Allobates albiventris, Souza & Ferrão & Kaefer & Cunha-Machado & Melo-Sampaio & Hanken & Lima, 2023

Souza, Jesus R. D., Ferrao, Miqueias, Kaefer, Igor Luis, Cunha-Machado, Antonio Saulo, Melo-Sampaio, Paulo Roberto, Hanken, James & Lima, Albertina Pimentel, 2023, A new pale-ventered nurse frog (Aromobatidae: Allobates) from southwestern Brazilian Amazonia, Vertebrate Zoology 73, pp. 647-675 : 647

Allobates albiventris sp. nov.

Chresonymy.

Allobates gasconi - Melo-Sampaio et al. (2018), Lima et al. (2020), Gagliardi-Urrutia et al. (2021), Jaramillo et al. (2021), Silva et al. (2022). Allobates gasconi C - Souza et al. (2020). Allobates gasconi SL4 - Ferreira et al. (2023).

Holotype.

INPAH45035 (field number APL21526), an adult male collected by J.R.D. Souza on February 5, 2020, in a forest fragment near BR 364 (08°52 ’27” S, 69°17 ’07” W, 166 m asl), municipality of Manoel Urbano, State of Acre, Brazil.

Paratopotypes.

Nineteen adult specimens collected by J.R.D. Souza and A.P. Lima at the same locality as the holotype: 13 males INPAH45036-40 (field numbers APL21371-75), INPAH45042-47 (field numbers 21479-80, 21511, 21518, 21525 and 21528, respectively) and MPEG44609-10 (field numbers APL21370 and 21380, respectively), and six females INPAH45048-51 (field numbers APL21476, 21481, 21512 and 21527, respectively) and MPEG44611-12 (field numbers APL21478 and 21515, respectively).

Paratypes.

Twenty-three adult specimens collected between 2018 and 2020 by J.R.D. Souza in the State of Acre, and between 2015 and 2016 by P.R. Melo-Sampaio in the States of Acre and Amazonas. ACRE: 10 females MPEG44607 (field number APL21355), INPAH45052-59 (field numbers APL21357, 21523-24 and 21530-34, respectively) and MPEG44613 (field number APL21522) and 7 males INPAH45060-63 (field numbers APL21520-21, 21354 and 21356, respectively), MPEG44608 (field number APL21358), MPEG44606 (field number APL21352) and MNRJ91679 (GenBank KY886578) from Parque Ambiental Chico Mendes (10°02 ’13” S, 67°47 ’36” W, 158 m asl), municipality of Rio Branco; and 2 males INPAH45064-65 (field numbers APL21350-51, respectively) collected near the bank of the Antimary River (09°29 ’16” S, 68°21 ’20” W, 168 m asl.); one female MNRJ91665 (GenBank KY886576) and one male MCP13630 (GenBank KY886577) from the municipality of Feijó (08°14 ’13” S, 70°22 ’44” W, 184 m asl). AMAZONAS: one male MNRJ91683 (GenBank KY886574) and one female MNRJ91684 (GenBank KY886575) from Reserva Extrativista Arapixi (08°58 ’21” S, 67°51 ’50” W, 125 m asl), municipality of Boca do Acre.

Referred specimen.

Brazil: Acre, one male (PRMS0360) collected by P.R. Melo-Sampaio on January 25, 2016, in Reserva Extrativista Arapixi, municipality of Boca do Acre.

Etymology.

The specific epithet Allobates albiventris is a combination of two Latin words, albus (white) and ventris (venter), in reference to the pale ventral coloration of the new species. Vernacular names: pale-ventered nurse frog (English), rana cuidadora de vientre blanco (Spanish), and rãzinha cuidadora de ventre branco (Portuguese).

Generic placement.

The new species is allocated to the genus Allobates based on molecular phylogenetic analysis and phenotypic characters proposed by Grant et al. (2017): paired dorsal digital scutes (character 2), tip of finger IV reaches the distal half of distal subarticular tubercle of finger III (character 5), finger III swollen in adult males (character 21), toe IV with basal webbing and lateral fringe on its preaxial side (characters 43), pale paracloacal marks (character 50) and absence of median lingual process (character 85).

Definition.

