Allobates hodli Simões, Lima & Farias, 2010, sp. nov

Allobates hodli sp. nov Figures 2–5. Epipedobates femoralis Hödl et al. 2004 p. 823, Catuaba, Acre population (partim). Allobates femoralis Amézquita et al. 2006 p. 1877, Catuaba, Acre population (partim); Lötters et al. 2007 p. 307, Fig. 379; Simões et al. 2008 p. 610, Fig. 2 B. (partim); Amézquita et al. 2009, Fig. 1, Catuaba pattern (partim). Holotype. INPA – H 16555 (original field number APL 2014). Adult male, collected by P. I. Simões and A. P. Lima after recording of advertisement calls at 07: 55 h, 25 th of November 2004, at Cachoeira do Jirau, on the left bank of the upper Madeira River (09.3347° S, 64.7375 ° W), approximately 125 km upstream from the city of Porto Velho, Estado de Rondônia, Brazil. Paratopotypes. INPA-H 16541–16554, INPA-H 16556–16569 (original field numbers APL 2000 –2013, 2015–2018, 2022–2030, 2032), 6 females, 22 males. Collected in the same locality as holotype, 23-25 November 2004 by P. I. Simões and A. P. Lima. Paratypes. All from Brazil. Acre: INPA-H 11621–11640,, 4 females, 17 males, Fazenda Catuaba, Municipality of Rio Branco, 10.0742 ° S, 67.6249 ° W, collected in February 2004 by A. P. Lima. Rondônia: INPA-H 16578, 16584–16587, 16589, 16591 –16592, 16597, 16602 –16603, 16605–16607, 16611–16614, 16620–16624, 16626, 16628, 16631, 16633, 16636–16637, 16639–16641, 16643, 16645 –16646, 16648, 13 females, 26 males, collected on the left bank of the upper Madeira River, across the river from the village of Fortaleza do Abunã, 160 km upstream from the city of Porto Velho, 72 km upstream from Cachoeira do Jirau, 9.5160 ° S, 65.3249 ° W, collected 05-08 January 2005 by P.I. Simões and A.P. Lima. INPA-H 16596, 16730, 16739, 16756, 16758, 16767, 16771, 16777–16778, 16788, 16805, 16818–16819, 2 females, 11 males, collected on the left bank of the upper Madeira River, across the river from the village of Mutum-Paraná, 121 km upstream from the city of Porto Velho, 34 km upstream from Cachoeira do Jirau, 9.5732 ° S, 64.9211 ° W, collected 10–13 January 2005 by P. I. Simões and A. P. Lima. Etymology. The specific epithet is a patronym for Dr. Walter Hödl, an Austrian biologist and professor who pioneered research on behavior and acoustic communication in anurans. For the past two decades, Walter and his students have dedicated special attention to the Allobates femoralis complex. Diagnosis. The new species is assigned to the genus Allobates by the combination of the following characters: presence of a pale dorsolateral stripe, dorsal skin texture granular posteriorly, basal webbing present only between Toes III and IV, Finger I longer than Finger II, finger discs generally weakly expanded (moderately expanded on Finger I), median lingual process absent, testes not pigmented, dark collar absent on throat, oral disc of tadpoles emarginate, not umbelliform. Allobates hodli is distinguished in life from all other species of Allobates (except Allobates femoralis, Allobates myersi and Allobates zaparo) for presenting relatively large body-size (average SVL = 24.76 ± 1.08 mm, males and females pooled), by the lack of brown or light-brown colors or patterning on dorsum and lateral surface of body, and by presenting dark and white marbling on anterior ventral surface of body, replaced by solid reddish-orange color on the ventral surface of hind limbs. Allobates hodli is distinguished from other taxa and morphotypes that form the A. femoralis complex by presenting advertisement calls consisting of groups of two notes repeated in series or bouts (instead of groups of one, three or four notes), and by presenting a conspicuous reddish-orange coloration on the ventral surface of legs, instead of an exclusively black and white reticulated pattern, observed in A. femoralis. Allobates hodli also has diffuse reddish-orange and black patches on dorsal surface of thighs, as opposed to regular, pale (yellowish to red) longitudinal flash marks extending onto the entire dorsal surface of thighs, generally margined by dark patches, observed in typical A. femoralis. A. hodli is distinguished from A. zaparo and A. myersi by the color of dorsum, which is uniformly black/ dark-brown in A. hodli (Fig. 2), but reddish in A. zaparo and brown to light-brown in A. myersi. Allobates myersi also lacks a pale dorsolateral stripe. A. hodli is largely sympatric to Ameerega picta, a dendrobatid frog that presents similar body size and color