A New of (Anura: : ) from Northeastern Brazil Author(s): Felipe de Medeiros Magalhães , Daniel Loebmann , Marcelo Nogueira de C. Kokubum , Célio Fernando Baptista Haddad , and Adrian Antonio Garda Source: Herpetologica, 70(1):77-88. 2014. Published By: The Herpetologists' League URL: http://www.bioone.org/doi/full/10.1655/HERPETOLOGICA-D-13-00054

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A NEW SPECIES OF PSEUDOPALUDICOLA (ANURA: LEPTODACTYLIDAE: LEIUPERINAE) FROM NORTHEASTERN BRAZIL

1 2 3 FELIPE DE MEDEIROS MAGALHA˜ ES ,DANIEL LOEBMANN ,MARCELO NOGUEIRA DE C. KOKUBUM , 4 5,6 CE´ LIO FERNANDO BAPTISTA HADDAD , AND ADRIAN ANTONIO GARDA 1 Programa de Pos–gradua¸´ ca˜o em Sistema´tica e Evolu¸ca˜o, Laboratorio´ de Anfıbios´ e Re´pteis (LAR), Departamento de Botanica,ˆ Ecologia e Zoologia (DBEZ), Centro de Biociencias,ˆ Universidade Federal do Rio Grande do Norte, Campus Universita´rio, Lagoa Nova, 59078–970, Natal, RN, Brazil 2 Laboratorio´ de Vertebrados Terrestres, Instituto de Cienciasˆ Biologicas,´ Universidade Federal do Rio Grande, Avenida Ita´lia, km 8, Vila Carreiros, 96.203–900, Rio Grande, RS, Brazil 3 Laboratorio´ de Herpetologia, Unidade Academicaˆ de Cienciasˆ Biologicas´ e Programa de Pos-gradua¸´ ca˜o em Cienciasˆ Florestais, CSTR/Universidade Federal de Campina Grande (UFCG), CEP 58708-110, Patos, PB, Brazil 4 Laboratorio´ de Herpetologia, Departamento de Zoologia, Instituto de Biociencias,ˆ Universidade Estadual Paulista Avenida 24 A, 1515, Bairro Bela Vista, 13506–970, Rio Claro, SP, Brazil 5 LAR, DBEZ, Centro de Biociencias,ˆ Universidade Federal do Rio Grande do Norte, Campus Universita´rio, Lagoa Nova, 59078–970, Natal, RN, Brazil

ABSTRACT: We describe a new species of Pseudopaludicola endemic to the Caatinga ecoregion of northeastern Brazil. The new species is characterized morphologically by small size, lack of T-shape terminal phalanges, smooth upper eyelids, presence of abdominal and vocal sac folds, light cream-colored vocal sac, and short hind limbs with tibia–tarsal articulation reaching the eye. The tadpole has a globular body shape, low tail fins, and a ventral oral disc bordered by a single row of marginal papillae with a wide anterior gap and two ventrolateral gaps; oral formula: 2(2)/2(1). The advertisement call consists of a well-defined sequence of notes comprising three nonconcatenated pulses, each with long interpulse intervals (111 6 21 ms) and average note duration of 238 6 31 ms. The mean dominant frequency is 5636 6 300 Hz, and increases from the first to the last pulse in each note. The advertisement call easily distinguishes the new species from all other congeners for which calls are known. Key words: Advertisement call; Caatinga; Distribution; Larval morphology; Pseudopaludicola pocoto

