Osteocephalus camufatus, Jungfer, Karl-Heinz, Verdade, Vanessa K., Faivovich, Julián & Rodrigues, Miguel T., 2016

Jungfer, Karl-Heinz, Verdade, Vanessa K., Faivovich, Julián & Rodrigues, Miguel T., 2016, A new species of spiny-backed treefrog (Osteocephalus) from Central Amazonian Brazil (Amphibia: Anura: Hylidae), Zootaxa 4114 (2), pp. 171-181 : 172-178

Osteocephalus camufatus sp. nov.

( Figs. 1–4 )

Osteocephalus buckleyi [Ca1_MTR12779_2748]— Jungfer et al. 2013

Holotype: MZUSP 142389 (field number MTR 12779), an adult male of 39.5 mm SVL with well-developed nuptial pads from Brazil: Amazonas: Igarapé-açu (04°20'40''S 58°38'06''W), right bank of Rio Abacaxis, 30 m asl., collected by Miguel T. Rodrigues, Sergio Marques de Souza, José Cassimiro and José Mário Guellere, on 9 January 2007 ( Figs. 1–4 ).

Paratype: MZUSP 157020 (field number MTR 13147), an adult male with well-developed nuptial pads from Brazil: Amazonas: Areal, left bank of Rio Abacaxis (04°35'49''S 58°13'14''W), 39 m asl., collected by Miguel T. Rodrigues, Sergio Marques de Souza, José Cassimiro and José Mário Guellere, on 20 January 2007.

Diagnosis and comparisons. Osteocephalus camufatus may be diagnosed as (1) a small to medium sized species (as defined by Jungfer 2010: 29) in males (females unknown); (2) skin on dorsum of males shagreen with a few irregular small tubercles, only some bearing keratinized tips; (3) skin on flanks coarsely areolate between limb insertions; (4) rounded, tuberculate canthus rostralis curved inward; (5) frontoparietal ridges not visible externally; (6) dentigerous processes of vomers angular; (7) thick tuberculate supratympanic fold from the posterior edge of the orbit sloping in an arch towards the arm insertion, not reaching below tympanum posteroventrally; (8) webbing on inner edge of third finger extending slightly beyond penultimate subarticular tubercle; (9) distal subarticular tubercle on Finger IV bifid; (10) dorsum boldly blotched irregularly; (11) throat, chest and venter creamy tan to creamy white with numerous irregular tan spots; (12) supralabial area with irregular light and dark markings; (13) flanks light with irregular dark markings; (14) vocal sacs paired, protruding ventral to angles of jaws; (15) juvenile colouration unknown; (16) tadpole habitat (most likely in pools along streams) and labial tooth row formula unknown; (17) colour of tibiofibular bones white in preservative.

O. camufatus is a member of the O. buckleyi species group as revealed by molecular data. A phylogenetic analysis using both maximum parsimony (MP) and likelihood (ML) inference resulted in trees that showed that O. camufatus was basal to a large and well-supported clade containing frogs from large areas of Amazonia and Guiana. The oldest available name for this clade is O. helenae ( Jungfer et al. 2013) . Uncorrected p distances of the mitochondrial 16S gene between O. camufatus and O. helenae from various localities were 1.3–2.6, while genetic divergences within O. helenae , whose subclade relationships are not yet sufficiently resolved, were 0.0–2.2 ( Jungfer et al. 2013: Appendix S4d).