pattern. However, A. hodli can be distinguished from Ameerega picta by lacking a bright (orange to red) flash mark on calf region. Description of holotype. Morphological measurements of holotype are presented in Table 1. Body robust, head slightly wider than long (HL/HW = 0.94) (Fig. 3 A). Eye diameter slightly larger than distance from nostril to anterior corner of the eye. Nares located posterolaterally to tip of snout, directed posterolaterally, visible in ventral and anterior view. Center of nostril not visible dorsally. Canthus rostralis convex from tip of snout to nostril, straight from nostril to anterior corner of the eye. Loreal region vertical. Tympanum well visible, with maximum diameter horizontal, corresponding to 44 % the maximum diameter of the eye. Maxillary teeth present. Tongue length twice as large as wide, attached anteriorly on first third. Median lingual process absent. Choanae round. A single vocal sac is present, corresponding to most of the area of the medial and posterior subgular region. Vocal sac round when expanded. When retracted, vocal sac forms two lateral slits at the level of maxilla articulation (Fig. 3, B). Skin granular on dorsum and dorsal surface of legs. Granules round, more developed on dorsal surface of urostyle region and shanks. Skin smooth ventrally and laterally. Dermal flap above cloaca absent. Palmar tubercle slightly triangular. Thenar tubercle well-developed, oval to elliptic, maximum diameter 1.28 times smaller than maximum diameter of palmar tubercle. Subarticular tubercles of Fingers II, III and IV are round, small, never exceeding the width of phalanges. Subarticular tubercle of Finger I elliptic, 1.21 times larger than thenar tubercle in maximum diameter. Supernumerary tubercles absent. Carpal pad and metacarpal ridges absent on hands. No fringes or webbing on fingers. A distal tubercle on finger IV is weakly developed (Fig. 3 C). Finger I is slightly (1.08 times) longer than Finger II. Length of finger IV does not reach distal subarticular tubercle of finger III when fingers are pressed against each other. Relative lengths of fingers: IV Length of shank corresponding to 48 % of snout-to-vent length (Table 1). Tarsal keel is tubercle-like, strongly curved at its proximal end, flattening towards the metatarsal tubercle. Metatarsal fold evident (but not folding over itself) running from the base of Toe V towards metatarsal tubercle, but not reaching it. Preaxial edge of tarsus smooth, with no fringe. Basal webbing present only between Toes III and IV, and II and III. Relative lengths of toes: I Variation in type series. Morphological measurements of individuals constituting type series are presented in Table 1. Morphological characters described for the holotype apply to all individuals in type series, except for the following: Males slightly smaller (4.42 %, in average) than females. Head slightly longer than wide in males (HL/HW = 1.04) and females (HL/HW = 1.05) in average. Maximum diameter of tympanum corresponding to approximately half the maximum diameter of the eye in males and females (Table 1). Vocal sac and slits absent in females. Palmar tubercle round to slightly triangular. A distal tubercle on finger IV is present in 28 of a total 83 (34.1 %) inspected specimens, but is absent or weakly developed in the remaining 54 specimens (65.9 %). Color in life. Males and females do not present dimorphism in relation to color and color pattern. Dorsal surface of body solid black to solid dark-brown (Fig. 2 B). Lateral surface of body solid black. Dorsolateral line white, thinner than lateral line (Fig. 2 A, 2 E). When continuous with flash marks on thighs, dorsolateral line becomes reddish-orange on groin. Lateral line white. Gular region solid black to dark bluish-gray in males and females (Fig. 2 D). In males, vocal sacs usually with a paler bluish-gray color when inflated. Mid abdomen white with irregular black to dark-gray blotches or speckling, merging with solid dark color of gular region. Abdomen bright reddish-orange posteriorly, with dark irregular spots appearing marginally from lateral edges. Ventral surfaces of hind limbs also bright reddish-orange, sometimes with small marginal dark spots (Fig. 2 C, 2 D). Plantar surface of feet brown. Ventral surfaces of arms bright reddish-orange, with bright yellow flash marks extending from dorsal surface of upper arms. Black to dark-gray spot ventrally on upper arm, at the