Adenomera juikitam, 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 : 542-549

Adenomera juikitam , new species

Figures 5–7

Holotype. AAG-UFU 1406, 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. Two adult males: AAG-UFU 0 807, on 18 November 2011, by A. A. Giaretta and K. G. Facure; AAG-UFU 1405, collected with the holotype.

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.

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 juikitam 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). Adenomera juikitam sp. nov. (adult male SVL 19.1–19.5 mm; Table 1 ) can also 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), and A. simonstuarti (adult male SVL 25.9–26.2 mm; Angulo & Icochea 2010) by its smaller body size. Adenomera juikitam sp. nov. has a more robust body in dorsal view compared to all the additional material examined by us (figs. 5–6; see Appendix 1).

* Holotype; ** 2nd harmonic peak frequency = dominant frequency.

Additional morphological and color pattern features that can also diagnose Adenomera juikitam sp. nov. from congeners (features of comparative species in parentheses): from A. ajurauna , by the absence of dark brown throat, and 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 of posterior surface of thighs on a black background, yellow to orangish yellow ventral surfaces in male specimens, and prominent row of tubercles on distal portion of forearms (Kok et al. 2007); from A. martinezi and A. saci , by possessing a very robust body in dorsal view (slender body in both A. martinezi and A. saci ; Carvalho & Giaretta 2013); 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 following set of morphological/color characters diagnoses Adenomera juikitam sp. nov. from Adenomera cotuba sp. nov. (data for the latter species in parentheses): dorsum with a marble-like and red coloration (black or very dark-colored dorsum); undersides of forearms with no antebrachial tubercles (undersides of forearms bearing a single or a few variably-sized distal antebrachial tubercles).

The advertisement call (fig. 8; Tables 3 –4) distinguishes Adenomera juikitam sp. nov. from A. ajurauna , A. bokermanni , A. engelsi , A. heyeri , A. lutzi , A. marmorata , A. nana , and A. saci by its pulsed call structure (nonpulsed structure in all aforementioned species; Table 4); from A. andreae , A. araucaria , A. coca , A. hylaedactyla , and A. simonstuarti (combined range 2–15 pulses/call; Table 4) by a greater number of pulses (16–21 pulses/call; Tables 3 –4). Additionally, Adenomera juikitam sp. nov. can be diagnosed from A. andreae , A. araucaria , A. coca , A. diptyx , A. hylaedactyla , A. lutzi , A. marmorata , A. nana , and A. simonstuarti (combined range 16–145 ms; Table 4) by a longer call duration (148–202 ms; Tables 3 –4); from A. andreae , A. diptyx , A. nana , and A. thomei (1st harmonic peak frequency combined range 2.15–3.05 kHz; Table 4), and A. andreae , A. araucaria , A. diptyx , A. marmorata , A. nana , and A. thomei (2nd harmonic peak frequency combined range 4.20–5.60 kHz; Table 4) by its lower frequencies (1st harmonic peak frequency 1.88–2.11 kHz, 2nd harmonic peak frequency 3.70–4.17 kHz; Tables 3 –4); and from A. bokermanni and A. lutzi (combined 1st harmonic peak frequency combined range 1.64– 1.83 kHz, 2nd harmonic peak frequency combined range 3.27–3.62 kHz; Table 4) by its higher frequencies (1st harmonic peak frequency 1.88–2.11 kHz, 2nd harmonic peak frequency 3.70–4.17 kHz; Tables 3 –4).

Both temporal and spectral traits of advertisement calls (Tables 2–4) diagnose Adenomera juikitam sp. nov. from the syntopic Adenomera cotuba sp. nov. (acoustic data for the latter species in parentheses): 16–21 pulses/call (versus 8–14 pulses/call); 1st harmonic peak frequency 1.88–2.11 kHz, and 2nd harmonic peak frequency 3.70–4.17 kHz (versus 1st harmonic peak frequency 1.73–1.83 kHz; 2nd harmonic peak frequency 3.33–3.80 kHz). Furthermore, Adenomera cotuba sp. nov. call consists 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 (fig. 4A), whereas Adenomera juikitam sp. nov. call is emitted in an intermittent pattern (fig. 8A).

