Bioacoustics of Adenomera juikitam

Remarks and discussion. Both newly described species occur in syntopy, and our acoustic data distinguish one from the other in call emission pattern, temporal (pulses/call) and spectral (frequency peaks) traits of their advertisement calls (see Table 4). Besides, both the dorsal coloration pattern [ A. cotuba sp. nov. (black or very dark-colored dorsum), A. juikitam sp. nov. (marble-like and red dorsum)], and the presence ( A. cotuba sp. nov. ) or absence ( A. juikitam sp. nov. ) of antebrachial tubercles are distinctive between both taxa. Given that the localities from where we heard calling males have no association with water bodies, we assume that both A. cotuba sp. nov. and A. juikitam sp. nov. possess a terrestrial reproductive mode with non-feeding larvae. An in-depth morphological and distributional revision of Adenomera ( L. marmoratus species group) was performed by Heyer (1973), who covered the various names that are currently placed under synonymy in other Adenomera species. All morphological variability and color patterns available to Heyer (1973) at that time were classified into three morphotype groups. In this respect, neither do Adenomera cotuba sp. nov. nor Adenomera juikitam sp. nov. fit any of these groups by the combination of i) lack of any distinctive dorsal coloration pattern, such as longitudinally arranged spots or dots, dorsolateral or vertebral stripes; ii) lack of dorsolateral folds or dorsal granular rows; iii) lack of toe tips developed into flattened disks. Thus, none of the available names listed by Heyer (1973) might be applied to both newly described Adenomera species. The assessment of the phylogenetic positions of Adenomera cotuba sp. nov. and A. juikitam sp. nov. (an ongoing project) would be a good opportunity to better understand the evolutionary scenario of their cooccurrence, at least at the type locality: a case of closely related taxa (sister species); or a case of taxa more distantly related (recovered in different clades, more closely related to other taxa than to each other). Other cases of pairs of Adenomera species with co-occurrence include two undescribed forest dweller species of Adenomera (referred as Forest Calls I and II) in the Amazon rainforest of southeastern Peru (Angulo et al. 2003), A. marmorata and A. ajurauna (Berneck et al. 2008) , and A. araucaria and A. engelsi in the Atlantic Forest (Kwet et al. 2009).

Description of holotype . AAG-UFU 1406 (figs. 5–7). Adult male. Body very robust in dorsal view. Snout rounded in dorsal view (fig. 7B), acuminate in lateral view (fig. 7A), head longer than wide. A well-developed shovel-like fleshy ridge on snout tip. 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 smooth; 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; finger tips rounded, slightly expanded, and with no webbing or fringing; inner metacarpal tubercle ovoid; outer metacarpal tubercle nearly rounded (fig. 7D). Subarticular tubercles conical, supernumerary tubercles rounded. No thumb asperities or prepollex. Dorsum profusely glandular/granular. Posterior half of dorsum, dorsal surface of shanks, and outer surface of tarsi with several minute tubercles. Vertebral pin-stripe absent. Posterior half of flanks with ill-defined 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), and with no webbing, ridged laterally. Inner metatarsal tubercle ovoid, outer nearly rounded (fig. 7C). Tarsal fold from the inner metatarsal tubercle extending about 1/2 length of tarsi. Subarticular tubercles conical, supernumerary rounded. Measurements of holotype . Morphometric characters (mm) and ratios (%) in relation to SVL ( 19.1 mm ): HL 8.2 (44.0), HW 7.4 (39.3), ED 2.1 (11.0), TD 1.2 (6.3), END 1.6 (7.9), IND 1.8 (9.4), FRL 4.7 (24.1), HAL 4.8 (25.1), TL 8.1 (45.0), SL 8.7 (46.6), TSL 5.8 (31.4), FL 9.3 (51.3). Coloration of holotype in alcohol (figs. 6A – B). Snout tip with a faded white coloration. Dorsum and flanks with a marble-like pattern, varying from pale cream to brownish gray. Granules have the same coloration of dorsum. White-tipped granules scattered on the posterior half of dorsum, dorsal surface of shanks, and outer surface of tarsi. Dorsal surface of limbs with brownish gray stripes/blotches on a faded light brown background. Upper and lower jaws covered with white-colored and marble-like spots/blotches alternately. Tympani light brown. Throat, belly, cream and ventral surface of limbs cream-colored, with melanophores. Posterior surface of thighs immaculate, and one white-colored tubercle on each side of cloaca. Coloration of holotype in life (fig. 5A). Dorsum with a marble-like and red coloration with some dark gray blotches/dots. White granules on dorsum and flanks. Glands on posterior surface of thighs yellow. Thighs with a medium brown coloration. Variation. No remarkable variation concerning morphology and color patterns was observed within Adenomera juikitam sp. nov. type series. Advertisement call. Three males were recorded (N = 143 analyzed calls; see Table 3 for individual sample sizes). Advertisement call (fig. 8; Tables 3 –4) consists of a pulsed signal with deep and regular amplitude modulation emitted in an intermittent pattern from 43–45 calls/minute (mean 44.7; SD = 0.6). Calls have up to 9 visible harmonics and a slight ascendant frequency modulation throughout their duration, and are composed of 16– 21 pulses (mean 18.1; SD = 2.1). Call duration varies from 148–202 ms (mean 177.3; SD = 17.4), and intercall interval from 0.76– 2.16 s (mean 1.18; SD = 0.05). Fundamental frequency (1st harmonic) peaks from 1.88–2.11 kHz (mean 1.98 kHz; SD = 0.09), and dominant frequency corresponds to the 2nd harmonic, peaking from 3.70– 4.17 kHz (mean 3.99 kHz; SD = 0.16). The other harmonics, if present, are increasingly weaker. FIGURE 8. Advertisement call of Adenomera juikitam sp. nov. (voucher AAG-UFU 0808) from Teresina de Goiás, central Brazil : A—A section of 15 calls (~ 20 seconds); B—Spectrogram (above) and respective oscillogram (below) of the 9th call in A, identified by a red outline. Sound file: Adeno_juikitamTeresGoiasGO1bAAGm671; 18:48h, 18 Nov 2011 , Air 25.0 °C. Natural history. Adenomera juikitam sp. nov. occurs in association with rocky limestone and sandy soil in open Cerrado environments. Males call exposed or under leaf litter.

Diagnosis. Adenomera juikitam 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) dorsum profusely glandular/granular with no distinctive dorsal granular rows or dorsolateral folds; 2) dorsum with a marble-like and red coloration with no distinctive color patterns; 3) toe tips not developed into flattened disks; 4) small size (adult male SVL 19.1–19.5 mm ; Table 1 ) and very robust body; 5) long (148–202 ms) advertisement call composed of 16–21 pulses ( Table 3 ). Comparisons with other species. Adenomera juikitam sp. nov. possesses a profusely glandular/granular dorsum, but lacks any distinctive dorsal granular rows or dorsolateral folds (figs. 5–6), whereas A. araucaria , A. coca , A. hylaedactyla , A. heyeri , A martinezi , and A. saci possess distinctive dorsal granular rows or dorsolateral folds (Kwet & Angulo 2002; Angulo et al. 2003; Boistel et al. 2006; Angulo & Reichle 2008; Carvalho & Giaretta 2013). Adenomera juikitam sp. nov. has a dorsum with a marble-like and red coloration 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 on the orbital region, followed by a chevron-like 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.