Adenomera cotuba, Carvalho, Thiago Ribeiro De & Giaretta, Ariovaldo Antonio, 2013

Carvalho, Thiago Ribeiro De & Giaretta, Ariovaldo Antonio, 2013, Bioacoustics reveals two new syntopic species of Adenomera Steindachner (Anura: Leptodactylidae: Leptodactylinae) in the Cerrado of central Brazil, Zootaxa 3731 (3), pp. 533-551 : 535-542

Adenomera cotuba , new species

Figures 1–3

Holotype. AAG-UFU 1400, adult male, collected in the Municipality of Teresina de Goiás (13°52'S, 47°15'W; approximately 840 m a.s.l.), northern State of Goiás, central Brazil, on 16–17 November 2012, by T. R. de Carvalho, B. F. V. Teixeira, and L. B. Martins.

Paratopotypes. Eight adult males: AAG-UFU 0 808, on 18 November 2011, by A. A. Giaretta and K. G. Facure; AAG-UFU 1397–1399, 1401–1404, collected with the holotype.

Diagnosis. Adenomera cotuba sp. nov. is assigned to the genus ( L. marmoratus species group and Adenomera genus definitions; sensu Heyer 1973, 1974a, respectively) by the following set of characters: 1) small body size (up to 34.1 mm; sensu Kok et al. 2007); 2) toes lacking fringing or webbing; 3) adult males lacking thumb spines; 4) first and second fingers of approximately equal length. The new species is diagnosed from the other 16 congeneric species by the following combination of characters: 1) small size (adult male SVL 18.6–20.5 mm; Table 1 ) and very robust body; 2) dorsum glandular/granular with no distinctive dorsal granular rows or dorsolateral folds; 3) black or very dark dorsal coloration with no distinctive color patterns; 4) toe tips not developed into flattened disks; 5) distal antebrachial tubercle present; 6) advertisement call consisting of a well-defined series of pulsed calls (7– 32 calls/series; Table 2) with progressive increment in amplitude in the first third of each call series when it reaches a sustained plateau.

Comparisons with other species. Adenomera cotuba sp. nov. (adult male SVL 18.6–20.5 mm; Table 1 ) can be diagnosed from A. andreae (mean adult SVL 23.3 mm, maximum 27.0; Heyer 1973), A. coca (adult male SVL 23.6–25.6 mm; Angulo & Reichle 2008), A. diptyx (mean adult SVL 22 mm; Boettger 1885), A. engelsi (adult male SVL 20.9–22.7 mm; Kwet et al. 2009), A. heyeri (adult male SVL 22.5–25.8 mm; Boistel et al. 2006), A. hylaedactyla (adult male SVL 22.2–24.3 mm; Angulo et al. 2003), A. lutzi (adult male SVL 25.7–33.5 mm; Kok et al. 2007), A. marmorata (mean adult SVL 20.8 mm, maximum 26.0; Heyer 1973), A. martinezi (adult male SVL 21.9–24.2 mm; Carvalho & Giaretta 2013), A. simonstuarti (adult male SVL 25.9–26.2 mm; Angulo & Icochea 2010) by its smaller body size. Adenomera cotuba sp. nov. has a more robust body in dorsal view compared to all the additional material examined by us (figs. 1–2; see Appendix 1). Adenomera cotuba sp. nov. possesses a glandular/granular dorsum with no distinctive dorsal rows or dorsolateral folds (figs. 1–2), whereas A. araucaria , A. hylaedactyla , A. heyeri , A. martinezi , and A. saci possess dorsolateral folds or distinctive granular/glandular rows (Kwet & Angulo 2002; Angulo et al. 2003; Boistel et al. 2006; Carvalho & Giaretta). Adenomera cotuba sp. nov. has a black or very dark-colored dorsum with no distinctive color patterns, whereas A. araucaria usually has longitudinally arranged dark marks (Kwet & Angulo 2002); A. engelsi has a maculated dorsal pattern, consisting of variably sized, longitudinally arranged spots and a distinctive triangle in the orbital region, followed by a chevronlike blotch forming an hourglass-shaped figure (Kwet et al. 2009); A. martinezi and A. saci have distinctive longitudinal rows of symmetrically arranged black spots (Bokermann 1956; Carvalho & Giaretta 2013); A. nana usually has a symmetrical pattern of dark marks on an orange-brown background (Kwet 2007); A. thomei has a mask-like pattern on the inverted triangle of the interorbital region (Almeida & Angulo 2006). The new species has no vertebral pin-stripe, whereas individuals of A. araucaria , A. coca , A. diptyx , A. hylaedactyla , A. martinezi and A.

saci always, usually, or sometimes do (Heyer 1973; De la Riva 1996; Kwet & Angulo 2002; Angulo & Reichle 2008; Carvalho & Giaretta 2013). Adenomera cotuba sp. nov. has its toe tips unflattened, whereas A. andreae , A. marmorata , and A. nana have toe tips developed into flattened disks (Heyer 1973; Kwet 2007). The new species can be diagnosed from all congeners (except A. lutzi ; see Kok et al. 2007) by the presence of a single or a few variably-sized distal antebrachial tubercles.