point of body insertion, continuous with gular region pattern. Dorsal surfaces of posterior and anterior limbs reddish to brick-brown (Fig. 2 B, 2 E). Dorsal and rear surfaces of thighs with irregular bright reddish-orange flash marks or patterning, same color as ventral surfaces of legs, with irregular black or darkbrown blotches or spots. Granules on dorsal surface of shanks usually darker than overall color of shanks. A yellow flash mark is present dorsally on upper arms, at the point of body insertion (Fig. 2 B, 2 E). The iris is evident, with metallic yellowish-brown pigmentation. Color in life of juveniles. Color of juveniles after metamorphosis is the same of adults. Dorsum and flanks are solid black to dark-brown, with dorsolateral and lateral lines white and conspicuous. Limbs generally reddish-brown. Bright yellow flash marks are present dorsally on the upper arms, and may reach the elbow. Dorsal surface of thighs with conspicuous longitudinal bright reddish-orange flash marks, lacking black or dark-brown blotches or spots (Fig. 2 F). Color in alcohol of holotype. Dorsum is solid black to dark-brown. A thin, pale white dorsolateral line is present, continuous from groin at hind limb insertion, over the orbit and nostril, to the tip of snout (Fig. 3 A). A pale white lateral line is present, broader than dorsolateral stripe, running from groin, over the insertion of arm, below nostril, to tip of upper lip. Lateral stripe is continuous on both sides of the body. Lateral surface between dorsolateral and lateral stripe solid black. Color of gular region and throat is solid black to darkbrown. Abdomen color is white with irregular black blotches or speckling. Abdomen color becomes solid black/dark-brown from chest towards the gular region. The black/dark-brown speckling over white background pattern is replaced posteriorly by a solid pale-tan pattern, continuous with the ventral color pattern of hind limbs (Fig. 3 B). Arms uniformly very pale-brown in dorsal view, paler on the axilla and carpal/metacarpal regions. Irregular dark blotches appear on dorsal surfaces of tarsus and fingers. Arms uniformly pale white to pale tan in ventral view, with a black patch (continuous with color pattern of gular region) on anterior surface of the arm. Surface of outer lateral edge of forearm and metacarpal region same color as dorsal surface of arms, extending laterally from elbow and reaching the palm of hands and ventral surface of fingers (Fig. 3 C). Legs are pale brown in dorsal view. Irregular pale, unpigmented patches, as well as irregular black blotches and spots are present on dorsal and rear surfaces of thighs (Fig. 3 A). The area immediately around vent is darker than the overall surface of thighs. Dorsal surfaces of shanks with darker granules. Inner dorsal surface of tarsal region is lighter than overall pattern of legs. Toes are generally darker than tarsal region in dorsal view. Ventral surface of legs is uniformly pale-tan with small brown spots appearing marginally from outer edges. Ventral surfaces of tarsal region and toes darker, same color as dorsal surface of legs (Fig. 3 B, 3 D). Tongue is cream-colored; large intestine (removed for the analysis of diet) is unpigmented. Testes are unpigmented. Color variation in type series. Color in alcohol described for the holotype apply to all individuals in type series, except for the following: Lateral stripe is usually continuous, but can be interrupted in some individuals, on one or on both sides of body. Gular region and throat solid black in females, solid black to dark-brown in males. Mature oocytes are pigmented, with black pigment concentrated on animal pole. Description of tadpoles. Tadpole measurements were obtained from four tadpoles in developmental stage 36 (Table 2). Tadpoles correspond to a lot under the same collection number, INPA-H 23693. The largest tadpole (TL = 24.7 mm, Fig. 4) was used for detailed description. Body is depressed, body width (6.0 mm) larger than body depth (4.8 mm), body length 16.1 mm. Snout nearly round, flattened anterodorsally in lateral view (Fig. 4 C). Tip of snout flattened anteriorly in dorsal view (Fig. 4 A). Nares small, directed anterolaterally, located 0.8 mm anterior to the eye, and 1.0 mm posterior to tip of snout. Nostrils narrowly spaced, distance between nostrils 0.9 mm. Eyes dorsal, directed dorsolaterally, 0.9 mm in maximum length, located 1.8 mm posterior to tip of