The new species shares with several other species of the group the following character states: 1) greenish ground colour, 2) strongly tuberculate canthus rostralis and upper eyelids and 3) posterior surfaces of thighs light with large dark brown spots in preservative. These three characters distinguish it from all frogs in the O. alboguttatus , O. leprieurii , O. planiceps and O. taurinus groups ( Jungfer et al. 2013) in which the ground colours are shades of tan or brown, the canthus rostralis is smooth to granulate and the posterior thigh surfaces are uniform. From other species in the O. buckleyi group it differs as follows (characters of O. camufatus in parentheses): Six upland species from the eastern Andean slopes between 600 and 2300 m differ as follows: in Osteocephalus carri , a predominantly brown species (bold blotches of green and brown), the canthus rostralis and upper eyelids are smooth (strongly tuberculate) and the iris is black with golden spots in life (light); O. duellmani is a tan species with or without dark brown blotches (bold blotches of green and brown), with the posterior surfaces of the thighs uniform tan (marbled) and the canthus and upper eyelid bearing a few low tubercles (strongly tuberculate); O. festae exhibits brown ground colour (bold blotches of green and brown), a dark brown iris in life (light, Fig. 4 ) and uniform tan posterior thigh surfaces (marbled). Males of Osteocephalus mimeticus , O. mutabor (the latter also occurring as low as 150 m asl.) and O. verruciger have a brown ground color lacking green (blotches in shades of green and brown), uniform posterior thigh surfaces (marbled dark brown), and heavily tuberculate dorsa with numerous spinous tubercles bearing keratinized tips during breeding (a few irregular small tubercles, few of them with keratinization). Species of the O. buckleyi group from the lowlands (<600 m asl.), that in some cases share the greenish ground colour of O. camufatus , differ as follows: Osteocephalus buckleyi has low tubercles or is smooth on the upper eyelid (strongly tuberculate), and has low or lacks tarsal tubercles (prominent). Breeding males of O. buckleyi exhibit dorsal tubercles, many with keratinized tips (few keratinized tips). Osteocephalus cabrerai has a row of tubercles on the lower jaw (absent) and an irregular, deep fringe on the outer edge of Finger IV (low tubercles on proximal segment of Finger IV). Osteocephalus cannatellai from lowlands, but also up to 1290 m asl. ( Ron et al. 2012), appears to be larger (38.5–57.2 mm SVL in males, mean, 46.8 mm, Ron et al. 2012) (to 40.4 mm, but note that the sample size is n=2), and differs by a longer supratympanic fold that reaches the arm insertion (not reaching lower level of tympanum); axillary membrane present (absent); usually a dark venter varying from light grey to brown with or without dark markings ( Ron et al. 2012) (yellowish white with small irregular brown spots). Osteocephalus helenae (Ruthven) is a variable frog throughout its range. Specimens from localities closest to the two sites known for O. camufatus , from about 230 km northwest of the type locality, near Manaus and other sites just north and south of the Amazonas in Amazonas, Brazil, exhibit an axillary membrane (absent), a scalloped fringe on the outer edge of Finger IV continued to the ulna (low, indistinct tubercles on proximal segment of Finger IV and single tubercles on ulna), and more webbing on the hand, reaching beyond the distal subarticular tubercle on Finger IV (to distal subarticular tubercle, Fig. 4 a). Specimens from near Rio Branco, Acre, Brazil, roughly 1100 km WSW of the type locality of O. camufatus , have posterior thigh surfaces brown, finely mottled with cream (bold dark brown markings on light ground) and lack tubercles on the eyelids (present).

Frogs in the closely related genus Dryaderces are similar in general appearance to some frogs of the O. buckleyi group, but can be distinguished as follows: They differ in exhibiting bold dark ventral reticulation (dark spotting) and uniform dark iris (light iris) in D. pearsoni (Gaige) , a longer snout of EN/HL 0.27–0.33 (shorter, EN/ HL 0.25), non-tuberculate canthus rostralis (tuberculate) and light, uniform venter (venter with small dark spots) in Dryaderces sp. ( Dryaderces pearsoni [Ca1_MTR13158_2768] of Jungfer et al. 2013) (KHJ, unpublished data). The inspection of a fresh specimen of “ Osteocephalus ” inframaculatus (Boulenger), a species until recently only known from the holotype and tentatively placed with the O. buckleyi group by Jungfer (2010), was placed in Dryaderces by Hoogmoed (2013). It is easily distinguishable from O. camufatus by its bold dark markings on throat and chest and has a longer snout with EN/HL 0.33 (0.25) and larger tympanum with TD/HL 0.26 (0.22– 0.23).