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.

Geographic distribution. In addition to the type locality (Teresina de Goiás), Adenomera juikitam sp. nov. specimens were collected in Colinas do Sul (CHUNB collection; see Additional examined material), approximately 95 km southwest of its type locality, both located in the Chapada dos Veadeiros microregion, northern Goiás, central Brazil.

Conservation status. The distribution of Adenomera juikitam sp. nov. is currently restricted to two localities in the Chapada dos Veadeiros microregion, as discussed earlier. Given this, we propose that the species be preliminarily assessed as Data Deficient (DD) according to the IUCN Red List Categories and Criteria (2012). In this respect, future studies on its distribution, population status and potential threats, as well as additional data collection efforts must be performed to be able to better assess its extinction risk.

Etymology. The epithet ‘juikitam’, used in apposition, is the combination of the terms ‘jui’, meaning frog, and ‘kitam’, meaning wart, both borrowed from Tupi indigenous language, and refers to the warty skin texture of the species.

Additional examined material. BRAZIL: GOIÁS: Colinas do Sul (CHUNB 36029–36030).

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).

Figures

FIGURE 5. Live adult male specimens of Adenomera juikitam sp. nov. from Teresina de Goiás, northern Goiás, central Brazil (voucher specimens of call recordings), evidencing the profusely glandular / granular dorsum with a marble-like and red coloration: A) paratopotype AAG-UFU 1405 (SVL 19.2 mm); B) holotype AAG-UFU 1406 (SVL 19.1 mm).

FIGURE 6. Dorsal (A) and ventral (B) views of the holotype of Adenomera juikitam sp. nov. (AAG-UFU 1406; SVL 19.1 mm), evidencing its robust body shape.

FIGURE 7. Adenomera juikitam sp. nov., holotype (AAG-UFU 1406), adult male. Lateral (A) and dorsal (B) views of head, and ventral views of foot (C) and hand (D).

Tables

TABLE 3. Advertisement call traits and recording air temperatures of the three recorded males of Adenomera juikitam sp. nov. from its type locality (Teresina de Goiás, northern Goiás, central Brazil). Mean + SD [CV] (range). N = number of analyzed calls.

Acoustic traits	AAG-UFU 0 807 N=42	AAG-UFU 1405 N=55	AAG-UFU 1406* N=46	Mean+SD (min – max)
Call duration (ms)	196.0+5.0 [2.6%] (182–202)	161.8+6.2 [3.8%] (148–177)	174.1+5.2 [3.0%] (164–188)	177.3+17.4 [3.1%] (148–202)
Intercall interval (s)	1.2+0.2 [16.7%] (1.0–1.6)	1.1+0.1 [9.1%] (1.0–1.3)	1.2+0.4 [33.3%] (0.8–2.2)	1.2+0.1 [19.7%] (0.8–2.2)
Pulses/call	20.2+0.6 [3.0%] (19–21)	16	18	18.1+2.1 [1.0%] (16–21)
Calls/minute	44.0+1.4 [3.2%] (43–45)	45	45	44.7+0.6 [1.1%] (43–45)
1st harmonic peak frequency (kHz)	1.90+0.04 [2.1%] (1.88–1.97)	2.08+0.02 [1.0%] (2.06–2.11)	1.96+0.04 [2.0%] (1.92–2.02)	1.98+0.09 [1.7%] (1.88–2.11)
2nd harmonic peak frequency (kHz)**	3.85+0.07 [1.8%] (3.70–3.94)	3.95+0.03 [0.8%] (3.89–3.98)	4.16+0.02 [0.5%] (4.13–4.17)	3.99+0.16 [1.0%] (3.70–4.17)
Temperature (°C)	25.0	25.0	25.8	(25.0–25.8)