Allobates albiventris sp. nov. is characterized by small adult size, SVL 14.3-16.4 mm (n = 22) in males and 15.6-17.8 mm (n = 16) in females. Dorsum smooth with a high concentration of granules in the medium posterior portion. Snout semi-truncated and semi-acuminate in dorsal and lateral views; Allobates canthus rostralis almost straight in dorsal view; loreal region flat; nostrils visible in ventral and lateral views. Tympanum diameter 34-48% of EL. Maxillary teeth present, visible under magnification; median lingual process absent. One subarticular tubercle on finger IV; fingers II and III weakly swollen in adult males; disc on finger II approximately the same width as distal phalanx; width of discs on fingers I, III and IV represent 1.3 ± 0.3, 1.5 ± 0.2 and 1.6 ± 0.2 of width of respective distal phalanges; tip of finger IV reaches the distal subarticular tubercle of finger III; nuptial excrescence on thumb absent; lateral keels present on fingers II-IV; supernumerary tubercles and metacarpal ridge absent; webbing absent between fingers; black gland absent on arm; tarsal keel present, tubercle-like, strongly curved towards the inner metatarsal tubercle; basal webbing present between toes II-IV, less developed between toes II and III; discs on toes II-V moderately expanded; disc on toe I not expanded, approximately the same width of distal phalanx; lateral keels present on all toes. Dorsum light brown with a dark brown band, diamond or hourglass-shaped marks; pale dorsolateral stripe present in preserved specimens, with an irregular upper border extending from the posterior region of the eyelids to the posteromedial region of the body or urostyle; pale ventrolateral stripe absent in preservative, discontinued when present in living specimens; dark brown oblique lateral stripe present, narrower from snout to anterior corner of eye, wider from the posterior corner of the eye to the groin, with an irregular lower border. Paired dorsal digital scutes white. Cream-colored forelimbs with scattered dark brown spots and blotches. Hind limbs light brown; anterior and dorsal portions of the thigh with dark brown spots, dorsal region light brown with scattered spots; a dark brown transverse bar present on thigh of some individuals, usually on tibia; comma-shaped, light brown to orange paracloacal mark. In life, males and females have a white belly and chest without melanophores; throat and vocal sac of males translucent white with scattered melanophores; throat white centrally and posteriorly, translucent laterally and anteriorly in females, with scattered melanophores distributed in the anterior region of the maxilla. Unpigmented intestine. Dark brown mature oocyte; unpigmented testes. Advertisement call with a duration of 42-60 ms and comprising two notes (the first note is shorter than the second), with an inter-note interval of 8-23 ms and dominant frequency of 4,953-6,331 Hz. Exotrophic tadpoles with 2 pyramidal papillae on each end of the anterior labium; 10-13 pyramidal and cylindrical papillae on the posterior labium; LTRF = 2(2)/3(1); gap in row A-2 ≈ 40% of A-1; relative length P-1> P-2> P-3; and P-3 ≈ 65% of P-1.

Diagnosis.

Allobates albiventris sp. nov. differs from other Allobates by the following combination of characters: males in life with a throat and vocal sac translucent white with melanophores uniformly distributed and a white belly; females in life with throat white centrally and posteriorly, translucent laterally and anteriorly, chest and belly white; small adult size, SVL 14.3-16.4 mm (n = 22) in males and 15.6-17.8 mm (n = 16) in females; one subarticular tubercle on finger IV; finger III of adult males weakly swollen; disc of finger II approximately the same width as the distal phalanx; interdigital membranes present between toes II, III and IV; paired digital scutes white; advertisement call with a duration of 42-60 ms and comprising two notes (the first note is smaller than the second), with an inter-note interval of 8-23 ms and dominant frequency of 4,953-6,331 Hz; exotrophic tadpoles with 2 pyramidal papillae on each end of the anterior labium, 10-13 pyramidal and cylindrical papillae on the posterior labium, LTRF = 2(2)/3(1), gap in row A-2 ≈ 40% of A-1, relative length P-1> P-2> P-3, and P-3 ≈ 65% of P-1.

Comparisons.

