Phyllodytes praeceptor, Orrico & Dias & Marciano-Jr, 2018

Orrico, Victor G. D., Dias, Iuri R. & Marciano-Jr, Euvaldo, 2018, Another new species of Phyllodytes (Anura: Hylidae) from the Atlantic Forest of northeastern Brazil, Zootaxa 4407 (1), pp. 101-110 : 102-107

Phyllodytes praeceptor sp. nov.

( Figs 1 , 2 and 3A )

Phyllodytes sp.— Faivovich et al. (2005); Jowers et al. (2008). Phyllodytes sp. 4—Dias et al. (2014)

Holotype. MZUESC 17484 , adult male ( Fig. 1 ), collected at Serra da Jibóia (12.869436° S; 39.461494° W, 684 m a.s.l), municipality of Santa Terezinha and Elísio Medrado, State of Bahia, Brazil, on 0 2 March 2015, by Iuri R. Dias and Carlos Augusto S. Costa.

Paratypes. Twenty eight specimens: MZUESC 17485, adult male, collected with the holotype; CFBH 23671 , adult male, collected at the Municipality of Una, State of Bahia, Brazil, on 8 June 2009, by Adriano B. Kury , Amazonas Chagas Jr., Alessandro Giupponi, Denis R. Pedroso, and Victor G. D. Orrico; MZUESC 7297–7299 , adult males, collected at “ Ponta da Tulha ”, Municipality of Ilhéus , on July 2008, by Mirco Solé ; MZUESC 9169–9170 and MZUESC 9175 , adult males and female, respectively, collected at “ Fazenda Capitão ”, Municipality of Itacaré, State of Bahia, on 29 November 2010, by Tadeu Medeiros ; MZUESC 10498–10499 , adult males, collected at “ Ponta da Tulha ”, Municipality of Ilhéus , on 21 August 2011 by Mirco Solé, Euvaldo Marciano Jr and Iuri Dias ; MZUESC 10626 , adult male, collected at “ São Roque do Paraguaçu ”, Municipality of Maragogipe , on June 2012, by Euvaldo Marciano Jr ; MZUESC 11584–11585 , adult males, collected at “ Lagoa Encantada ”, Municipality of Ilhéus , on 21 February 2011, by Iuri R. Dias and Mirco Solé ; MZUESC 11610–11612 , adult males, collected at the Municipality of Una, State of Bahia, on 18 February 2012, by Euvaldo Marciano Jr, Paulo Henrique Ribeiro and Leandro Oliveira ; MZUESC 13016 and MZUESC 13026 , adult males, collected at “ Reserva Michelin ”, Municipality of Igrapiúna , on 11 August 2012, by Euvaldo Marciano Jr ; MZUESC 13027 , adult male, collected at “ São Roque do Paraguaçu ”, Municipality of Maragogipe, State of Bahia, on 13 August 2012, by Euvaldo Marciano Jr ; MZUESC 14199–14200 , MZUESC 14207 , and MZUESC 14212 , adult males, collected at “ Acuípe ”, Municipality of Ilhéus , on 26 February 2015, by Euvaldo Marciano Jr and Mirco Solé ; MZUESC 17481–17483 , adult males, collected at the Municipality of Una, State of Bahia, on 0 6 June 2013, by Euvaldo Marciano Jr and Mirco Solé ; MZUESC 17486–17487 , adult males, collected at “ Reserva Michelin ”, Municipality of Igrapiúna , between 23–31 March 2015, by Iuri R. Dias, Euvaldo Marciano Jr, Caio V. Mira- Mendes, Francisco F.R. Oliveira and Leandro Drummond.

Referred specimen. MRT 6144, not examined, collected at “Brazil: Bahia, Uruci-Una”.

Generic placement. A member of Phyllodytes , by possessing fang-like odontoids; molecular data also supports the placement of P. praeceptor as sister taxon of P. luteolus ( Faivovich et al. 2005; Jowers et al. 2008).