Description of holotype. Snout short (EN/HL 0.245) and blunt, head as long as wide. Nostrils raised, opening laterally. Snout truncate in dorsal and lateral outline. Canthus rostralis well-developed, rounded, describing an inwardly curved line, bearing large tubercles. Skin of head coarsely shagreen, orbits with a few additional small tubercles, some bearing small keratinized tips. A few more scattered keratinized tips on some tubercles of the head and anterior part of the body. No frontoparietal crests evident externally. Loreal region strongly concave bearing low tubercles. Lips flared below the eye. Choanae oblique, elliptical, though slightly angular. Dentigerous processes of vomers short, considerably shorter than choanae width, angular, not in contact with each other, bearing 4 teeth on the left and 3 on the right. The anterior edges of the dentigerous processes are in line with the posterior third of the choanae, their posterior edges well behind the posterior margins of the choanae. Tongue elliptical, slightly wider (by 6%) than long. The vocal sacs are paired, subgular and protrude ventral to the jaw articulation. A thick glandular supratympanic fold from the posterior part of the orbit medially, covering tympanic annulus dorsally from “11” (when tympanum is thought to be a clock face) to “3”, then sloping in a curve towards the arm insertion, reaching no further than the lower one third level of the tympanum. The latter is conspicuous, rounded (barely wider than high), with about 66% the diameter of the eye. Skin on dorsum coarsely shagreen with a few low, irregularly spaced tubercles. Transversal furrows on the shoulders are absent. Skin smooth between eye and tympanum and areolate posterior to the tympanum above the arm insertion, very coarsely areolate laterally between the limb insertions. Throat and belly areolate. Cloacal opening situated at about half the level of thighs, surrounded by large, irregular warts (except on the cloacal flap, which is smooth). Skin on arms shagreen with a few faint tubercles dorsally, hidden surfaces finely shagreen. A row of low ulnar tubercles also encompasses the proximal segment of Finger IV. Axillary membrane absent. Dorsal surfaces of hind legs shagreen, posterior surfaces of thighs and ventral parts of shank smooth, proximal three fourths of thigh coarsely areolate ventrally. A row of low outer tarsal tubercles from the heel to the proximal subarticular tubercle of Toe V. On the heel, three and four low tubercles, respectively, directed dorsally and laterally. Finger and toe discs elliptical and wider than long. Diameter of disc on Finger III is 74% of tympanum diameter. Relative finger length is I <II <IV <III. On the thumb dark brown nuptial excrescences on the posterolateral side from its base to the level of the distal end of the subarticular tubercle. A large elliptical thenar tubercle. Two rounded palmar tubercles. Proximal segments of Fingers II–IV tuberculate, two supernumerary tubercles each on Finger II and Finger IV. Subarticular tubercles conical except the distal ones on Finger III and Finger IV, which are bifid. Webbing formula is I basal II 1 ½—2 ¾ III 2 ⅓— 2 IV.

On the foot a large elliptical inner metatarsal tubercle and a small rounded plantar tubercle. A larger rounded conical outer metatarsal tubercle in line with the row of tarsal tubercles. The latter form a shallow fringe on the distal part of the proximal toe segment that is continued to the toe disc. A few indistinct supernumerary tubercles on the proximal segments of Toes III–V. Subarticular tubercles single and conical. Relative lengths of appressed toes I <II <III ≤ IV <V. Webbing formula: I 1—2 - II 1—2 III 1—1 + IV 1 +— 1 V.

Measurements and proportions. SVL 39.5; HL 14.3; HW 14.3; TL 22.2; FL 26.8; ED 4.7; TD 3.1; FD 2.3; EN 3.5; IN 3.4; TE 2.0. HL/SVL 0.36; HW/SVL 0.36; TL/SVL 0.56; FL/SVL 0.68; TD/ED 0.66; TD/FD 1.35; EN/ HL 0.25; EN/SVL 0.09; HL/HW 1.00; TE/TD 0.65; TD/HL 0.22.

Colour in preservative. The ground colour of head and dorsum is light (green in life) with numerous, more or less irregular blotches in tan and dark brown (various shades of brown in life). This pattern extends to the lateral sides of the head and body. One ill-defined dark brown mark somewhat more conspicuous than others has two arms between the eyes (including the orbits), two between the tympana and on midbody the posterior two arms diverging like the lower part of an X and are continued on the flanks. Two additional ill-defined dark brown marks posteriorly to the proximal part of the sacrum, continued to the flanks. Throat and belly with small irregular brown spots. Although there are light areas on the upper lip, there are no discrete labial marks distinguishable from the rest of the pattern. Tympanum tan. Arms dorsally and laterally with irregular dark brown crossbars, with irregular brown spotting ventrally. Legs dorsally with irregular dark brown crossbars, posterior surfaces of thigh and calf marbled dark brown. Ventral surfaces of thigh tan with lighter areolae, of femur tan peppered with darker markings. Webbing tan, slightly marbled. Subcloacal warts are in creamy white and different shades of tan.