Characteristics of the compared species are presented within parentheses unless stated otherwise. Males of Allobates albiventris sp. nov. are easily distinguished from those of A. flaviventris , A. fuscellus , A. grillicantus , A. kamilae , A. melanolaemus , A. nidicola , A. ornatus , A. paleci , A. paleovarzensis , A. tapajos , A. tinae , A. trilineatus , A. vanzolinius and A. velocicantus by having a translucent white throat and vocal sac in life (violaceous to gray in A. flaviventris , A. pacaas and A. paleovarzensis ; yellow in A. grillicantus , A. kamilae , A. paleci , A. tapajos and A. tinae ; gray to black in A. fuscellus , A. melanolaemus , A. nidicola , A. trilineatus and A. vanzolinius ; gray in A. ornatus ; whitish centrally and yellow laterally in A. velocicantus ). Additionally, A. albiventris sp. nov. differs from A. pacaas by having only one subarticular tubercle on finger IV (two tubercles); from A. tapajos by the presence of melanophores on the vocal sac of males (absent); from A. flaviventris , A. nidicola , A. paleovarzensis and A. vanzolinius by having a maximum SVL of 16.4 mm in males (minimum SVL 16.7 mm in A. flaviventris , 18.5 mm in A. nidicola , 18.3 mm in A. paleovarzensis and 21.5 mm in A. vanzolinius ).

Males of Allobates caeruleodactylus , A. conspicuus , A. grillisimilis , A. subfolionidificans and A. sieggreenae have a throat and vocal sac coloration similar to A. albiventris sp. nov. However, A. albiventris sp. nov. differs from these species by the presence of dark marks or a dark brown, wide longitudinal band on the dorsum (uniform light brown dorsum in all mentioned species). In addition, A. albiventris sp. nov. differs from A. caeruleodactylus by having white digital scutes in life (blue); from A. conspicuus and A. sieggreenae by the absence of a continuous ventrolateral stripe (ventrolateral stripe present); from A. grillisimilis by having regularly distributed melanophores on the throat, vocal sac and chest (melanophores, when present, only on the jaw); and from A. subfolionidificans by having a dorsolateral stripe (absent) and females in life with a white chest and belly (yellow).

Although A. albiventris sp. nov. has been confused with A. gasconi , they are easily distinguished by the coloration of breeding adults. Males of the new species are easily distinguished from those of A. gasconi sensu stricto by the translucent white throat and vocal sac (gray to dark gray; Fig. 5 ), white chest (translucent to pinkish grey) and white belly without melanophores (belly pinkish grey anteriorly, whitish grey centrally, light or translucent grey with white and brown small blotches laterally, and yellowish or translucent grey posteriorly; Ferreira et al. 2023; present study). Female A. albiventris sp. nov. have a white throat centrally and posteriorly but translucent laterally and anteriorly (light to bright yellow), a white chest (bright to whitish yellow) and a white belly (belly yellowish to whitish cream). Moreover, finger III of adult males is only slightly swollen (moderately to highly swollen; Ferreira et al. 2023; present study).

The advertisement calls of Allobates albiventris sp. nov. differ from A. gasconi sensu stricto by a call duration of 50 ± 4 ms (94 ± 33 ms), exclusively composed of 2 notes (2-4 notes, mainly 3 notes) with the first note always shorter than the second (notes with similar duration) and an inter-note interval of 16 ± 4 ms (30 ± 4 ms; Ferreira et al. 2023). Calls of A. albiventris sp. nov. and A. trilineatus are similar: both are composed of two notes and are arranged in call series. However, the former species differs from A. trilineatus by having a call duration of 42-60 ms (60-80 ms) and the first note always shorter and with a lower dominant frequency than the second one (similar duration and dominant frequency in both notes; Jaramillo et al. 2021). Calls of A. albiventris sp. nov. have two notes exclusively, which differs from A. caeruleodactylus , A. melanolaemus , A. nidicola , A. paleovarzensis , A. sieggreenae , A. subfolionidificans , A. tapajos and A. tinae (calls composed of one note in each species). Moreover, calls of A. albiventris sp. nov. are commonly arranged in call series (single calls emitted regularly through time in A. caeruleodactylus , A. nidicola and A. subfolionidificans ) with a call duration of 42-60 ms (151-507 ms in A. grillicantus ; 122-305 ms in A. grillisimilis ; 180-340 ms in A. paleci ; and 1,870-2,890 ms in A. velocicantus ) and are composed exclusively of two notes (3-15 notes in A. grillicantus and A. grillisimilis ; 16-33 ms in A. paleci ; and 66-138 in A. velocicantus ). As in A. albiventris sp. nov., regular calls of A. flaviventris are composed of two notes, but in the former species calls are emitted with a dominant frequency of 4,953-6,331 Hz (3,618-4,651 Hz in A. flaviventris ). The advertisement calls of A. conspicuus , A. fuscellus , A. ornatus , A. pacaas and A. vanzolinius are unknown.