Diagnosis. A medium-sized species (SVL 20.7–25.8 mm in males) characterized by: (1) dorsum of body, arms, and legs cream with scattered dark brown spots; (2) a dark brown stripe extending from the eyes; (3) snout short, semicircular (to truncated) in dorsal view, vertical (to truncated) in profile; (4) vomerine teeth in two dense patches, disposed in a transverse plane, behind the choanae; (5) one anterior large, and additional smaller subequal odontoids on each side of the mandible; (6) dorsal skin smooth; (7) vocal sac externally visible; (8) venter areolate with two paramedial rows of developed tubercles; (9) small tubercles in the ventral side of the thighs, the most medial more developed; (10) a tubercle at the tibio-tarsal articulation; (11) unpigmented nuptial pad visible, rounded, moderately expanded, (12) advertisement call consisting of a series of 6–12 pulsed notes, average duration of 5.34 s with notes lasting 0.295 s and dominant frequency ranging between 2928.5–3273.0 Hz.

Comparison with other species. Character states of Phyllodytes praeceptor in parentheses. All species of Phyllodytes have multiple tubercles on the tarsus in various arrangements (a single large tubercle on posteroventral internal margin of tarsus, near to the junction with shank) and, with the exception of P. tuberculosus , different snout shapes in dorsal view (semicircular to truncated). Below we list other diagnostic morphological characters. Specimens of P. amadoi have snout with a small apical tubercle (absent) and two large anterior odontoids on both sides of the mandible (one larger odontoid). Specimens of P. acuminatus and P. megatympanum have a large tympanum, TD> 7 % of SVL, (small, TD ~ 6 % of SVL). Specimens of P. brevirostris , P. edelmoi , P. kautskyi , P. luteolus and P. megatympanum have an immaculate dorsum (spots and blotches on dorsum). Specimens of P. gyrinaethes have a hidden tympanum (distinct) and a mottled dorsal pattern (spots and blotches on dorsum). Male specimens of P. kautskyi and P. maculosus are larger, combined SVL = 38.0– 43.5 mm (SVL = 20.7–25.8 mm). Specimens of P. luteolus have a snout mucronated in dorsal view (semicircular to truncated) and acute in lateral view (vertical to truncated), rows of tubercles in the forearm (inconspicuous), venter with various rows of developed tubercles (only the two paramedial are well-developed). Specimens of P. maculosus have a deeply mottled dorsal pattern (spots and blotches on dorsum). Specimens of P. megatympanum have a bright yellow groin in live specimens (no conspicuous coloration). Specimens of P. melanomystax have a conspicuous large dark brown stripe on the snout and canthus rostralis (absent or thin faded stripe in P. praeceptor ) and lack organized paramedial ventral rows of enlarged tubercles (present). Specimens of P. punctatus lack organized paramedial ventral rows of enlarged tubercles (present). Specimens of P. tuberculosus lack organized paramedial ventral rows of enlarged tubercles (present) and have supranumerary tubercles in the plantar surface (absent). Specimens of P. wuchereri have a dorsal pattern consisting of large black and white stripes and blotches (spots and blotches on dorsum).

Description of holotype. An adult male in good state of preservation, with a piece of muscle removed from the right thigh for molecular analyses. Raw measurements are detailed in Table 1. Head wider than long (HL 89.5 % of HW; HW 37.7% of SVL; HL 33.8 % of SVL); snout truncated in dorsal and lateral views ( Figs 1 and 2 ); nostrils small, rounded, slightly protuberant, situated dorsally and directed anteriorly, nearer to the tip of snout than to eye; internarial distance smaller than eye–nostril distance (IND 65.2 % of END), eyes large (ED 33.8% of HL; 30.2 % of HW; 113 % of END), prominent, situated laterally, directed anterolaterally; interorbital space and dorsum of snout flat; canthus rostralis distinct, rounded; loreal region oblique, slightly concave; tympanum evident, relatively large (TD 18.2 % of HL), nearly circular, separated from posterior border of eye by approximately the diameter of tympanum; tympanum diameter smaller than internarial distance (TD 93.3 % of IND, eye to nostril distance (TD 60.9 % of END), eye diameter (TD 53.8 % of ED), and interorbital distance (TD 31.8 % of IOD); its diameter slightly larger than width of discs on third finger (TD/DF3 = 116.7 %) and of fourth toe (TD/4TD = 127.3 %); tympanic annulus evident; supratympanic fold developed, covering dorsal edge of tympanum, nearly straight, slightly curved downwards and extending until the insertion of arm; vocal sac externally developed, subgular, single; vomerine teeth forming a straight line behind small, rounded, widely separated choanae; each side of mandible with one anterior, large, and smaller subequal odontoids; pupil horizontal.