* SVL was measured from all three specimens of A. juikitam sp. nov. type series; see Material and Methods section.

Additional morphological and color pattern features that can also diagnose Adenomera cotuba sp. nov. from congeners (comparative species with features in parentheses): from A. ajurauna , by the absence of dark brown throat, and little white dots on upper and lower lips, and dorsal surface of arms (Berneck et al. 2008); from A. araucaria , by having white-tipped granules on dorsal surface of shanks (dorsal surface of shanks smooth; Kwet & Angulo 2002); from A. heyeri , by possessing profuse tubercles on the sole of feet (smooth sole of feet with scant small tubercles), and the absence of yellow throat and belly in male specimens (Boistel et al. 2006); from A. lutzi , by the lack of a distinctive yellow, orange or red spotted/mottled pattern on posterior surface of thighs on a black background, and yellow to orangish yellow ventral surfaces in male specimens (Kok et al. 2007); from A. martinezi and A. saci (Carvalho & Giaretta 2013) , by possessing a very robust body in dorsal view (slender body in A. martinezi and A. saci ); from A. simonstuarti , by the absence of very dark, nearly solid stripes on undersides of arms, extending from wrist to the arm insertion (Angulo & Icochea 2010).

The advertisement call (fig. 4; Tables 2, 4) distinguishes Adenomera cotuba sp. nov. from all congeners by consisting of a well-defined series of pulsed calls with progressive increment in amplitude in the first third of each call series when it reaches a sustained plateau. The new species can additionally be diagnosed from A. ajurauna , A. bokermanni , A. engelsi , A. heyeri , A. lutzi , A. marmorata , A. nana , and A. saci by possessing a pulsed call structure (non-pulsed structure in all aforementioned species; see Table 4); from A. andreae , A. hylaedactyla , and A. simonstuarti (combined range 2–7 pulses/call; Table 4) by a greater number of pulses (8–14 pulses/call; Tables 2, 4), and from A. martinezi (15–21 pulses/call; Table 4) by a fewer number of pulses (8–14 pulses/call; Tables 2, 4); from A. andreae , A. hylaedactyla , and A. lutzi (combined range 16–64 ms; Table 4) by a longer call duration (69– 191 ms; Tables 2, 4); from A. andreae , A. diptyx , A. hylaedactyla , A. martinezi , A. nana , and A. thomei (1st harmonic peak frequency combined range 1.88–3.05 kHz; Table 4), and A. andreae , A. araucaria , A. diptyx , A. hylaedactyla , A. marmorata , A. nana , and A. thomei (2nd harmonic peak frequency combined range 3.96–5.60 kHz; Table 4) by its lower frequencies (1st harmonic peak frequency 1.73–1.83 kHz, 2nd harmonic peak frequency 3.33– 3.80 kHz; Tables 2, 4).

Description of holotype. AAG-UFU 1400 (figs. 1–3). Adult male. Body very robust in dorsal view. Snout rounded in dorsal view (fig. 3B), acuminate in lateral view (fig. 3A), head longer than wide. Nostrils closer to the snout tip than to the eyes; canthus rostralis indistinguishable; loreal region slightly concave; supratympanic fold developed; discrete, ovoid post-commissural gland; upper eyelids glandular; vocal sac subgular with a fold from jaw to forearm on each side, vocal slits present; vomerine teeth in two straight rows posterior to choanae. Tongue ovoid, free behind. Relative finger lengths IV <I ~ II <III; fingers with no webbing or fringing; finger tips rounded, slightly expanded; inner metacarpal tubercle ovoid; outer metacarpal tubercle nearly rounded (fig. 3D). Subarticular and supernumerary tubercles rounded. No thumb asperities or prepollex. Undersides of forearms bearing a few variably-sized distal antebrachial tubercles. Dorsum glandular/granular. Posterior half of dorsum, dorsal surface of shanks, and dorsal and outer surfaces of tarsi with profuse minute granules. Vertebral pin-stripe absent. Posterior half of flanks with granular rows. Throat and belly smooth. Ventral surface of thighs areolate. Posterior surface of thighs with no distinctive pattern, possessing distinctive nearly rounded glands on each side of cloaca. Relative toe lengths I <II <V <III <IV; toe tips rounded, slightly expanded (toe tip character state B; see fig. 1B in Heyer 1973), without webbing, ridged laterally. Inner metatarsal tubercle ovoid, outer rounded (fig. 3C). Tarsal fold from the inner metatarsal tubercle extending 1/3 length of tarsi, distal portion barely enlarged. Subarticular tubercles conical, supernumerary rounded.