Tadpoles of Allobates albiventris sp. nov. easily differ from those of A. gasconi sensu stricto by having a LTRF = 2(2)/3(1) and a tail highly pigmented with brown spots of various shapes and sizes resembling a marbled pattern (LTRF = 2(2)/2(1) and a tail poorly pigmented with brown spots; Ferreira et al. 2023); from those of A. nidicola by being exotrophic and having a spiracle (endotrophic, spiracle absent); from A. subfolionidificans and A. tapajos by having two pyramidal papillae on each side of the anterior labium (six in A. subfolionidificans ; four or five in A. tapajos ); from A. velocicantus by having pyramidal and cylindrical papillae on the posterior labium (only pyramidal in A. velocicantus ); from A. grillicantus by having LTRF = 2(2)/3(1) [LTRF = 2(2)/3 in A. grillicantus ]; from A. grillisimilis and A. paleovarzensis by having LTRF = P-1> P-2> P-3 (P-3 = P-2 = P-1 in A. grillisimilis ; P-2> P-1> P-3 in A. paleovarzensis ); from A. caeruleodactylus by the gap in row A-2 ≈ 40% of A-1 and P-3 ≈ 65% of P-1 (A-2 gap ≈ 58% of A-1 and P-3 ≈ 37% of P-1 in A. caeruleodactylus ). Tadpoles of A. conspicuus , A. flaviventris , A. fuscellus , A. melanolaemus , A. ornatus , A. pacaas , A. tinae , A. sieggreenae , A. trilineatus and A. vanzolinius are unknown.

Description of the holotype.

Adult male, INPAH45035 (Figs 4A-C ; 6A, C ; 8A-C ; Table 3 ). Snout-vent length 14.6 mm. Head wider than long (HW/HL = 1.04); HW equals 35% of SVL and HL equals 33% of SVL. Eye diameter exceeds distance from eye to nostril (EL/END = 1.33); EL equals 43% of HL. Interorbital region flat; IOD equals 88% of HW. Tympanum rounded, visible to the naked eye. Snout slightly rounded in dorsal and lateral view. Inter-nostril region flat; nostrils rounded, laterally positioned and visible in lateral and ventral view; IND equals 49% of IOD. Canthus rostralis straight in dorsal view; loreal region flat. Maxillary teeth present. Median lingual process absent. Vocal sac single, subgular. Lateral folds of vocal sac present at the level of angle of maxilla.

Palmar tubercle rounded and conspicuous, diameter 0.42 mm. Thenar tubercle elliptical and conspicuous, width 0.29 mm. Diameter of thenar tubercle equals 69% of that of the palmar tubercle. Subarticular tubercles protruding, oval on finger I and rounded in other fingers; two tubercles on finger III but one in each of the others; distal tubercle smaller than proximal tubercle on finger III; tubercle on finger I larger than others. Supernumerary tubercles absent. Lateral keels on fingers I-IV, poorly defined on finger I. When placed side by side, the tip of finger IV reaches the distal subarticular tubercle of finger III. Preaxial phalangeal swelling on finger II and III. Relative length of fingers: IV <II <I <III. Discs are wider than the third phalanx on fingers I, III and IV, but approximately the same width on finger II. Paired dorsal digital scutes present.

Tibia and thigh lengths approximately the same (TIL/THL = 1.01), equal 49% and 48% of SVL, respectively. Foot length 97% of tibia length. Tarsal keel conspicuous and curved, narrowing towards the internal metatarsal tubercle. Internal metatarsal tubercle protuberant, elliptical. External metatarsal tubercle small and round, protruding, smaller than diameter of internal metatarsal tubercle. Metatarsal fold absent. Lateral keels present on preaxial and postaxial sides of each toe. Basal webbing between toes II and IV. Subarticular tubercles rounded and evident; one each on toes I and II but two each on toes III-V. Discs rounded, wider than distal phalanx on toes II, III and IV but of similar width on toe I; disc of toe V with smaller expansion compared to toes II-IV. Paired dorsal digital scutes present.

Dorsal skin smooth with small flattened and barely visible tubercles, mostly on the posterior portion; skin on arms smooth; skin on legs smooth with small tubercles. Ventral surface of body, arms and legs smooth.