Forelimbs not hypertrophied, forearms slightly larger (in cross-section) than arms, with four outer tubercles in the forearm near to the hand being the closest to the hand the larger. Hands large (HAL 84.4 % of HL), outer and inner carpal tubercles developed, elliptical; fingers not webbed, small fringe present between fingers III and IV, and IV and V; fingers in crescent order of size, II <V <III <IV; adhesive discs developed (adhesive discs diameter approximately two times finger width), transversally elliptical; disc on finger II, smaller than of other fingers; prepollex indistinct; nuptial pad on the internal base of the finger II, no dark nuptial excrescence; subarticular tubercles large, rounded, single; no supernumerary tubercles.

Hind limbs long (THL+TBL+TAL+FL equals 155.3 % SVL, not hypertrophied; thigh length smaller than tibia length (THL 94.4 % of TBL; THL 44.3 % of SVL; TBL 46.9 % of SVL); sum of thigh and tibia lengths smaller than SVL (THL+TBL 91.2 % of SVL); a single large tubercle on posteroventral internal margin of tarsus, near to the junction with shank. Tarsal length smaller than foot length (TAL 73.8 % of FL). Foot length smaller than thigh and tibia lengths (FL 83.2 % of THL; FL 78.5 % of TBL). Plantar surface without supernumerary tubercles; inner metatarsal tubercle large, rounded; outer metatarsal tubercle small and rounded; toes fringed; discs on toe I, smaller than of other toes; plantar formula, I 0+ – 2½ II 1 – 2 III 1 ½ – 2½ IV 3 ½ – 2 V.

Dorsal surfaces smooth; calcar appendage and supra-cloacal crest absent. Venter and ventral surfaces of thighs warty, each thigh with a large mesal pericloacal tubercle; remaining ventral surfaces smooth.

In preservative, dorsum uniformly creamy with small, irregular dark patches; wide brown stripe extending from the posterior corner of the eye to the insertion of arm; all ventral surfaces white, with the exception of a few minute dark flecks in the mental region and the undersides of the jaws, tarsus, tibia and palmar, plantar surfaces.

Variation. The type specimens are alike in morphological traits, although the female (n = 1) is larger than the males. Variation in measurements is presented in Table 1. Lateral dark brown stripe may extend from the eyes until or after the insertion of the arm. The amount of spots on the dorsum is variable. Only one specimen has no spots on the dorsum (MZUESC 17845). Some specimens (e.g., MZUESC 7298; 10498; 11584; 13026) have black spots on limbs, especially more evident on the hind limbs. A thin faded brown stripe on snout and canthus rostralis extending to the eyes can be found in some individuals (e.g., MZUESC 9175; MZUESC 11610; MZUESC 14207; MZUESC 14212). Snout in dorsal and lateral views vary from semicircular to truncate.

Etymology. The specific epithet is a Latin word meaning “teacher” or “instructor”. The name is given as homage to Dr. Miguel Trefaut Rodrigues for his continuous formation of herpetologists.

Geographic distribution. Known from the coastal lowlands of Bahia, from municipality of Maragogipe to the south of the state in the municipality of Una. Specimens are also known from higher areas such as in Serra da Jiboia (684 m a.s.l), Santa Terezinha municipality ( Fig. 4 ).

Advertisement call. The advertisement call ( Fig. 5 ) of Phyllodytes praeceptor has a total duration of 3.02– 9.41 s (5.34 ± 1.53, n = 28). It is emitted at intervals of 29.5– 99.2 s (48.5 ± 21.2, n = 27) and with a dominant frequency of 2928.5–3273.0 Hz (3045.4 ± 115.3, n = 28). Each call is composed of 6–12 notes (8.39 ± 1.55, n = 28) with structured pulses lasting 0.141– 0.538 s (0.295 ± 0.075, n = 235), emitted at intervals of 0.236– 1.057 s (0.389 ± 0.102, n = 207), resulting in a note rate of 1.28–2.02 (1.61 ± 0.2, n = 28) notes/s. The interval between the final two notes of the call is generally much larger than the previous intervals. The notes dominant frequency range is 1378.1–3617.6 Hz (2998.1 ± 275.1, n = 235).

Notes are composed by isolated pulses and/or by 1–11 pulse groups with 2–8 pulses in each group. Usually, the last pulse group is the largest among them and always composed of 6–15 more aggregated pulses. The total number of pulses per note is 17–58 (28.7 ± 9.4, n = 89) and pulse emission rate is 67.2–141.8 pulses/s (98.9 ± 15.8, n = 89). The notes exhibit amplitude modulation, usually starting with low intensity and increasing during the note.

