Osteocephalus festae (Peracca, 1904)

Ron, Santiago R., Toral, Eduardo, Venegas, Pablo J. & Barnes, Charles W., 2010, Taxonomic revision and phylogenetic position of Osteocephalus festae (Anura, Hylidae) with description of its larva, ZooKeys 70, pp. 67-92 : 71-79

Osteocephalus festae (Peracca, 1904)

Hyla festae Peracca, 1904:39. Holotype: MZUT An208, a female from "Valle Santiago" ("= lower Río Zamora" according to Trueb and Duellman 1971) Provincia Morona Santiago, Ecuador (Fig. 3G-H).

Osteocephalus buckleyi (part) Trueb and Duellman 1971. Synonymy fide Trueb and Duellman 1971: 23.

Diagnosis.

Throughout this section, coloration refers to preserved specimens unless otherwise noted. Osteocephalus festae is a medium-sized species of Osteocephalus having the following combination of characters: (1) size sexually dimorphic; maximum SVL in males 56.1 mm, in females 84.9 mm; (2) skin on dorsum bearing tubercles in males, smooth in females; (3) skin on flanks areolate; (4) hand webbing formula II 2½-3¼III3½ -2IV; foot webbing formula varying as shown in Table 3 and Fig. 4; (5) dorsum brown, usually with irregular dark marks; (6) venter varying from cream to tan, with ill to well defined brown chocolate blotches; (7) narrow, cream to light brown, labial stripe confluent with similarly colored suborbital mark; (8) flanks cream to light brown with darker reticulations anteriorly and dark blotches posteriorly; (9) dermal roofing bones of the skull weakly exostosed; (10) bones green in life; (11) iris dark brown without reticulations, in life; (12) paired vocal sacs located laterally, behind jaw articulation, (13) in life, juveniles with red iris, and pale elbows, knees, and heels; (14) larvae with LTRF of 4/7 or 5/7.

Osteocephalus festae is most similar to Osteocephalus verruciger . Both species differ from other Osteocephalus by the combination of a brown iris (in life) and the presence of brown marks in the venter (in life and preservative). Osteocephalus festae differs from Osteocephalus verruciger in having: (1) less dorsal ornamentation in males (fewer and less developed dorsal tubercles in Osteocephalus festae ), (2) smaller tympanum (1/5 of head length in Osteocephalus festae vs. 1/4 in Osteocephalus verruciger ), and (3) more tooth rows in larvae (LTRF = 4/7 to 5/7 in Osteocephalus festae vs. 2/5 in Osteocephalus verruciger ; Fig. 5). Mitochondrial DNA sequences show that Osteocephalus festae and Osteocephalus verruciger are not sister species (Fig. 2). Osteocephalus festae differs from Osteocephalus mutabor Jungfer & Hödl, 2002 in having chocolate blotches in the venter (blotches absent in Osteocephalus mutabor ). It differs from most species of Osteocephalus (except Osteocephalus verruciger , Osteocephalus heyeri Lynch, 2002, and Osteocephalus subtilis Martins & Cardoso, 1987) in having a dark brown iris in life (iris bronze to golden with or without black straight lines or irregular black reticulations in Osteocephalus alboguttatus (Boulenger, 1882), Osteocephalus buckleyi , Osteocephalus cabrerai (Cochran & Goin, 1970), Osteocephalus deridens Jungfer et al., 2000, Osteocephalus exophthalmus Smith & Noonan, 2001, Osteocephalus fuscifacies Jungfer et al., 2000, Osteocephalus leoniae Jungfer & Lehr, 2001, Osteocephalus leprieurii ( Duméril & Bibron, 1841), Osteocephalus mutabor , Osteocephalus oophagus Jungfer & Schiesari, 1995, Osteocephalus pearsoni (Gaige, 1929), Osteocephalus phasmatus MacCulloch & Lathrop, 2005, Osteocephalus planiceps Cope, 1874, Osteocephalus taurinus Steindachner, 1862, and Osteocephalus yasuni Ron & Pramuk, 1999). Osteocephalus mimeticus (Melin, 1941) can be discriminated from Osteocephalus festae in having a black iris with golden marks. Osteocephalus festae differs from Osteocephalus subtilis and Osteocephalus heyeri in size (maximum male SVL 38.8 mm in Osteocephalus subtilis , 36.1 mm in Osteocephalus heyeri vs. 56.1 mm in Osteocephalus festae ). The presence of areolate skin in the flanks, specially anteriorly, distinguish Osteocephalus festae from Osteocephalus leprieurii , Osteocephalus mutabor , Osteocephalus pearsoni , Osteocephalus planiceps , and Osteocephalus yasuni (smooth to granular skin on flanks; Trueb & Duellman, 1971). Osteocephalus taurinus has weakly areolate skin restricted to the axillary region. Osteocephalus festae further differs from Osteocephalus buckleyi and Osteocephalus cabrerai in lacking prominent tarsal tubercles ( Jungfer 2010).