In preservative (Fig. 4A-C ), dorsal surface of body and limbs light brown; numerous dark brown melanophores form a longitudinal band, which is slightly constrained behind the eyes and diffuse towards the cloaca (Fig. 4A ). A narrow and cream-colored dorsolateral stripe with an irregular upper border extends from posterior region of eyelids to mid-posterior region of body (Fig. 4B ). Lateral stripe dark brown; darkest from the tip of the snout to the region above the axilla; lower border regular on snout but irregular in ventrolateral region of body (Fig. 4B ). Paler oblique stripe diffuse, extends from the inguinal region to the axilla. Ventrolateral stripe absent. Ventrolateral region beige; melanophores form small dark brown irregular spots. Transverse dark brown bar on thigh and tibia is widest on tibia (Fig. 4A ). Anterior region of thigh light brown, posterior region dark brown; paracloacal marks cream, conspicuous. Chest, throat and vocal sac cream with small dark brown melanophores; belly cream, lacks melanophores or dark spots. Ventral surface of arms beige with scarce brown melanophores; light brown on forearms. Mid-ventral surface of thigh and tibia cream, without melanophores; ventrolateral surface with irregular dark brown spots (Fig. 4C ). Palmar and plantar surfaces dark brown (Figs 4C , 5A, C ). Tongue longer than wide, with anterior third attached to the floor of the mouth, cream-colored (Fig. 4B ).

Coloration in life is similar to that in preservative. Dark marks, spots, stripes, lines and bars are more conspicuous. Background coloration of the dorsum cream. Ventrolateral stripe discontinuous from the posterior corner of the eye to the axilla; small iridescent dots and spots visible below the dark brown band (Fig. 8A-C ). Iris metallic bronze, pupil black. Ventral surface of arms and legs varies between light gray and rosaceous gray. Throat and vocal sac translucent white; chest and belly white. Paired digital dorsal scutes white.

Variation in the type series.

Variation in morphometric measurements of Allobates albiventris sp. nov. is summarized in Table 3 . Sexual dimorphism is present in SVL and 12 body ratios. Females are larger than males (SVL; S2 = 10.3, F = 50.48, df = 36, adj p = 0.0002) but smaller in EN (S2 = 0.0006, F = 8.46, df = 33, adj p = 0.0152), THL (S2 = 0.0028, F = 20.94, df = 33, adj p = 0.0004), TIL (S2 = 0.0073, F = 11.64, df = 36, adj p = 0.0062), FL (S2 = 0.0025, F = 8.31, df = 36, adj p = 0.0152), UAL (S2 = 0.0010, F = 7.55, df = 36, adj p = 0.0195), FAL (S2 = 0.0006, F = 6.58, df = 33, adj p = 0.0266), HANDI (S2 = 0.0005, F = 8.87, df = 36, adj p = 0.0148), HANDII (S2 = 0.0004, F = 9.33, df = 36, adj p = 0.0139), HANDIV (S2 = 0.0005, F = 7.09, df = 36, adj p = 0.0220), WPF (S2 = 0.00003, F = 42.28, df = 27, adj p <.0001), WTT (S2 = 0.00002, F = 38.79, df = 27, adj p <.0001) and EL (S2 = 0.0003, F = 13.55, df = 36, adj p = 0.0035).

Unlike the holotype, a third subarticular tubercle is present on the proximal portion of toe IV in 53% of the rest of the type series (12 males and 8 females). When present, it is approximately half the size of other subarticular tubercles on the same toe (Fig. 7G, H ).

In preservative, dorsal coloration of the type series ranges from light to dark brown (Fig. 7 ). Dark hourglass-like markings are present in 45% of males (n = 10) and 44% of females (n = 7) and are more noticeable in individuals with lighter background coloration (e.g., Fig. 7B, C ). In the other specimens, a light-to-dark-brown band extends down the center of the dorsum from the interorbital region to the urostyle. The light dorsolateral line is present in all males and females. However, its variable thickness is more evident in specimens lacking hourglass markings (Fig. 7E ). Conspicuous dark transverse bars on the tibia, which are barely visible or absent on the thigh, are present in 71% of specimens (12 males and 15 females). Both males and females lack visible melanophores on the belly (Fig. 7D, F ) but the sexes differ with respect to the presence and concentration of melanophores on the chest and throat; melanophores are present on the chest in 72% of males (n = 16) but only 31% of females (n = 5). Although melanophores are present on the throat of all individuals, females have fewer of them and they are distributed mainly in the anterior and peripheral region of the throat, while males have more, evenly distributed, melanophores.

As in the holotype, coloration in life is similar to that in preservative (Fig. 7 ). The lateral brown stripe is darkest from the tip of the snout to the region above the axilla, becoming lighter and more diffuse as it extends to the inguinal region (Fig. 8A, E, H ).

Advertisement call.