Bioacoustic comparisons with other species. The advertisement call of Phyllodytes praeceptor has a pulsed structure being readily distinguishable from the call of P. acuminatus , P. kautskyi , P. megatympanum and P. melanomystax , which show unpulsed structure (Campos et al., 2014; Nunes et al., 2007; Simon & Gasparini, 2003, Marciano Jr. et al. 2017).

The calls of Phyllodytes amadoi , P. luteolus , P. edelmoi , P. tuberculosus , P. gyrinaethes and P wuchereri (Weygoldt 1981; Lima et al. 2008; Juncá et al. 2012; Roberto & Ávila 2013 Cruz et al. 2014; Magalhães et al. 2015; Vörös et al. 2017) are more similar to P. praeceptor because all of them consist of a series of multipulsionated notes and present overlap in some acoustic parameters, mainly in dominant frequency and call duration (except P. gyrinaethes , with shorter call and P. amadoi with high dominant frequency).

The number of notes per call is higher in P. edelmoi (22–29), P. amadoi (13-17) and P. tuberculosus (14–23), and their ranges do not overlap with the variation of P. praeceptor (6–12). The mean number of notes of P. praeceptor (8.39 ± 1.55, 6–12) is smaller than the mean of P. wuchereri (16.18±3.25, 10–21) and larger than of P. gyrinaethes (4.90 ± 0.60, 4–6).

The note duration in P. praeceptor (0.295 ± 0.075) is longer than in all species of the genus with described calls: P. luteolus (0.125, no range available), P. edelmoi (0.10 ± 0.003, 0.04–0.16), P. tuberculosus (0.17 ± 0.047, 0.07–0.25), P. gyrinaethes (0.04 ± 0.01, 0.02–0.07), P. wuchereri (0.19 ± 0.04, 0.11–0.32 and 0.12 ± 0.013, 0.04–0.14), P. kautskyi (0.08 ± 0.012, no range available), P. melanomystax (0.07 ± 0.04, no range available), P. acuminatus (0.10 ± 0.03, 0.03–0.17), P. megatympanum (0.092 ± 0.08, 0.009–0.24) and P. amadoi (0.043 ± 0.02, 0.008–0.119).

Finally, the call of Phyllodytes praeceptor differs from all species of the genus by having an accentuated increase in amplitude from the first to the last pulse of each note ( Fig. 5 ), concentrating energy at the last cluster of pulses.

Molecular data. Uncorrected pairwise genetic distances of 803 pb of 16S generated in this study are 1 % in relation to Phyllodytes sp. ( AY843722 ; voucher MRT 6144) and 9.6 % to P. luteolus ( AY843721 ). Given this results, we conclude that the specimen MRT 6144, sequenced by Faivovich et al. (2005), should be identified as P. praeceptor .

Figures

FIGURE 1. Phyllodytes praeceptor sp. nov., holotype (MZUESC 17484; SVL 22.8 mm), dorsal and ventral views.

FIGURE 3. Phyllodytes praeceptor sp. nov. in life.A) holotype (MZUESC 17484) and B) specimen not collected.

FIGURE 4. Geographic distribution of Phyllodytes praeceptor sp. nov. Geographic coordinates in decimal degrees, Datum WGS 84. (Star) -12.869436 S, -39.461494 W; (1) -12.836035 S, -38.866291 W; (2) -13.828639 S, -39.218833 W; (3) - 14.32797222 S, -39.07811111 W; (4) -14.53912 S, -39.15461; (5) -14.600967 S, -39.062332 W; (6) -15.07488889 S, -39.0525 W; (7) -15.18401S, -39.06638 W.

FIGURE 5. Advertisement call of Phyllodytes praeceptor (MZUESC 17484, holotype). A) Waveform and B) audiospectrogram.Recorded on 02 March 2015 at 22 h 17 min. Air temperature during recording = 22°C.

FIGURE2. Phyllodytes praeceptor sp. nov., holotype(MZUESC 17484; SVL 22.8 mm, scalebar = 2 mm).A) Dorsalview of the head; B) Lateral view of the head (left side); C) Left hindlimb (notice the tubercle near the heel); D) Plantar view of the left hand.