Holotype.

The holotype is an adult female with SVL = 78 mm (Fig. 3G, H; Peracca, 1904). The descriptions provided by Peracca (1904) and Jungfer (2010) are adequate.

Variation.

Variation in dorsal and ventral coloration of preserved specimens is shown in Figures 6 and 7. Dorsal coloration consists of a light brown to dark brown background with irregular marks. There is sexual dimorphism in dorsal tuberculation: in females the dorsum is smooth while in males it varies between having scant and ill-defined non-keratinized tubercles (most males from Río Napinaza, e.g., QCAZ 26488) to having abundant keratinized tubercles (two males from Chonza Alta, e.g., CORBIDI 758; Fig. 3B).

Ventral surfaces of preserved specimens (Fig. 7) have a cream (QCAZ 39364) to tan (QCAZ 39806) background with darker brown marks that are more distinct and abundant in females (e.g., QCAZ 39811) than in males (e.g., QCAZ 39799); a male from Río Lejía (CORBIDI 623) has an immaculate venter. Ventrally, limbs vary from brown to cream; in QCAZ 39809 and 39811 cream dots are present on hindlimbs; scant cream tubercles can be present in the external edge of the forearm (e.g., QCAZ 39804). The vent region is dark brown to brown bordered by a lighter area (cream to tan). Flanks are areolate in the anterior half and smooth posteriorly. The areolate portion is cream with dark brown reticulation; the posterior half is cream (e.g., QCAZ39810) to light brown (e.g., QCAZ 39806) with dark brown blotches.

Head shape is rounded in dorsal view and rounded (e.g., QCAZ 39803) to bluntly rounded (e.g., QCAZ 39800-01) in lateral view. Lateral head coloration varies between dark brown (QCAZ 11625) to light brown (QCAZ 39810). Except for QCAZ 39802 and 41039, there is a lighter (brown to cream) subocular mark. A tan (QCAZ 39805) to cream (QCAZ 39364) labial stripe is always present. The tympanic annulus is concealed dorsally and has lighter color than the background. Variation in hand and foot webbing is shown in Table 3. The distal subarticular tubercle on Finger IV is single in all specimens.

Morphometric data pertain to adults and are summarized in Table 4. In the examined series, the largest male has a SVL of 56.09 mm and the largest female 84.94 mm; mean male SVL = 49.47 mm (n = 12; SD = 5.10), mean female SVL = 67.92 mm (n = 27; SD = 10.08). Females are significantly larger than males (t = 5.52, df = 23, P <0.001). A MANOVA on the residuals of the regressions between SVL and the other measured variables indicates lack of significant differences between sexes in size-free morphometry (F = 1.052, df = 17, P = 0.433).

Color in life.

Based on digital photograph of adult female QCAZ 41039 (Fig. 3A): dorsum dark brown with irregular light brown and yellowish green marks; canthal region dark brown with yellowish green subocular mark and labial band; tympanum brown; flanks greenish brown with dark brown reticulation anteriorly and irregular dark brown marks posteriorly; dorsal surfaces of thighs and shanks dark brown with transversal brown bands bordered with light brown; dorsal surfaces of forelimbs dark brown with irregular brown marks; venter light tan with irregular brown marks; bones green; iris dark brown. Female CORBIDI 761 has a predominantly light brown dorsum with irregular brown marks; clear areas on flanks and below the eye and tympanum are light yellow.