THE Pseudopaludicola comprises 18 (Haddad and Cardoso, 1987) to 18 in 2013 species of small in South America, (Frost, 2013). Some of the recently described occurring from northern Argentina to Ven- species occur in heavily studied areas (such as ezuela east of the Andes (Frost, 2013). The Minas Gerais and Sa˜o Paulo states; Toledo, genus forms the basal taxon in the leptodac- 2010; Toledo et al., 2010). The discovery of tylid subfamily Leiuperinae (Pyron and new species in well-studied regions suggests Wiens, 2011). They are frequently found that additional undescribed species are likely calling during the day (and occasionally at to occur in poorly known areas such as the night) around open areas in tropical forests semiarid Brazilian Caatinga (Tabarelli and (Amazon and Atlantic forests) and in open Silva, 2003; see Roberto et al., 2013). formations (Chaco, Pampas, Cerrado, and The most recent compilation for the herpe- Caatinga). Several new Pseudopaludicola spe- tofauna of the Caatinga lists 173 species (48 cies have been described in recent years anurans, 3 caecilians, 10 turtles, 3 crocody- (Toledo, 2010; Toledo et al., 2010; Pansonato lians, and 109 squamates; Rodrigues, 2003). et al., 2012; Roberto et al., 2013) and the calls These numbers are likely to increase substan- and tadpoles of described species have been tially, however, as 40% of the biome has never characterized (Pereira and Nascimento, 2004; been surveyed, and about 80% remains Laufer and Barreneche, 2008; Giaretta and understudied until recently (Tabarelli and Facure, 2009). The number of recognized Silva, 2003). Indeed, several lizard (Arias et species increased from 5 in the late 1980s al., 2011a,b; Passos et al., 2011) and (e.g., Pombal et al., 2012) species have been 6 CORRESPONDENCE: e-mail, [email protected] recently described from the region.

77 78 HERPETOLOGICA [Vol. 70, No. 1

FIG. 1.—Geographic distribution of Pseudopaludicola pocoto sp. nov. in South America. The inset shows the northeastern region of Brazil and the grey area represents the boundaries of the Caatinga biome. Symbols denote the type locality (triangle) and additional localities where the new species was collected (circles). CEARA´ (CE): 1—Santa Quite´ria, 2—Novas Russas, 3—Fortaleza, 4—Missa˜o Velha, RIO GRANDE DO NORTE (RN): 5—Macaıba,´ 6—Serra Negra, PARAIBA´ (PB): 7—Patos, 8—Serra de Santa Catarina, PERNAMBUCO (PE): 9—Betania.ˆ

Here we describe a new species of Pseudo- followed the terminology for external mor- paludicola, which is widespread in the Caa- phology from Duellman (1970). Specimens tinga ecoregion. We characterize the species, used in this description are housed in the advertisement call and larval external mor- Ce´lio F.B. Haddad Collection at the Depar- phology, and we compare it to allied species. tamento de Zoologia, Universidade Estadual Paulista, Campus de Rio Claro, Sa˜o Paulo, MATERIALS AND METHODS Brazil (CFBH) and in the Herpetological We collected frogs at several localities Collection of Universidade Federal do Rio throughout northeastern Brazil (see geograph- Grande, Rio Grande, Rio Grande do Sul, ic distribution, Fig. 1). We euthanized spec- Brazil (FURG). Tissue samples are housed in imens by rubbing lidocaine cream onto their Cole¸ca˜o de Anfıbios´ de Re´pteis da Universi- abdomens or through CO2 asphyxiation. We dade Federal do Rio Grande do Norte individually tagged each specimen, collected (CLAR–UFRN) and Laboratorio´ de Herpe- tissue samples, fixed specimens in 10% tologia da Universidade Federal de Campina formalin, and transferred them to 70% Grande (LHUFCG). Specimens examined for ethanol for permanent storage (collecting species comparisons are listed in Appendix I. permits to AAG SISBIO 32527–1, DL SIS- We described the advertisement call for the BIO 12545-2, and MNCK SISBIO 25267-1). new species based on recordings of nine We measured morphometric variables with individuals from five localities (Table 1; all the use of a Digimess digital caliper (60.01 latitude and longitude readings based on mm) according to Pansonato et al. (2013) and WGS84 data): Missa˜o Velha (78140S, 39880W; March 2014] HERPETOLOGICA 79

TABLE 2.—Measurements (in millimeters) of Pseudopalu-

, PB: dicola pocoto sp. nov. type series from municipalities of ´ Fortaleza, Novas Russas, and Santa Quite´ria, Ceara´ State, Brazil. n ¼ number of measured individuals.