Measurements of holotype. Morphometric characters (mm) and ratios (%) in relation to SVL (20.5 mm): HL 7.8 (38.0), HW 6.9 (33.7), ED 2.1 (10.2), TD 1.2 (5.9), END 1.5 (7.3), IND 1.7 (8.3), FRL 4.8 (23.4), HAL 5.0 (24.4), TL 8.6 (42.0), SL 8.6 (42.0), TSL 5.9 (28.8), FL 9.5 (46.3).

Coloration of holotype in alcohol (figs. 2A–B). Snout tip with a faded white coloration. Dorsum and flanks black with dark-colored blotches indistinguishable. Dorsal surface of limbs with dark brown stripes/blotches on a slightly lighter brown background. White-tipped granules scattered on the posterior half of dorsum, dorsal surface of shanks, and outer surface of tarsi. Larger scant pale orange granules on posterior half of body. Posterior half of flanks with orange-colored granular rows towards inguinal region. Upper and lower jaws covered with whitecolored spots/blotches, white commissural gland. Tympani reddish brown. Throat, belly, and ventral surface of limbs cream, with melanophores, throat tending to a mottled pattern, dark brown laterally, coinciding with the expanded vocal sac. Posterior surface of thighs with a few dark brown spots on a medium brown background, and one white-colored tubercle on each side of cloaca. Posterior surface of tarsi and heel with several cream-colored granules. Cream-colored tarsal fold from the inner metatarsal tubercle extending to 1/3 length of tarsi.

Coloration of holotype in life (fig. 1A). Blackish brown with barely distinguishable non-uniform darker blotches. Arms, some portions of dorsum, legs, and glands (jaw and posterior surface of thighs) orange.

Variation. Within the type series, it is restricted to the extent, distribution, and coloration of the granules scattered on dorsum. The specimens AAG-UFU 1398–1399, 1401–1403 have a white faded well-developed shovel-like fleshy ridge on snout tip. Specimens have a single or a few variably-sized distal antebrachial tubercles on undersides of forearms. In life, dorsum varies from blackish brown or gray with barely distinguishable nonuniform darker blotches to an almost uniformly black coloration. Some portions of dorsum, arms, legs, interorbital region, and granules on flanks have a reddish orange coloration.

Advertisement call. Six males were recorded (N = 397 analyzed calls; see Table 2 for individual sample sizes). Advertisement call (fig. 4; Tables 2, 4) consists of well-defined series of 7–32 calls (mean 22.6; SD = 5.8) with a progressive increment in amplitude in the first third of each call series when it reaches a sustained plateau, which is emitted from 1–2 series/minute (mean 1.1; SD = 0.2). Series duration varies from 3.5– 10.9 s (mean 8.3; SD = 2.0). Calls have up to 9 visible harmonics and a slight ascendant frequency modulation throughout their duration, emitted from 7–42 calls/minute (mean 23.6; SD = 7.7). Calls are composed of 8–14 pulses (mean 11.6; SD = 0.9) with deep and regular amplitude modulation. Call duration varies from 69–191 ms (mean 109.2; SD = 13.1), and intercall interval from 0.12– 1.00 s (mean 0.24; SD = 0.03). Dominant frequency peaks from 1.73–1.83 kHz (mean 1.78 kHz; SD = 0.01) in the 1st harmonic, or from 3.33–3.80 kHz (mean 3.63 kHz; SD = 0.08) in the 2nd harmonic. Dominant frequency corresponds to the 2nd harmonic (67% of males recorded), or corresponds to either the 1st harmonic or the 2nd harmonic (33% of males recorded) among calls analyzed for each male. The other harmonics, if present, are increasingly weaker in sound energy.

FIGURE 4. Advertisement call of Adenomera cotuba sp. nov. (AAG-UFU 1397) from Teresina de Goiás, central Brazil: A— Oscillogram of an entire advertisement call (call series of aprox. 10.5 seconds) showing the progressive increment in amplitude until reaching a sustained plateau. B—Spectrogram (above) and respective oscillogram (below) of the 13th call in A, identified by a red outline. Sound file: Adeno_cotubaTeresGoiasGO1aTRC_AAGm671; 21:53h, 16 Nov 2012, Air 21.4 °C.

