Bioacoustics of Pristimantis ventrigranulosus

Description of holotype . Dorsal skin, including the head ( Fig. 1 A) and hind limbs coarsely shagreen with some enlarged non-queratinized granules, larger toward flanks; skin on sides of head and dorsal forelimbs smooth; gular region ( Fig. 1 B), hind and forelimbs smooth; belly granular, granules small ( Fig. 1 C). Head slightly longer than wide (head length/head width = 1.1) ( Fig. 1 A and 2A). Snout truncate in dorsal view and protruding in lateral view ( Fig. 2 A–B). Nostrils situated and directed posterolaterally ( Fig. 2 B); nostrils visible from front and in lateral views but not in dorsal and ventral views. Canthus rostralis sloped and slightly concave in lateral view; loreal region nearly flat and vertical ( Fig. 2 B). Tongue ovate, premaxillary and maxillary teeth indistinct, dentigerous process of prevomers large and situated posteromedial to choanae, vocal slits not visible. Eye length 16.5 % of SVL, pupil elliptical horizontally ( Fig. 2 B). Tympanic membrane evident, circular, posterodorsally concealed, tympanic annulus well visible ( Fig. 2 B), its diameter 58% smaller than that of EL; supratympanic fold present, prominent and well visible ( Fig. 2 B). Hands relatively small, length 29% of SVL ( Fig. 2 C). Relative length of adpressed fingers: II <IV <I <III ( Fig. 2 C). Finger I (3.4 mm) longer than Finger 2 (3.0 mm). Discs on Finger I, II and IV moderately expanded; disc on Finger III expanded, bearing lateral fringes ( Fig. 2 C). A large, heart-shaped, outer metacarpal tubercle on median base of palm ( Fig. 2 C); a smaller inner metacarpal tubercle on base of Finger I ( Fig. 2 C); two prominent and well-developed subarticular tubercles on each finger ( Fig. 1 C). Forearm long (84 % longer than arm) and robust (80 % wider than arm). Shank length 56% of SVL. Relative lengths of adpressed toes: I <II <V <III <IV ( Fig. 1 D); inner metatarsal tubercle elliptical and well developed ( Fig. 2 D); outer metatarsal tubercle smaller than inner ( Fig. 2 D); one subarticular tubercle on each toes I and II, two subarticular tubercules on toes III and IV ( Fig. 2 D); three subarticular tubercules on toe IV. Hands lacking lateral fringes and webbing ( Fig. 2 C); feet presenting webbing slightly developed between toes II −III and III −IV ( Fig. 2 D). Tarsal fold present and well developed ( Fig. 2 D). Measurements of holotype (in mm). SVL 24.8; HL 9.8; HW 4.4; EL 4.1; EN 3.6; IND 2.9; EE 5.5; TYH 2.4; TYL 2.8; F3 1.3; F4 1.1; FA 5.0; TL 13.9; TH 13.0; FL 11.3; T4 1.2. Coloration. In life, dorsum grayish brown with dark brown markings consisting of oblique bars beginning in the middorsal region toward to the flanks ( Fig. 3 ). Bars also present on dorsal surfaces of the limbs, arms, fingers and toes ( Fig. 3 ). Internal surfaces of the thighs pale brown, not barred. Inguinal region, dorsal surfaces of the thighs and hands (near to articulation radio-humerus) with orange spots. Interorbital and loreal region with dark brown bars between level of eyes and nostrils ( Fig. 3 ). Tip of the snout white ( Fig. 3 ). Labial and subocular dark brown vertical bars ( Fig. 3 ). Supratympanic fold dark brown. Dorsal portion of iris golden and ventral portion dark gold ( Fig. 3 ). Venter cream white with pale brown reticulate spots on ventral surfaces of thighs, gular region and under axillae. The coloration of preserved specimens resembles life coloration, although brown colors fade to gray and orange spots fade to grayish white. Variation. The finger discs of some individuals of type series are not expanded and lack fringes: MNRJ 75887(finger II and III, left hand); MNRJ 75886 (finger IV, left hand); MNRJ 75889 (finger I, left hand). Subcloacal