Paratypes (n ¼ 14)

Measurements Holotype Mean 6 SD Range o Velha/CE ´ ıba/RN ´ ıba/RN ´ ıba/RN ˜ Snout–vent length 14.3 13.3 6 1.0 11.5–14.5 Head length 5.6 4.9 6 0.5 4.0–5.6 Head width 5.6 5.4 6 0.4 4.7–6.2 Eye diameter 1.7 1.6 6 0.1 1.4–1.9 C) Municipality/state 8 Interorbital distance 3.0 2.8 6 0.2 2.4–3.0 Eye–nostril distance 1.2 1.1 6 0.1 1.0–1.3 Internarial distance 1.0 1.1 6 0.1 1.0–1.2 Eye–snout distance 2.2 2.1 6 0.1 2.0–2.3 Hand length 4.0 3.9 6 0.2 3.5–4.2 Thigh length 7.6 6.8 6 0.4 6.2–7.6 Tibia length 7.7 7.4 6 0.3 6.9–8.0 Tarsus length 4.0 3.7 6 0.3 3.3–4.1 Foot length 8.0 7.9 6 0.4 7.3–8.7 87 (5513–5685) 24 Maca 100 (5513–5857) 24 Maca 142 (5168–5513) 24.3 Maca 87 (5340–5685) – Missa 125 (5857–6374) – Morada Nova/CE 97 (5168–5685) – Novas Russas/CE 155 (5513–6202) 26 Serra de Santa Catarina/PB 108 (5340–5857) 25.3 Serra de Santa Catarina/PB 94 (5186–5513) 25 Serra de Santa Catarina/PB 300 (5168–6373) 363 m above sea level [asl]), Morada Nova 0 0 6 6 6 6 6 6 6 6 6 6 (586 S, 38822 W; 50 m asl), and Nova Russas (48420S, 408330W; 230 m asl) municipalities, Ceara´ State; Aguiar municipality (78000S, 388130W; 380 m asl), Paraıba´ State and ´ 8 0 8 0

SD (range). Brazilian state acronyms: RN: Rio Grande do Norte, CE: Ceara Macaıba municipality (5 53 S, 35 22 W; 11 ´ ıba. 6 m asl), Rio Grande do Norte State. Frogs were recorded with the use of a Marantz Para 15 (82–136) 5608 20 (94–166) 5581 26 (49–160) 5340 11 (78–135) 5562 6 (81–109) 6278 16 (105–156) 5455 18 (43–128) 5872 15 (87–147) 5621 14 (85–146) 5376 21 (43–166) 5636 PMD 661 coupled with a Sennheiser ME66 6 6 6 6 6 6 6 6 6 6 directional microphone (Rio Grande do Norte; from 1800 to 2100 h), a Sony TCM sp. nov. Mean 5000 EV coupled with a Sennheiser ME66 (Morada Nova, Ceara´; at 2000 h), an Olympus S11 with a built-in microphone 1 (4–8) 106 0.6 (3–5) 127 0.6 (3–5) 104 1 (4–8) 124 1 (4–6) 97 1 (3–7) 126 0.5 (3–5) 92 0.6 (3–5) 116 0.5 (3–5) 116 1 (3–8) 111 (Missa˜o Velha, Ceara´; at 1927 h), and a 6 6 6 6 6 6 6 6 6 6 Microtreck II coupled with a Sennheiser ME66 directional microphone (Paraıba;´ from 1800 to 2300 h). We analyzed adver- tisement calls (15 notes per recording) in Pseudopaludicola pocoto Raven Pro v1.4 and constructed audio spectrograms with the following parameters: fast Fourier transform (FFT) window width ¼ 512, frame ¼ 100, overlap ¼ 75, and flat top filter. Variables used in comparisons are listed in Table 1. We follow the terminology 25 (190–284) 3 5 16 (226–289) 3 4 37 (126–263) 3 4 15 (224–281) 3 6 4 (204–220) 3 5 15 (237–290) 3 5 14 (176–227) 3 4 26 (194–286) 3 4 23 (202–282) 2–3 3 31 (126–290) 3 5 6 6 6 6 6 6 6 6 6 6 for frog call descriptions used by Duellman and Trueb (1986) and McLister et al. (1995), who consider a ‘‘note’’ as a single unit of sound, consisting of one or more pulses, produced during a single airflow cycle. We

1.—Advertisement call parameters of deposited call recording files in the following collections: Arquivos Sonoros da Universi- ABLE T Collection numberASUFRN145 Note duration (ms) 228 Pulses/note Pulse duration (ms) Interpulse interval (ms) Dominant frequency (Hz) Temperature ( ASUFRN146 268 ASUFRN153 220 ASUFRN224 266 ASUFRN225 211 DL005 269 LHUFCG453 207 LHUFCG452 245 LHUFCG306 243 Mean 238 dade Federal do Rio Grande do Norte 80 HERPETOLOGICA [Vol. 70, No. 1