Natural history. Adenomera cotuba sp. nov. occurs in Cerrado environments of central Brazil associated to rocky limestone and sandy soil at the border or inside partially shadowy environments. Males call exposed or under leaf litter. Excited calling males emit their calls in relays, so that this emission pattern can be perceived as a ‘wave’ passing by the observer. A calling male excites the nearest one and so on, even making it possible to predict when a given male will start its call emission based on the approaching calling wave. This phenomenon reported for A. cotuba sp. nov. might be classified as unison bout singing, previously reported for other Neotropical anurans (see Schwartz 1991).

Geographic distribution. Adenomera cotuba sp. nov. is known from its type locality (Teresina de Goiás). The species was also heard in Uruaçu (14°43'S, 49°15'W; approximately 575 m a.s.l.) (T.R. de Carvalho pers. obs.), approximately 235 km southwest of its type locality, both localities in northern Goiás, central Brazil. Preserved specimens (CHUNB collection; see Additional examined material section) from Goiânia (central Goiás) and Figueirópolis (southern Tocantins) were also assigned to A. cotuba sp. nov., suggesting a more widespread distribution of this species in the Cerrado of central and northern Brazil.

Conservation status. Adenomera cotuba sp. nov. is currently known from its type locality, and other three localities, as discussed earlier, and we suspect a more widespread distribution for the species. However, future studies on fluctuations and potential threats at a population level are still required for a more accurate assessment of the conservation status of this species according to IUCN guidelines for the next Red List of Threatened Species (IUCN 2013), and we suggest classifying this species as Least Concern (LC) while additional data are obtained.

Etymology. The term ‘cotuba’ is an appositive that was borrowed from Tupi indigenous language and stands for robust, fleshy, or well-nourished, related to the very robust body shape of the species.

Additional examined material. BRAZIL: GOIÁS: GOIÂNIA (CHUNB 56517, 56452–56453); TOCANTINS: Figueirópolis (CHUNB 62864, 62897).

Figures

FIGURE 1. Live adult male specimens of Adenomera cotuba sp. nov. from Teresina de Goiás, northern Goiás, central Brazil (voucher specimens of call recordings), evidencing the glandular / granular dorsum with a black or very dark-colored dorsal coloration: A) holotype AAG-UFU 1400 (SVL 20.5 mm); B) paratopotype AAG-UFU 0 808 (SVL 19.6 mm); C) paratopotype AAG-UFU 1397 (SVL 18.6 mm); D) paratopotype AAG-UFU 1398 (SVL 20.0 mm); E) paratopotype AAG-UFU 1399 (SVL 19.3 mm).

FIGURE 2. Dorsal (A) and ventral (B) views of the holotype (AAG-UFU 1400; SVL 20.5 mm), and dorsal view of two adult male paratopotype specimens of Adenomera cotuba sp. nov., (C) AAG-UFU 1401 (SVL 19.2 mm), and (D) AAG-UFU 1402 (SVL 20.1 mm), evidencing its robust body shape with a black coloration.

FIGURE 3. Adenomera cotuba sp. nov., holotype (AAG-UFU 1400), adult male. Lateral (A) and dorsal (B) views of head, and ventral views of foot (C) and hand (D).

Tables

TABLE 1. Morphometric measurements (mm) of the type series of Adenomera cotuba sp. nov. and Adenomera juikitam sp. nov. (including the holotypes) from Teresina de Goiás, northern Goiás, central Brazil. Mean + SD (range).

Snout-vent length	Adenomera cotuba sp. nov. N=9 males 19.7+0.6 (18.6–20.5)	Adenomera juikitam sp. nov. N=2 males 19.3+0.2 (19.1–19.5)*
Head length Head width Eye diameter	7.8+0.4 (7.0–8.3) 7.0+0.3 (6.4–7.3) 1.9+0.1 (1.7–2.1)	8.2+0.3 (8.0–8.4) 7.4+0.2 (7.2–7.5) 2.1+0.1 (2.0–2.1)
Tympanum diameter Eye-nostril distance Internarial distance	1.4+0.1 (1.2–1.5) 1.6+0.1 (1.5–1.7) 1.7+0.1 (1.5–1.7)	1.2 1.6+0.1 (1.5–1.7) 1.8+0.1 (1.7–1.8)
Hand length Forearm length Thigh length	4.7+0.2 (4.3–5.0) 4.4+0.2 (4.2–4.8) 8.2+0.3 (7.6–8.6)	4.8 4.7+0.1 (4.6–4.7) 8.1+0.7 (7.6–8.6)
Shank length Tarsus length Foot length	8.3+0.4 (7.7–8.9) 5.4+0.4 (4.8–6.0) 9.0+0.5 (8.0–9.6)	8.7+0.3 (8.5–8.9) 5.8+0.3 (5.6–6.0) 9.3+0.7 (8.8–9.8)