granules of three individuals (MNRJ 75886, ZUFG 5893 and MNRJ 75889) are absent. The pattern of the dorsal bars is variable in some of the specimens. For variation in morphometrics see Table 2 . SVL 23.5 (± 1.9) 20.2 – 25.4 HL 9.5 (± 1.0) 8.2 – 11.4 HW 8.4 (± 0.9) 6.9 – 9.3 EL 3.6 (± 0.4) 3.1 – 4.2 EM 3.3 (± 0.4) 2.6 – 3.7 IND 2.7 (± 0.1) 2.5 – 2.9 EE 5.3 (± 0.4) 4.8 – 5.9 TYH 2.2 (± 0.3) 1.7 – 2.4 TYL 2.4 (± 0.3) 1.9 – 2.8 F3 1.4 (± 0.2) 1.1 – 1.6 F4 1.1 (± 0.1) 1.0 – 1.4 FA 4.7 (± 0.8) 3.5 – 5.9 TL 13.8 (± 1.7) 10.0 – 15.6 TH 13.2 (± 1.3) 10.8 – 15.0 FL 12.4 (± 1.5) 9.6 – 14.2 T4 1.2 (± 0.2) 1.0 – 1.5 cillatus group and the new species described. Data include ranges (first row for each species) and mean ± standard deviation in parentheses. * Data not available. Species Notes/call Call length Note length Note rate Pulses Fundamental (ms) (ms) frequency (Hz) P. dundeei 8 530 50 13.7 * 1808 − 2497 * * * * * * P. fenestratus 2 – 4 157 – 458 (2.6 ± 0.6) (265.2 ± 81.6) 50 – 91 (63 ± 11.4) 7.7 – 12.7 (10.1 ± 1.5) 9 – 17 (12.9 ± 42.2) 1542 – 2048 (1746.7 ± 158) P. koehleri 3 – 8 173 – 644 (5.7 ± 1.0) (421 ± 159.8) 20 – 54 (35.5 ± 6.6) 11.8 – 17.3 (14.1 ± 1.8) 5 – 9 (7.5 ± 1) 1732 – 1971 (1853.5 ± 72.1) P. s a m a i p a t a e 1 – 3 82.2 – 1062 (2 ± 0.2) (291.7 ± 168.1) 59 – 141 (89 ± 16.4) 2.7 – 14.9 (8.5 ± 2.1) 11 – 23 (16.4 ± 2.6) 1535 – 1834 (1704.9 ± 64.3) P. vilarsi 8 521 * * 3 − 21 (8 ± 6) 14 * * 1959 − 2256 * P. ventrigranulosus 4 − 7 202 − 411 (4.9 ± 0.8) (289 ± 60) 24 − 74 (43.8 ± 8.8) 15.6 − 19.8 (17.1 ± 1.1) 4 − 9 (6.2 ± 1.2) * continued. Species Dominant Notes frequency (Hz) Calls No. of speci- mens No. of Populations Source P. dundeei 3273 − 4737 * 2 1 1 1 Heyer & Muñoz (1999) P. fenestratus 1710 – 3591 55 (3086.3 ± 580.7) 22 6 4 Padial & De La Riva (2009) P. koehleri 3245 – 3971 119 (3662.4 ± 128.9) 21 6 2 Padial & De La Riva (2009) P. s a m a i p a t a e 2922 – 3853 160 (3326.7 ± 175.9) 98 12 4 Padial & De La Riva (2009) P. vilarsi 3799 − 4284 8 * 1 1 1 Heyer & Barrio- Amorós (2011) P. ventrigranulosus 3451.8 − 4334.8 108 (4021.0 ± 270.4) 22 3 1 Present work Advertisement call. Acoustic parameters and comparisons to other species of the P. conspicullatus group are summarized in Table 3 . Advertisement calls of Pristimantis ventrigranulosus have no harmonic structure ( Fig. 4 B) and the notes are pulsed, having an average of 6.2 pulses per note ( Fig. 4 A). Calls are composed by four, five, six or seven notes with dominance of five notes (±50%) ( Fig. 4 A). Mean call length is 289 ± 60 ms (range, 202–411 ms) and mean note length is 43.8 ± 8.8 ms (range, 24–74 ms). Mean of the first band energy frequency is 3386.1 ± 313.7 Hz (range, 2127.2–3652.4 Hz) and mean dominant frequency 4021 ± 270.4 Hz (ranging 3451.8–4334.8 Hz). We prefer not to classify the first energy frequency as fundamental frequency because the dominant frequency is not multiple of this first frequency. The maximum intensity is released on the second frequency band, classified as dominant frequency ( Fig. 4 C). In general, the calls had an ascending modulation at the beginning and the last note is the longest, with intermediate notes having similar length ( Fig. 4 A). Amplitude modulation also increases at the beginning of notes and decreases toward the end. Comparisons with similar species show that advertisement call of new species is more similar to P. k o e h l e r i calls, but call length and dominant frequencies distinguish them ( Table 3 ). Natural history. Adult males were found calling on bushes, litter and about 60 – 100cm above the ground after 18:30h, on the 18th October 2009 . Calling were positioned nearly vertical with their heads directed toward the ground. They were found only