(ASUFRN), Daniel Loebmann Sound Col- lection (DL), and Laboratorio´ de Herpeto- logia da Universidade Federal de Campina Grande (LHUFCG). We collected larvae in a pond at the gates of Escola Agrıcola´ de Jundiaı(5´ 8530S, 358210W; 11 m asl), Macaıba´ municipality, Rio Grande do Norte State, Brazil, in June

SD (range). 2012, a week after amplectant pairs were

6 observed in the same pond. No other species of frogs were observed reproducing at this site and no other larvae were collected during this period. An extensive survey of frogs of the region has been published for the region (Magalha˜es et al., 2013), and a key to anuran larvae of the area is being completed by FMM. Although we were not 110 (5510–6030) Toledo (2010) 180 (4390–4910) Toledo (2010) 531 (3359–5469) Pansonato et al. (2013) 263320 (5170–6370)300 (5168–6373) Toledo (2010) This study Pereira and Nascimento (2004) 247 (3187–4399) Pansonato et al. (2013) 6 6 6 6 6 6 6 able to rear larvae to metamorphosis to confirm their identity in this study, our knowledge of the species and their larvae in the region, and the characteristics of the site where they were collected, enable us to attribute the larvae to the new species unequivocally. We anesthetized and pre- served larvae in 10% formalin and took 0.80 (1–4) 5750 0.51 (1–3) 4600 0.70 (3–6) 5720 0.8 (1–4) 4547 0.3 (3–6) 3989 6 6 6 morphometric measurements with the use of 6 6 Mitutoyo digital calipers (60.01 mm), except

species that emit calls with nonconcatenated pulses. Mean for eye diameter, interorbital and internarial distance, and spiracle and cloacal tube length, which were measured with an ocular micrometer in a Leica-EZ4D stereomicro- scope. We described larvae with the use of the terminology and measurements from Pseudopaludicola 21 (49–166) 3 5636 7 (0–26) 3.07 10 (0–32) 2.08 4 (3–40) 3.3 2 2 4593 6 (1–30) 4.3 Altig and McDiarmid (1999) and determined 4 (0–12) 4.93 6 6 6 6 6 6 development stage according to Limbaugh 6 and Volpe (1957), as modified by Gosner (1960); variables used in this work are listed in Table 4. The specimen used for the illustration and description (AAGARDA 9438) and the remaining lot with 11 specimens (AAGARDA 8825) were also deposited in the CLAR–UFRN. 31 (126–290) 111 22 (25–115) 12 19 (30–90) 19 9 (87–112)10 (30–100) 3 20 420 10 (40–110) 20 6 6 6 6 6 6 6 SPECIES DESCRIPTION 85 76 99 60 4040 30 2 4200–5800 Haddad and Cardoso (1987) 70 3.—Advertisement call parameters of Pseudopaludicola pocoto sp. nov. ABLE

T (Figs. 2, 3; Tables 1, 2)

sp. nov. 238 Holotype.—CFBH 26842, adult male, Santa Quite´ria Municipality, Ceara´ State, Brazil (048190S, 408100W; 20 m asl), collect- P. serrana P. saltica P. murundu P. pocoto P. saltica P. mineira P. falcipes SpeciesP. ameghini Note duration (ms) Interpulse interval (ms) Pulses/noteed on 25 Dominant frequency (Hz) March 2009, by D. Reference Loebmann. March 2014] HERPETOLOGICA 81

TABLE 4.—Measurements (in millimeters) of Pseudopalu- dicola pocoto sp. nov. larvae at Gosner Stages 29–31 from Escola Agrıcola´ de Jundiaı,´ Macaıba´ municipality, Rio Grande do Norte State. n ¼ number of measured individuals.

Stages 29–31 (n ¼ 12)

Measurements Mean 6 SD Range Total length 10.6 6 0.4 10.0–11.3 Body length 4.2 6 0.2 4.0–4.5 Body height 2.1 6 0.2 1.7–2.3 Body width 2.6 6 0.2 2.2–2.9 Tail length 6.4 6 0.3 6.1–6.8 Maximum tail height 2.4 6 0.3 1.8–2.7 Tail muscle height 1.2 6 0.2 1.0–1.4 Tail muscle width 0.7 6 0.1 0.6–0.8 Eye diameter 0.4 6 0.04 0.4–0.5 Interorbital distance 1.2 6 0.2 0.9–1.4 Internarial distance 0.6 6 0.1 0.4–0.7 Eye–snout distance 1.5 6 0.1 1.3–1.7 Nare–snout distance 0.7 6 0.1 0.5–0.8 Spiracle length 1.0 6 0.1 0.9–1.2 Cloacal tube length 1.1 6 0.1 0.9–1.2 Mouth width 0.6 6 0.04 0.6–0.7