The advertisement call of Allobates albiventris sp. nov. is formed by a pair of notes that is emitted singly or in a series of as many as 16 calls. Calls emitted in series of one, two, three, four or five calls correspond to 88% of recorded call arrangements (Fig. 9A-E ). Calls have an average duration of 50 ± 4 ms (42-60 ms). The first note of each call is always shorter (13 ± 2 ms; 8-20 ms) than the second one (20 ± 2 ms; 14-26 ms) (Fig. 10B ), and the inter-note interval ranges from 8 to 23 ms (16 ± 4 ms). Call series with two calls have a duration of 220-610 ms (320 ± 70 ms), while series with three, four or five calls have a duration of 370-1,030 ms (600 ± 110 ms), 580-1,420 ms (950 ± 170 ms) and 790-1,700 ms (1,260 ± 200 ms), respectively. The inter-call interval within call series is 130-390 ms (210 ± 50 ms); the interval between call series is 410-4,400 ms (1,010 ± 670 ms). Notes have modulated frequencies, ascending from beginning to end (Fig. 10B-E ). The first note has a slightly lower dominant frequency (5,409 ± 211 Hz; 4,952-5,857 Hz) than the second note (5,849 ± 250 Hz; 5,189-6,331 Hz). Lower and upper frequency values are presented in Table 4 .

Eggs and larvae.

Descriptions of quantitative characters of tadpoles are based on six specimens at Gosner stage 34. Morphometric measurements are presented in Table 5 . Body ovoid in dorsal view, ellipsoid in lateral view (Fig. 10A-C ). Body length (BL) 31-33% of total length (TL) and tail length 67-69% of TL; body wider than tall (BH 50-65% of BW) and longer than wide (BW 61-80% of BL); HWLE 72-93% of BW; snout rounded in dorsal and lateral view; END 60-78% of ED; eyes directed dorsally and laterally; IOD 26-33% of HWLE. Nostrils located dorsolaterally and directed anterolaterally, visible in dorsal and lateral view; inter-nostril distance 38-44% of HWLE. Fleshy ring present on inner margin of nostrils, round, not ornamented. Spiracle single, sinistral, tubular, 0.46-0.67 mm long; it is attached laterally, a little below half body length and just dorsal to the intestine. Gut coiled. Vent tube dextral, 1.23-1.60 mm long. Dorsal fin arises around 2 mm from the junction of tail with body, shallow edge anteriorly, maximum height at mid posterior region of tail (Fig. 10B ). Dorsal fin higher than ventral fin. Tail tip acuminate, not flagellated. Maximum tail height 2.44-2.69 mm. Width of tail musculature 35-50% of body width; height of tail musculature 59-77% of body height.

Oral disc positioned anteroventrally, laterally emarginate, oval in ventral view (Fig. 10B, C ), 1.44-1.93 mm wide, and corresponding to 37-49% of body width at height of spiracle. Anterior labium with four short pyramidal papillae distributed in a single row and two papillae at each end of the labium (Fig. 10D, E ). Posterior labium with a single row of 10-13 papillae, of which one or two are pyramidal at each end and the rest are cylindrical. Cylindrical papillae vary in size along the labium, being shorter at the ends and medially (Fig. 10D, E ). Submarginal papillae absent. Upper jaw sheath arch-shaped, longer than lower jaw sheath and without median cut. Lower jaw V-shaped. Sheaths with serrations along their entire length. Labial formula of the keratodont row (LTRF) is 2(2)/3(1). Row A-1 measures 1.16 ± 0.05 mm; A-2 measures 1.07 ± 0.04 mm but is interrupted in the central region by a gap of approximately 40%. Row P-1 measures 1.02 ± 0.11 mm, with a small medial gap. Rows P-2 and P-3 are complete; they measure 0.98 ± 0.08 mm and 0.67 ± 0.14 mm, respectively (Fig. 10D ).

In preservative, body and tail muscles assume different shades of cream, with brown melanophores forming blotches and spots of various shapes and sizes. Fins cream but translucent, with brown spots of various shapes and sizes resembling a marbled pattern. Venter cream but translucent, with thickened brown melanophores mainly in the central region. Internal organs are visible through the skin (Fig. 10C ).

Geographic distribution and natural history.