There is significant change in coloration between juveniles and adults. The following description is based on a digital photograph of juvenile QCAZ 38081 (Fig. 3E-F). The dorsum beige with black interorbital band and two large medial ovoid black blotches; flanks dark brown; dorsal surfaces of thighs and shanks brown with cream transversal bars; dorsal surfaces of arms cream, dorsal surfaces of forearms brown with cream transversal bars; knees, elbows, and heels cream; anterior half of the venter cream, posterior half light brown; bones green; iris bright red.

Morphometric comparisons.

Three components with eigenvalues> 1.0 were extracted from the PCA for males (Table 5). The three components accounted for 76.4% of the total variation. The highest loadings for the PCA for males were foot length and tibia length for PC I, head length for PC II, and eye diameter and tympanum diameter for PC III (Table 5). The morphometric space of Osteocephalus festae overlaps with Osteocephalus verruciger (Fig. 8) but only slightly with Osteocephalus buckleyi . There are significant differences in PC scores between Osteocephalus festae and Osteocephalus buckleyi along PC II and PC III (t = 2.46, df = 9, P = 0.035; t = 6.76, df = 13, P <0.001, respectively) but not along PC I (t = 1.61, df = 7, P = 0.115). There are significant differences only along PC III between Osteocephalus festae and Osteocephalus verruciger , (t = 9.03, df = 9, P <0.001).

Three components with eigenvalues> 1.0 were extracted from the PCA for females (Table 5). The three components accounted for 80.3% of the total variation. The highest loadings for the PCA for females were tibia length and femur length for PC I, eye diameter and tympanum diameter for PC II, and head width and head length for PC III (Table 5). There is little overlap in the morphometric space of Osteocephalus festae with Osteocephalus verruciger and Osteocephalus buckleyi (Fig. 8). Principal Components scores are significantly different between Osteocephalus festae and Osteocephalus verruciger along PC I and PC III (t = 4.96, df = 21, P <0.001; t = 4.91, df = 21, P <0.001, respectively) but not along PC II (t = 0.85, df = 21, P = 0.403). Similarly, Osteocephalus festae and Osteocephalus buckleyi differed along PC I and PC III (t = 4.96, df = 21, P <0.001; t = 4.91, df = 21, P <0.001, respectively) but not along PC II (t = 0.85, df = 21, P = 0.403).

In the DFA classification procedure, 24 out of 25 specimens of Osteocephalus festae were classified correctly. The misclassified female (QCAZ 38420) was assigned to Osteocephalus verruciger . The multivariate analyses (PCA and DFA) show morphometric differentiation between Osteocephalus festae and the closely related Osteocephalus verruciger and Osteocephalus buckleyi .

Tadpoles.

Letters in parenthesis refer to individual tadpoles on each lot. The following description is based on lot QCAZ 30511 of ten larvae in Stages 25 (A), 26 (B), 31 (C), 32 (D), 33 (E), 34 (F), 35 (G), 39 (H), 40 (I) and 42 (J). Tadpoles were collected at Río Napinaza by E. E. Tapia and I. G. Tapia on October 2003. These larvae belong to the exotrophic, benthic guild as defined by McDiarmid and Altig (1999). Morphometric data are provided in Table 6. In dorsal view, a tadpole in Stage 39 (QCAZ 30511H; Fig. 5A) shows elliptical body, widest between eye and spiracle, with rounded snout. Eyes relatively large (body length about 7.89 times larger than eye diameter), directed and positioned dorsolaterally, not visible in ventral view, and separated by a distance 1.27 times the internarial distance. External nares oval, located dorsolaterally, at about one fourth the distance between anterior margin of snout and anterior margin of eye. In profile (Fig. 5B) body depressed (body width/body height = 0.18), flattened ventrally, snout slightly rounded. Oral disc not emarginated. Spiracle sinistral, inner wall free from body, its tip closer to the vent than the eye. Spiracle opening rounded.

Tail musculature robust, decreasing in size towards tip of tail. Dorsal fin not extending onto body, slightly convex and attaining its maximum height at mid length of tail; tail tip rounded; ventral fin convex, beginning at tail-body junction and tapering gradually towards tail tip. Medial vent tube with both walls attached directly to ventral fin, opening directed posteroventrally. Limbs with subarticular patches. Dorsal body, middle body, supraorbital, infraorbital, posterior supraorbital, and posterior infraorbital lateral lines evident. No glands.