in “Palmeiral” vegetation ( sensu Ribeiro & Walter 1998 ) near to the Piranhas River. This kind of phytophysiognomy represents a secondary formation resulted of anthropogenic disturbance of an area of primary forest classified as gallery forest ( sensu Ribeiro & Walter 1998 ). The actual pattern can be characterized as “Palmeiral” formed by the palm tree named “babaçú” ( Attalea speciosa Mart. ), which has a high capacity to adapt to anthropogenic environments (J. D. A. Pereira, pers. com.). Other species found at the type locality and vicinities include: Ameerega berohoka Vaz-Silva & Maciel 2011 ; Barycholos ternetzi ( Miranda-Ribeiro 1937 ) ; Chiasmocleis albopunctata ( Boettger 1885 ) ; Dendropsophus cruzi ( Pombal & Bastos 1998 ) ; D. minutus ( Peters 1872 ) ; D. nanus ( Boulenger 1889 ) ; D. rubicundulus ( Reinhardt & Lütken 1862 “1861”); Elachistocleis cesarii ( Miranda-Ribeiro 1920 ) ; Eupemphix nattereri Steindachner 1863 ; Hypsiboas albopunctatus ( Spix 1824 ) ; H. lundii ( Burmeister 1856 ) ; H. paranaiba Carvalho & Giaretta 2010 ; H. raniceps Cope 1862a ; Leptodactylus fuscus ( Schneider 1799 ) ; L. labyrinthicus ( Spix 1824 ) ; Leptodactylus aff. latrans ( Steffen 1815 ) ; L. martinezi ( Bokermann 1956 ) ; L. mystaceus ( Spix 1824 ) ; L. podicipinus ( Cope 1862b ) ; Lithobates palmipes ( Spix 1824 ) ; Osteocephalus aff. taurinus Steindachner 1862 ; Phyllomeduza azurea Cope 1862; Physalaemus centralis Bokermann 1962 ; P. cuvieri Fitzinger 1826 ; Pseudopaludicola saltica ( Cope 1887 ) ; Rhinella mirandaribeiroi ( Gallardo 1965 ) ; R. ocellata ( Günther 1858 ) ; R. schneideri ( Werner 1894 ) ; Scinax fuscomarginatus ( A. Lutz 1925a ) ; S. fuscovarius ( A. Lutz 1925b ) ; Scinax aff. ruber ( Laurenti 1768 ) ; and, Trachycephalus typhonius (Laurenti 1758) ( Oliveira et al. 2010 ; W. Vaz-Silva, unpubl. data;).

Remarks. Traditionally, the most important character states used to group species within the Pristimantis conspicillatus group (sensu Lynch & Duellman, 1997 ), were a smooth belly, together with Finger I longer than Finger II. The first to report a slightly granular belly in members of this group were Heyer & Muñoz (1999) for P. dundeei . Nonetheless, P. dundeei , the only other species of Pristimantis inhabiting the dry forests formations of the Cerrado Biome, was recently removed from the P. conspicillatus group by Hedges et al. (2008) , probably due to its granular belly. Pristimantis dundeei is now placed on the P. peruvianus group, a group including Andean and Amazonian species sharing a granular belly and a first finger shorter than the second, except in the case of P. peruvianus and P. dundeei . However, the granular texture of P. dundeei differs from the texture of members of the P. peruvianus group, which have a more vascularized ventral skin and larger flat “granules” that is usually referred as an aerolate belly (J. M. Padial, pers. obs.). In addition, the specimen identified by Hedges et al. (2008) as P. peruvianus , and included in their molecular phylogeny corresponds to P. re i c h l e i (Padial & De la Riva 2009 ), a species with the first finger shorter than the second and with aerolate belly. Moreover, the advertisement call of P. dundeei is identical in structure to the call of other members of the P. conspicillatus group, and characters of advertisement calls of this group have been shown to content informative phylogenetic information ( Goicoechea et al. 2010 ). Therefore, given the doubtful status of the P. peruvianus group, and the shared call structure and most morphological characters between P. dundeei and other members of the P. conspicillatus group, including P. ventrigranulous , we reassign P. dundeei to the P. conspicillatus group.