Allobates albiventris sp. nov. is known from only five localities in southwestern Brazilian Amazonia: four in the State of Acre and one in the State of Amazonas (Figs 1 and 11 ). The species inhabits the leaf litter of primary and secondary ombrophilous forests at elevations between 125 and 184 m asl (Fig. 11 ). It has a diurnal habit and is generally active between 0500 and 1800 h, with vocal activity peaks between 0500-0900 h and 1600-1800 h.

Allobates albiventris sp. nov. breeds in the rainy season between November and March. Males vocalize both on litterfall and while perched on shrubs or fallen branches up to 40 cm above ground (Fig. 8M ). Clutches are deposited on the adaxial portion of living, attached leaves of small shrubs approximately 10-15 cm from the ground (Fig. 12F-H ). We found eight egg clutches-three at the type locality (Manoel Urbano, Acre), four in Parque Ambiental Chico Mendes (Rio Branco, Acre) and one in Reserva Extrativista Arapixi (Boca do Acre, Amazonas). The number of eggs per clutch ranged from 17 to 31 (Fig. 12F, G ). Two clutches were found on the same leaf (nest) (Fig. 12H ). In freshly laid eggs, approximately half of the animal pole is darkly pigmented; the rest of the egg is white. The eggs are surrounded by an opaque, colloidal gel (Fig. 12F, G ), which becomes denser and more opaque over the course of larval development.

Four mating pairs were observed in courtship, one at the type locality and three in Parque Ambiental Chico Mendes. Each observation began with the approach of a female to the perch where a male was emitting courtship calls. In each case, the male, perceiving the approach of a female, began to emit courtship calls interspersed with advertisement calls. He then jumped from the call perch and attempted to guide the female (Fig. 12B ) by conducting her to an oviposition site (bushes or seedlings) located up to 3 m from the perch. During the courtship march (sensu Rocha et al. 2018), which lasted between 3 and 5 min, the male continued to emit advertisement and courtship calls while the female sporadically made short stops. Once arriving at the oviposition site, the male jumped to the adaxial surface of the leaf, located 10-15 cm from the ground, and continued vocalizing. The female followed the male and positioned herself underneath the leaf, at the edge closest to the ground. She then observed the male, raising her head toward the leaf. In all courtships, females positioned themselves vertically, with forelimbs only lightly touching the ground, for up to 1 min before jumping to the leaf (Fig. 12C ). After the jump, the female approached the male. On one occasion, the female faced the male and put her snout on the male’s pectoral region, then turned in the opposite direction. The male then climbed onto the female’s back and they initiated amplexus (it was not possible to clearly discern the type of amplexus). In the other courtships, the female approached the male and quickly was grabbed by him. The male positioned himself laterally, snout to snout, and with one hand held the female’s head, either by the region between the eyes and nostrils or directly on the snout (Fig. 12D ). The resulting cephalic amplexus lasted from 1 to 4 min. During and after amplexus, a barely audible vocalization (similar to “cheeps”), was emitted by the male. Following amplexus, on one occasion the male quickly jumped into the leaf litter and returned to vocalize within 3 min. In the three other courtships, the male remained on the leaf while the female deposited eggs (Fig. 12E, H ) but left the leaf before she finished. Two males initiated advertisement calls while the female was still ovipositing (Fig. 12H ), while the third left the nest without vocalizing. On two occasions oviposition started with the male still in amplexus.

During oviposition, females repeatedly moved their heads upwards. This movement was interspersed with continuous clockwise or counterclockwise rotations relative to the vertical plane. Oviposition lasted ~11 to 15 min and ended when the female stopped the tilting motion with her head. However, she remained at the nest, on the clutch, and performed sporadic returns (apparently, hydrating the clutch, as her skin became excessively moist). Residence time of each female after oviposition ranged from 10 to 15 min, and the total time in the nest from 21 to 30 min. Males returned to the nest between 25 and 30 min after the female left, probably to hydrate the eggs and promote swelling of the surrounding jelly. We collected one clutch immediately after the female’s departure, prior to the male’s return, and the embryos developed normally. Only one male was observed performing larval transport (Fig. 12I ).

Figures

Figure 1. Geographic distribution of the new species (yellow symbols): Type locality = star (1 Manoel Urbano), paratype localities = circles (2 Antimary River; 3 Parque Ambiental Chico Mendes) and additional localities = rhombus (4, Feijo; 5, Reserva Extrativista Arapixi). Type localities of other Allobates to which it is compared (squares): 6 A. subfolionidificans; 7 A. flaviventris; 8 A. tinae; 9 A. gasconi (red square); 10 A. vanzolinius; 11 A. fuscellus; 12 A. velocicantus; 13 A. conspicuus; 14 A. ornatus; 15 A. trilineatus; 16 A. sieggreenae; 17 A. melanolaemus; 18 A. caeruleodactylus; 19 A. nidicola; 20 A. paleovarzensis; 21 A. grillisimilis; 22 A. tapajos; 23 A. grillicantus; 24 A. pacaas; 25 A. paleci; 26 A. kamilae. Abbreviations: BOL, Bolivia; COL, Colombia; ECU, Ecuador; PER, Peru.