Oral disc anteroventral (Fig. 5B; average transverse width 4.35 mm; 58% of body width), not emarginate, LTRF 4/7; papillae distributed around oral disc; tooth rows complete except for medial gap in row A4; A1 = 304, A2 = 322, A3 = 311, A4 = 108 + 112; P1 = 177, P2 = 235, P3 = 234, P4 = 328, P5 = 284, P6 = 330, and P7 = 177.

In preservative, dorsum brown with darker marks between eyes; dark brown dorsolateral stripes extend from mid-body to base of tail; caudal musculature beige with brown spots (Fig 5); skin of flanks, spiracle, vent tube, fins, and around the eyes transparent; belly and fins transparent with white blotches.

Tadpole variation and comparisons with other species.

In QCAZ 38074, 26321, 26053, 26498 and 26284 the caudal musculature is cream with brown dots; fins can have dark brown spots without white blotches (e.g., QCAZ 38074, 26321). The LTRF is the same in all stages but in stage 42, rows A2-A4 and P1-P3 have approximately half the number of teeth.

In preservative, ten tadpoles collected in Chonza Alta, Peru, lot CORBIDI-CL-10 in Stages 37 (A-B), 36 (C), 34 (D), 32 (E), 31 (F), 42 (G, H, I) and 44 (J) have dorsum brown with darker marks between the eyes; dark brown dorsolateral stripes from mid-body to base of tail; caudal musculature cream with abundant melanophores; skin of flanks, spiracle, vent tube, and fins transparent; skin around the eyes brown; belly and fins transparent with abundant melanophores. Oral disc with LTRF 5/7; papillae distributed around oral disc; tooth rows complete except for medial gap in row A5.

In life (Fig. 5E-F; QCAZ 38074, stage 33; based on digital photograph), dorsum dark brown with darker marks between the eyes; dark brown dorsolateral lines from mid-body to base of tail; tail musculature light brown with small dark brown melanophores; white dots at tail-body junction; skin is transparent ventrally in anterior half of body and ventrolaterally in the posterior half; tail musculature light brown with dark brown spots; fins transparent. Iris bronze. Live tadpoles from Chonza Alta (CORBIDI-CL-10) have dorsum and caudal musculature olive brown; skin transparent ventrally with bright brown flecks, gut visible through the skin; fins translucent brown.

Larvae of Osteocephalus verruciger differ from those of Osteocephalus festae (in parentheses) by being smaller, having uniform dark body (tan to cream), LTRF = 2/5 (4/7 to 5/7); and having a dorsal gap in marginal papillae (marginal papillae complete). For comparison, larvae of Osteocephalus verruciger is shown in Figure 5 G–H. Differences were verified in 30 Osteocephalus verruciger larvae from four localities (lots QCAZ 1579, 10798, 21405 and 36751). Larvae of Osteocephalus festae have the highest number of tooth rows known among Osteocephalus (LTRF = 2/3 in Osteocephalus oophagus , 2/6 in Osteocephalus buckleyi and Osteocephalus taurinus ; Hero 1990; Jungfer and Schiesari 1995).

Distribution and ecology.

Osteocephalus festae has been recorded at nine localities in the Ecuadorian (Loja, Morona Santiago, and Zamora-Chinchipe provinces) and Peruvian Amazon basin (Mariscal Cáceres and Rioja provinces). Localities with known elevation ( Río Napinaza, Miasí, San Francisco, Reserva Tapichalaca, Río Lejia, Chonza Alta, Camñopite Bajo, and Naranjillo) range between 1000 and 2200 m of elevation. The elevation at San Francisco (2200 m) is the highest known for Osteocephalus . Maximum airline distance between localities is 440 km. Osteocephalus festae and Osteocephalus verruciger have similar elevational ranges and seem to replace each other latitudinally in Ecuador (Fig. 1). Records of Osteocephalus verruciger from Peru (e.g., Trueb and Duellman 1970) are likely misidentified Osteocephalus mimeticus ( Jungfer 2010). Thus, the southernmost confirmed records of Osteocephalus verruciger are those from Provincia Morona Santiago, Ecuador.

