture, but this character is easily diagnosable under a stereomicroscope. The dorsal skin texture of this species varies from scarcely warty (almost smooth) to densely and homogeneously warty with few or abundant enlarged warts. We consider the skin texture to be warty, although it has also been considered as rugose ( Boulenger, 1902), shagreened, or smooth to finely areolate ( Padial et al., 2005a, b). The relevant distinction is that the dorsal skin of this species lacks granules (i.e. hard, keratinized structures, usually rounded or conical) or tubercles (enlarged, prominent, conical warts). All dorsal warts are always flat, low, and constitute soft structures. As in O. granulosus and O. sanderi , there are two colour morphs. The most commom morph consists of a pale to dark brown or reddish brown dorsum, with pale and dark irregular flecks, a W-shaped mark on occipital region, and a x-shaped mark on the mid-dorsum, one or two broad dark oblique bands on flanks, and dark interocular, labial, and transversal bars on the extremities. This pattern occurs in 60 of 91 (66%) specimens for which the colour pattern was noted. Another 26 specimens (29%) show the following colour pattern: a pale to dark brown or reddish brown dorsum outlined by a pair of pale dorsolateral bands, a sacral stripe, and two wide dark brown stripes on flanks, one anterior to the groin and one posterior to the arm insertion, with the transverse bars on the extremities less evident. The intensity and tonalities of both patterns varies. A third, rare colour pattern, shared only with E. madidi , is the presence of a thin, white (in alcohol, yellow in life) mid-dorsal stripe from snout to vent. This pattern was observed in five specimens (one female and four males). In all three morphs, the ventral pattern is similar: overall cream with fine mottling on throat and chest, mottling varying in density, intensity, and colour, from grey to dark brown. Other variable characters are as follows. Although breeding males of O. cruralis do not have nuptial pads, a nonswollen white region can be observed on the dorsal surface of the thumbs of some individuals. Axillary glands can be present or absent, or present on only one side; finger fringes can be present (weak) or absent; a faint thin mid-dorsal fold is shown in some specimens; the number of supernumerary tubercles on a single toe varies from two to four, and from weak to prominent; the degree of enlargement of finger tips of fingers III and IV varies, although this variation seems to be related to fixation. The most divergent specimens studied by us are those from La Hoyada (MNK A 5577 and ZFMK 72644), which are overall dark greyish-brown, and have conspicuous finger and toe fringes. Specimens from the lowlands of Peru (KU207749, 215461–2) seem to have slightly indented ungual flaps on the fingers. Specimens from higher altitudes are more affected by parasitic subdermal mites (see Wohltmann, Köhler & Martin, 2006), which may lead one to think they have unusual skin structures.

Remarks: The specimens AMNH 91579, 153046, 153085, 153086, and KU 173230–32 were identified in collections as O. cruralis , but they are neither O. cruralis nor any other known species of Oreobates . The specimens AMNH 91579, KU 173230–32, and MZUM 64120 and 135341, identified by Lynch (1989) as O. cruralis , do not correspond with any known species of Oreobates . The specimen KU 182814 illustrated as O. cruralis (see Harvey & Keck 1995: fig 3) is an adult female of O. discoidalis . The comparison between O. discoidalis and O. cruralis provided by Cei (1987) includes some observations that do not correspond with characters of O. cruralis . The broad range of adult size and intraspecific genetic distances, the broad altitudinal gradient occupied by this species (including several life zones), and the broad latitudinal distribution, together with some differences in advertisement calls ( Padial et al., 2008), suggest that the name O. cruralis is perhaps still being applied to more than one species. The best candidates to be recognized as new species are those populations from humid montane forests and cloud forests in the departments of Cochabamba and Santa Cruz, Bolivia, but our data are still inconclusive.

Distribution: This species inhabits the lowland rainforests, humid forests, and cloud forests of the Andean foothills from 200 to 2000 m a.s.l., from Department Cusco in southern Peru to Department Santa Cruz in central Bolivia ( Figs 4 , 5 ). This species also reaches the semideciduous forests of the inter- Andean valleys of central Bolivia. Cei (1987) tentatively cited O. cruralis for Argentina without locality, but Lavilla & Cei (2001) discarded this possibility. Köhler (2000), Reichle et al. (2001), and Padial et al. (2008) described its advertisement call. Some data on its biology and ecology can be found in Köhler (2000), Doan & Arizábal (2002), and Duellman (2005).

Figures

Figure 4. Type localities of members of Oreobates: (1) O. quixensis, San José de Moti, Prov. Napo, Ecuador; (2) O. simmonsi, Río Piuntza, 1830 m a.s.l., Cordillera del Cóndor, Prov. Morona-Santiago, Ecuador; (3) O. saxatilis, Ponga de Shilcayo, 470 m a.s.l., Department San Martín, Peru; (4) O. lehri, Apurimac River Valley, 2445 m a.s.l., Department Cusco, Peru; (5) O. granulosus, Santo Domingo, Carabaya, Department Puno, Peru, 1800 m a.s.l.; (6) O. madidi, Arroyo Huacataya, Serranía Eslabón, 1500 m a.s.l., Department La Paz, Bolivia; (7) O. sanderi, Arroyo Bilunto, Chunirumi Valley, 1800 m a.s.l., near Santa Cruz de Valle Ameno, Department La Paz, Bolivia; (8) O. zongoensis, Valle de Zongo, 1250 m a.s.l., Department La Paz, Bolivia; (9) O. choristolemma, Serranía de Bellavista c. 1000 m a.s.l., Department La Paz, Bolivia; (10) O. cruralis, Department La Paz, Bolivia, 4000 m a.s.l. (in error); (11) O. heterodactylus, gruta Facendinha, State Mato-Grosso, Brazil; (12) O. ibischi, km 68.5 on Santa Cruz de la Sierra-Samaipata road c. 750 m a.s.l., Department Santa Cruz, Bolivia; (13) O. sanctaecrucis, El Chapé, Department Santa Cruz, Bolivia, 2060 m a.s.l.; (14) O. discoidalis, Tucumán, Prov. Tucumán, Argentina.

Figure 5. Altitudinal distribution across habitat types of members of the genus Oreobates.

Figure 6. Type specimens of some members of Oreobates. A–B, holotype of O. cruralis (BM 1947.2.15.70); C–D, holotype of O. simmonsi (KU 147068); E–F, paralectotype of O. discoidalis (BM 1947.2.15.63); G–H, holotype of O. granulosus (BM 1947.2.15.72); I–J, lectotype of O. quixensis (MNCN 1708).