FIG.2.—Pseudopaludicola pocoto sp. nov., CFBH Paratypes.—CFBH 26843–26847, all adult 26842 (holotype) from Santa Quite´ria Municipality, Ceara´ State. (A) Dorsal and (B) lateral views of head, (C) left males, collected with the holotype: CFBH hand, and (D) left foot. 20185–20287 adult males, Novas Russas Municipality, Ceara´ State, Brazil (048410S, 0 dominant frequency 5636 6 300 Hz (range 40833 W; 270 m asl), collected on 16 March 5168–6374 Hz). 2008, by D. Loebmann: FURG 2179–2184, The new species is distinguished morpho- adult males, Fortaleza Municipality, Ceara´ logically from all congeners belonging to the State, Brazil (038460S, 388390W; 17 m asl), P. pusilla species group (P. boliviana, P. collected on 25 January 2009, by D. Loeb- ceratophyes, P. llanera, and P. pusilla) by the mann and I.J. Roberto. absence of either T-shaped terminal phalan- Diagnosis.—The new species is assigned to ges (see Cardozo and Sua´rez, 2012) or the genus based on the small size and expanded toe tips (disks or pads). We did presence of hypertrophied antebrachial tu- not include P. canga as a member of P. pusilla bercles (Lobo, 1995). It is distinguished from group based a on recent reassessment of its all other species of the genus by the following osteological features (Cardozo and Sua´rez, combination of characters: (1) smaller size 2012). Also, the new species is differentiated (SVL range ¼ 11.5–14.5 mm in adult males); from P. boliviana, P. ceratophyes, and P. (2) light cream-colored vocal sac with a llanera by the absence of palpebral tubercles longitudinal fold; (3) absence of T-shaped (tubercles are present on the upper eyelids of terminal phalanges (phalange shape similar to these three species; Lynch, 1989). P. facilpes; see Fig. 2B in Cardozo and Sua´rez, Compared to other species of Pseudopalu- 2012); (4) short hind limbs (tibio-tarsal dicola that are not part of P. pusilla group (P. articulation reaching eye); (5) abdominal folds ameghini, P. canga, P. facureae, P. falcipes, P. complete; (6) advertisement call emitted as a giarettai, P. hyleaustralis, P. mineira, P. series of well-defined sequences of three murundu, P. mystacalis, P. parnaiba, P. salt- nonconcatenated pulses per note with long ica, P. serrana, and P. ternetzi), the new intervals (111 6 21 ms; range 43–166 ms) species differs morphologically from P. fal- between each pulse; (7) mean note duration cipes by the presence of a continuous 238 6 31 ms (range 126–290 ms); (8) average abdominal fold (abdominal fold interrupted 82 HERPETOLOGICA [Vol. 70, No. 1 or absent in P. falcipes; Lobo, 1994); from P. two ventrolateral gaps) distinguishes the larva canga, by the absence of dorsal folds and small of P. pocoto from those of P. mineira, P. size with SVL reaching 14.5 mm in males murundu,andP. serrana (gaps on the (dorsal folds are present in P. canga and male posterior labium absent, Pereira and Nasci- SVL range ¼ 14.6–16.2 mm; Giaretta and mento, 2004; Toledo, 2010; Toledo et al., Kokubum, 2003); from P. murundu, P. saltica, 2010), P. boliviana (only one central gap on and P. serrana by shorter hind limbs with the posterior labium; Kehr and Schaefer, tibio-tarsal articulation reaching the eyes 2005), P. falcipes,andP. facureae (two (these three species have very long hind limbs ventrolateral and one central gap on the with tibio-tarsal articulation reaching beyond posterior labium; Giaretta and Facure, the end of the snout; Toledo, 2010) and by the 2009). Also, the labial tooth row formula presence of a light cream-colored vocal sac [2(2)/2(1)] separates the larva of P. pocoto (vocal sac is dark gray in P. serrana and P. from the tadpoles of P. facureae and P. murundu; Toledo, 2010). Compared to P. falcipes [2(2)/3 in these species; Giaretta and ameghini (males SVL range ¼ 14.1–19.3 mm; Facure, 2009]. Pansonato et al., 2013) and P. giarettai (males Description of the holotype.