snout. Distance between medial margins of the eyes is 1.4 mm. Spiracle single, sinistral, forming a free tube opening posterodorsally below body axis in lateral view, 5.0 mm posterior from tip of snout (Fig. 4 C). Vent tube medial, free, 0.9 mm in length, opening dextrally. Tail musculature reaches maximum depth (2.4 mm) approximately at the end of first third of tail length, and maximum width at body-tail insertion (2.6 mm). Ventral tail fin originates at body-tail insertion. Dorsal tail fin originates slightly posterior (0.8 mm) to body-tail insertion, and reaches maximum high 14.5 mm from tip of snout, corresponding to the region of maximum tail depth. At maximum depth of tail, depth of musculature is 1.4 mm, dorsal fin 1.5 mm and ventral fin 1.1 mm. Oral disc is positioned anteroventrally, emarginate laterally, transversely elliptical, 2.6 mm in transverse width. Anterior labium continuous with snout, 2.6 mm in length. Marginal papillae absent dorsally on anterior labium (gap 1.7 mm, 74 % of total anterior labium length), present only laterally, on its outer margins. Posterior labium free from body wall, 2.4 mm in length, with a single row of marginal papillae. All papillae with rounded tips (Fig. 5). Labial tooth row formula is 2 (2)/ 3 (1). Rows A- 1 and A- 2 with same length (2.1 mm), A- 2 with a large medial gap (0.6 mm). Rows P- 1, P- 2 and P- 3 with same length (2.0 mm), P- 1 presenting a very narrow medial gap ( Color in preservative is dark to light tan. Body is darker than tail, with scattered brown melanophores in higher densities on anterior dorsum. High concentrations of melanophores also appear posteriorly on dorsum at the top and on flanking regions of tail muscle insertion (Fig. 4 A). Melanophores are evenly distributed on anterior ventral surface of body. Posterior ventral surface of body is transparent, not pigmented, and intestines are clearly visible through skin (Fig. 4 B). Tail musculature is light tan, tail fins transparent, with scattered brown melanophores forming irregular blotches on tail surface (Fig. 4 C). Advertisement and courtship calls description and variation. Advertisement calls of Allobates hodli consist in trills of calls formed by two whistle-like notes with ascending frequency modulation (Fig. 6 A, 6 C). Measurements of advertisement call characteristics of holotype and average values for 60 males from type series are presented on Table 3. The average maximum frequency of calls within type series is 3425.0 ± 184.7 Hz, and average duration of calls (summed durations of first and second notes, and inter-note silent interval) 0.164 ± 0.011 s. First note is less modulated (average difference between lower and higher frequency = 470.7 ± 94.8 Hz) than the second note (average difference between lower and higher frequency = 740.7 ± 115.0 Hz) and shorter in duration (0.033 ± 0.004 s, in comparison to second note, 0.056 ± 0.007 s). Courtship calls of A. hodli are quite distinct from their advertisement calls and are constituted by a continuous pulsed tone (Fig. 6 D), emitted only in the presence of females near the male’s calling perch. Average maximum frequency and duration of courtship calls obtained from calls of four individuals were 3190.2 Hz and 0.571 s, respectively (Table 4). The average pulse emission rate between calls was 125.2 pulses per second. Individuals Molecular phylogeny and genetic distances. From an initial sequence database containing 203 16 S rDNA sequences (including outgroups), a total of 93 unique haplotypes were used in the phylogenetic analysis (Table 5). Phylogenetic reconstructions support the existence of two basal clades within the Allobates femoralis group, both forming the sister clade to Allobates zaparo (Fig. 7 A). One of the basal clades contains Allobates hodli and the second contains samples from areas nearby Allobates femoralis type-locality, which we refer to as Allobates femoralis sensu stricto (clade femo 0 4, Fig. 7 B). A. hodli is marginally paraphyletic to populations that occur in the southern reaches of the Brazilian State of Acre (clade Acre 0 1, Fig. 7 B), which present advertisement calls constituted by four notes and color pattern more similar to that of A. femoralis than to that of A. hodli. Samples from the locality Monte Alegre were not clearly positioned within A. hodli or Acre 0 1 clade. This locality probably corresponds to a relictual contact zone between these clades. Allobates hodli and clade