Colour in life. Colours were taken from photographs ( Fig. 4 ). Dorsal surfaces covered by bold blotches of different shades of green and brown. A light mark posteroventral to the eye is light green, the posterior part of the upper lip dark brown, of the lower lip white. The tympanum is tan. The iris is light tan in its upper half and creamy white in its lower one, the latter bearing a diffuse dark brown median vertical streak. Upper and lower halves are separated by a weakly demarcated reddish brown horizontal streak and are both finely reticulated black. Some light blue coloration can be seen on the hidden surface of the thigh. Outer tarsal and heel as well as ulnar tubercles are tipped white.

Variation in the paratype. An adult male slightly larger than the holotype (40.4 mm SVL) with welldeveloped nuptial pads. The snout is bluntly rounded in dorsal aspect. The dentigerous processes bear five teeth on each side. Keratinized tips on tubercles are lacking entirely. Coloration is similar, but the large tan dorsal mark is less conspicuously outlined. The belly is spotted evenly. There is slightly more webbing on the hand with I basal II 1 2/3—2 2/3 III 2—2 IV and little variation on the foot: I 1 +—2 II 1—2 - III 1—1 1/3 IV 1 1/3— 1 V. There is also little variation in proportions.

Measurements and proportions. SVL 40.4; HL 15.0; HW 14.9; TL 21.2; FL 25.9; ED 5.0; TD 3.4; FD 2.1; EN 3.7; IN 3.3; TE 1.9. HL/SVL 0.37; HW/SVL 0.37; TL/SVL 0.53; FL/SVL 0.64; TD/ED 0.68; TD/FD 1.62; EN/ HL 0.25; EN/SVL 0.09; HL/HW 1.01; TE/TD 0.56; TD/HL 0.23.

Distribution and habitat. The new species is so far only known from two sites about 54 km apart along the terra firme forests of the right bank of the Rio Abacaxis, a black water river south of the Amazonas that discharges into Paraná do Arariá, a white water channel delimiting the southern border of Ilha de Tupinambarana ( Fig. 5 ). This is a huge island (about 300 km long) extending between Nova Olinda do Norte on the lower Rio Madeira to Parintins on the Amazonas. Habitat at Igarapé-açu consisted of typical terra firme forest with higher trees reaching up to 40 m and a diameter at breast height of around 80–100 cm. The understory was particularly rich in low palm trees and the leaf litter was dense. The specimen was obtained close to a small stream perched on a tree about 1 m high. At Areal, a site further upstream (also referred to as Paca or Pacamiri locally) the local habitat consisted of an extensive white sand area (campinarana) with scattered vegetation near the margin of the river with abundant clumps of ground bromeliads, gradually replaced by denser areas covered by palm trees and then terra firme forest. The terra firme forest with large trees became more evident farther from the river margin, where the second specimen was obtained.

Etymology. The species name camufatus is the Latinized past participle of Italian camuffare, to disguise or mask, from which the word camouflaged is derived, in allusion to the shape-dissolving pattern of greens and browns of the new species.

Figures

FIGURE 4. Adult male holotype of O. camufatus n. sp. from Igarapé-açu, Rio Abacaxis, Estado Amazonas, Brazil. Enclosure: close-up of the eye.

FIGURE 5. Map of the collecting sites of Osteocephalus camufatus sp. nov. (red dots) in Estado Amazonas, Brazil. The type locality is Igarapé-açu.

FIGURE 1. a. Dorsal, b. ventral view of the preserved holotype of O. camufatus sp. nov.

FIGURE 2. Lateral view of the head, circumcloacal area and posterior surface of thigh of the preserved holotype of O. camufatus sp. nov.

FIGURE 3. a. Right hand and forearm and b. right foot of the preserved holotype of O. camufatus sp. nov. Not to scale.