—Body ellipti- SVL range ¼ 16.2–18.0 mm; Carvalho, 2012) cal and robust. Head elliptical, as wide as long. has a smaller size and less robust body. Snout subelliptical in dorsal view and rounded Even though we found no reliable charac- in profile (Fig. 2A,B). Nostrils protuberant, ters that morphologically distinguish adults of directed dorsolaterally. Canthus rostralis P. pocoto from P. facureae, P. hyleaustralis, P. rounded. Loreal region slightly concave. mineira, P. mystacalis, P. parnaiba, and P. Choanae rounded. Eye not protuberant as a ternetzi, the distinctive advertisement call result of fixation, and its diameter represents distinguishes the new species from these about 57% of the interorbital distance; inter- species and from all other congeners for orbital area flat. Tympanum not visible which call descriptions are available. The call externally. Vocal sac singular, slightly expand- of P. pocoto is characterized by well-defined ed externally with longitudinal folds; vocal slits sequences of three nonconcatenated pulses developed, laterally on mouth floor. Vomerine per note. This distinguishes the new species teeth absent. Tongue elliptical, longer than advertisement call from P. canga (Pansonato wide. Finger length I,II,IV,III. Toe length et al., 2012), P. facureae (Andrade and I,II,V,III,IV. Finger and toe tips without Carvalho, 2013), P. giarettai (Carvalho, disks, slightly expanded and round (Fig. 2012), P. hyleaustralis (Pansonato et al., 2C,D). Thumb with keratinized brown nuptial 2012), and P. parnaiba (Roberto et al., pad. Finger webbing absent and toe webbing 2013), which emit calls with single pulsed reduced I–II 2þ–3 III 3þ–4 IV–V. Fringes notes. Additionally, the call structure (three developed on all toes (mainly II, III, and IV) nonconcatenated pulses/note) distinguishes and less developed on fingers. External fringe the calls of P. pocoto from P. boliviana (calls on Toe V continues almost to the external with sets of five notes each one formed by 3–6 metatarsal tubercle. Fingers and toes with concatenated pulses; Dure´ et al., 2004) and P. conical, singular subarticular tubercles. Large mystacalis (12–14 concatenated pulses/note; subconical ulnar tubercle. Internal metacarpal Pansonato et al., 2013). A longer interpulse tubercle elliptical; external metacarpal tuber- interval and note duration distinguish the cle ovoid. Hind limbs robust and long with advertisement call of P. pocoto from all other tibia-tarsal articulation reaching eye. Thigh congeners that emit calls with nonconcaten- length similar to tibia length; foot slightly ated pulses (Table 3). Such parameters also longer than thigh. Toes long. Supernumerary distinguish calls of P. pocoto from those of P. tubercles absent on the sole of foot. Metatar- ternetzi (note duration and interpulse interval sal tubercles present, internal elliptical and are below 100 and 10 ms, respectively, larger than the external; external more protu- Cardozo and Toledo, 2013). berant and conical in shape compared to The marginal papillae configuration (single internal. Well-developed fold from internal row of marginal papillae with one anterior and metatarsal tubercle to the mid-ventral tarsus, March 2014] HERPETOLOGICA 83 ending in a tarsal tubercle less protuberant than the external metatarsal tubercle. Abdom- inal folds are also present; belly skin smooth. Ventral surface of thigh granular. Skin texture smooth. Measurements of the holotype are presented in Table 2. Coloration of the holotype.—In preserva- tive, dorsal surfaces of dorsum and limbs are pale brown, belly is while, and vocal sac is pale cream-colored. White spots on upper lips extending to the flanks. Dorsal surface of legs with brown stripes. Color in life.—There are no data about FIG. 3.—Unvouchered male of Pseudopaludicola pocoto color in life of the holotype. Therefore, color sp. nov. in life from Esta¸ca˜o Ecologica´ do Serido,´ Serra in life and its variation are described based on Negra Municipality, Rio Grande do Norte State, Brazil. paratypes and specimens from other localities (Fig. 3). As with most congeneric species, 0.39). The ratio of eye diameter to eye–snout individuals of P. pocoto vary in whether they distance ranges from 0.70 to 0.90 (mean ¼ have a vertebral line (white, orange or red). 