Most of our specimens of Osteocephalus festae are from Río Napinaza, a river surrounded by secondary forest, pastures and agricultural lands. At the collection site, the river has an average width of 2.85 m and an average depth of 23 cm with fast running water and waterfalls that reach 10 m in height ( Salazar-Valenzuela 2007). Tadpoles were found in small ponds in the margins of the river. Adults were observed at night next to the river or within the forest on vegetation 40 to 250 cm above the ground.

All the specimens collected in Las Cataratas de Paraiso (Chonza Alta) and Camñopite were found at night on vegetation 50 to 300 cm above the ground, next to fast running streams. Tadpoles (CORBIDI-CL-10) were found in a rocky stream with average width of 4 m and an average depth of 30 to 40 cm with fast running water, close to the base of a waterfall. At both sites the streams are surrounded by secondary forest, pastures and agricultural lands. The specimens from Bajo Naranjillo and Río Lejia were found at night on branches 150 to 200 cm above the ground (in primary forest at Río Lejia and secondary forest surrounded by pastures at Naranjillo).

At Las Cataratas de Paraiso (Chonza Alta), on 1 December 2007, we found twelve males calling from the low vegetation and six amplectant pairs (Fig. 3B). Recently metamorphosed individuals were perching on leaves and rocks at the shore. On 4 November 2008, at the same stream, we only found one adult non-amplectant female, two adult males, several tadpoles, and 12 freshly metamorphosed juveniles on leaves and rocks (e.g., CORBIDI 1962-64). The rainy season in this region generally starts in December but during our surveys heavy rains fell since the first week of November. Three gravid females (CORBIDI 761, SVL 68.6 mm; CORBIDI 762, SVL 69.1 mm; CORBIDI 764, SVL 66.6 mm) contained 1080, 1388 and 1290 eggs respectively. A gravid female CORBIDI 624 (SVL = 71.2 mm) from Río Lejia, collected on 29 January 2008, contained 780 eggs. The color of eggs in preservative is black and brownish-cream.

Vegetation types for Ecuadorian localities (according to the classification of Sierra et al. 1999) are: (1) Evergreen Foothill Forest of the Eastern Slopes of the Southern Andes, characterized by abundant epiphytes, trees reaching 30 m of height with Podocarpus as dominant species (Reserva Tapichalaca), (2) Amazonian Mountain Range Evergreen Foothill Forest, characterized by a mixture of Amazonian and Andean vegetation with a canopy of 30 m ( Río Napinaza and Miasí), and (3) Cloud Montane Forest of the Eastern Slopes of the Southern Andes, characterized by trees covered by mosses and abundant epiphytes (San Francisco; Cerón et al. 1999).

Vegetation types of the Peruvian localities (according to Duellman and Pramuk 1999) are Humid Subtropical Forest, characterized by of a variety of moderate to large trees including Juglans neotropica , Cedrela fissipes , Tabebuia , and genera common in the Amazon lowlands like Brosimum , Cordia , Inga , Piper , and Swietenia . At some collecting sites, the forest has been cleared for citrus and coffee plantations.

Taxonomic remarks.

Jungfer (2010) ascribed two females (EPN 5578, MHNG 2560.60) and three males (EPN 5577, EPN AA-5611, EPN 5607) to Osteocephalus festae . Based on data from Jungfer (2010), both females differ from the holotype and 18 adult females analyzed here (in parentheses) in having a venter uniform tan without marks (brown marks present), webbing almost reaching the ultimate subarticular tubercle in the inner edge of third finger (web reaching half the distance between ultimate and penultimate subarticular tubercles), and larger tympanum size with TD/HL = 0.23-0.25 (TD/HL = 0.14-0.22 among 39 adult males and females). In addition, we did not find the sexual dimorphism in relative tympanum size reported by Jungfer ( Student’s t = 1.227, df = 23, P = 0.232). Males assigned to Osteocephalus festae also seem to differ from our series in the extent of the axillary membrane (covering half of the upper arm vs. one third to one fourth in our series). The discrepancies suggest that at least some of the specimens assigned to Osteocephalus festae by Jungfer (2010) may belong to a different species.