Figure 4. Dorsal, dorsolateral and ventral views of the male holotype INPAH 45035 (A - C) and a female paratype INPAH 45051 (D - F) of Allobates albiventris sp. nov. Scale bar: 5 mm. Photographs by J. R. D. Souza.

Figure 5. Coloration of the vocal sac and throat of Allobates albiventris sp. nov. (A, B) and A. gasconi sensu stricto (C, D). Photographs by J. R. D. Souza (A, B) and A. P. Lima (C, D).

Figure 6. Ventral view of the hand (A, B) and foot (C, D) of Allobates albiventris sp. nov. (A, C) Male holotype INPAH 45035. (B, D) Female paratype INPAH 45051. Scale bar: 0.5 mm (A, B) and 1 mm (C, D). Photographs by J. R. D. Souza.

Figure 7. Paratypes of Allobates albiventris sp. nov. A Female, MPEG 44612, SVL 16.2 mm. B Male, INPAH 45038, SVL 14.7 mm. C, F Female, INPAH 45054, SVL 17.0 mm. D Male, INPAH 45060, SVL 15.6 mm. E Male, INPAH 45046, SVL 14.9 mm. G, H Male, INPAH 45064, SVL 16.4 mm. White rectangle in (G) delimits the magnified region (H) illustrating the third tubercle on toe IV (arrow). Photographs by J. R. D. Souza.

Figure 8. Coloration in life of Allobates albiventris sp. nov. from Manoel Urbano and Rio Branco, State of Acre, Brazil. A - C Male holotype, SVL 14.6 mm; D - F Female, INPAH 45051, SVL 16.8 mm; G - I Male, MNRJ 91679, SVL 16.0 mm; J - L Female, MPEG 44613, SVL 16.0 mm; M Male, uncollected; N Male, INPAH 45044, SVL 15.3 mm; O Male, uncollected. Photographs by J. R. D. Souza (A-F, J-O) and P. R. Melo-Sampaio (G-I).

Figure 9. Advertisement calls of the holotype of Allobates albiventris sp. nov. (INPAH 45035, FNJV 53687). A Oscillogram showing the continuous emission of calls with variable arrangements. Spectrograms and oscillograms of the four most common call arrangements: single call (B) and series of two (C), three (D) and four calls (D). Note that each call is composed of two notes. Air temperature: 22 ° C. Abbreviations: dB, decibels; kHz, kilohertz; s, seconds.

Figure 10. Preserved tadpole of Allobates albiventris sp. nov. (lot INPAH 45066), Gosner stage 34. (A) Dorsal, (B) lateral and (C) ventrolateral views of the body, and (D) ventral and (E) ventrolateral views of the oral disc. Scale bar: 10 mm (A - C) and 1 mm (D, E). Photographs by J. R. D. Souza.

Figure 11. Geographic distribution of Allobates albiventris sp. nov. Star = type locality (1 Manoel Urbano); circles = additional paratype localities (2 Antimary River; 3 Parque Ambiental Chico Mendes); and rhombus (4 Feijo; 5 Reserva Extrativista Arapixi). White triangles denote sampled localities where the new species was not recorded.

Figure 12. Habitat and natural history of Allobates albiventris sp. nov. A Typical understory of open ombrophilous forest at the type locality in Manoel Urbano, State of Acre, Brazil. B Beginning of courtship behavior, in which a male is leading a female to an oviposition site. C Female (unvouchered) positioning herself to jump to the adaxial surface of the leaf, where the male is vocalizing. D Mating pair (unvouchered) in cephalic amplexus. E Mating pair (unvouchered) on the leaf, with the female in oviposition and the male silent. F Recently deposited clutch, with the smallest clutch recorded (17 eggs). G The largest clutch recorded (31 eggs). H Mating pair on a leaf, where a male vocalizes while a female deposits a second clutch on the same leaf. I Male INPAH 45045 carrying 10 tadpoles on his back. Photographs by J. R. D. Souza.