0.77). The ratio of snout width to head width Usually, dorsal surfaces of body and limbs are ranges from 0.34 to 0.52 (mean ¼ 0.44). light brown. In some individuals, well-defined Specimens with a vertebral line, a feature dark brown stripes are present on the dorsal usually present in other species of the genus, surface of thighs (a few), the interorbital were recorded within the type series of P. region (single), and postcranial region (single pocoto. W-shaped stripe). Scattered orange blotches Etymology.—The specific epithet refers to are also present on the dorsal surface of the the similarity of the advertisement call to the body and thighs. The upper jaw has white sound of a horse trotting, which in Portuguese spots, extending to the flanks; the belly and is expressed by the onomatopoeia pocoto´. vocal sac are light cream-colored. Distribution.—Pseudopaludicola pocoto has Variation in the type series.—The type been collected in three adjacent states in series comprises only males (n ¼ 14, Table Brazil at sites within the Caatinga ecoregion: 2); therefore, comparisons between males and (1) in Rio Grande do Norte State it was found females are not possible. Males have nuptial in Escola Agrıcola´ de Jundiaı(Maca´ ıba´ pads well developed, as well as a single Municipality) and Esta¸ca˜oEcologica´ do rounded vocal sac. The ratio of head to Serido,´ Serra Negra Municipality (68390S, snout–vent length ranges from 0.34 to 0.39 378240W; 178 m asl); (2) in Paraıba´ State at (mean ¼ 0.37). The tympanic membrane is not Serra de Santa Catarina, Aguiar Municipality visible (or is difficult to discern) and does not and Patos Municipality (078010S, 378160W; exhibit circumferential grooves. The head is 250 m asl); and (3) in Ceara´ State at Fortaleza slightly wider or equal to its length; the ratio Municipality, semipermanent ponds between of head width to head length ranges from 0.81 Crateus´ and Nova Russas municipalities and to 1.00 (mean ¼ 0.92). Hand length comprises at Santa Quite´ria, Morada Nova and Missa˜o approximately one-half the foot length (the Velha municipalities (Fig. 1). Additionally, the ratio of hand length to foot length ranges new species has been documented in Reserva 0.45–0.55; mean ¼ 0.49). The ratio of foot Particular do Patrimonioˆ Nacional Maurıcio´ length to SVL ranges from 0.54 to 0.65 (mean Dantas, Betaniaˆ municipality, Pernambuco ¼ 0.59), whereas the ratio of hand length to State, where it was identified as Pseudopalu- SVL ranges from 0.26 to 0.33 (mean ¼ 0.29). dicola sp. 2 (Borges-Nojosa and Santos, 2005). The forearm length to hand length ratio Natural history notes.—The new species ranges from 0.50 to 0.63 (mean ¼ 0.56). The can be found in open areas within the ratio of internarial distance to interorbital Caatinga ecoregion. Males can be found distance ranges from 0.33 to 0.46 (mean ¼ calling at dusk (1730 h) and are active mostly 84 HERPETOLOGICA [Vol. 70, No. 1

FIG. 4.—Advertisement call of Pseudopaludicola pocoto sp. nov. from Escola Agrıcola´ de Jundiaı,´ Macaıba´ Municipality, Rio Grande do Norte State. (A) Amplitude of the waveform; (B) Spectrogram. Air temperature ¼ 24.08C. during the night (the last recording was taken recorded at night calling on the ground at the at 2300 h). We observed that males preferen- margins of temporary ponds. The advertise- tially call from the margins of shallow ment call of P. pocoto consists of a well– temporary ponds (depth » 5 cm ) with sandy defined sequence of notes, each one formed or muddy bottoms, actively call during the by sets of three nonconcatenated pulses (Fig. entire rainy season, and maintain their activity 4) with mean note duration of 238 6 31 ms for as long as the reproductive sites remain (range ¼ 126–290 ms) emitted at intervals of flooded (usually from March–September). We 220 6 59 ms (range 136–507 ms) between also found males of Dendropsophus branneri, each note. Also, P. pocoto may occasionally Dermatonotus muelleri, Elachistocleis cesarii, emit notes with one, two (more frequent), or albifrons, P. cuvieri, Pseudopa- four nonconcatenated pulses. One or two ludicola mystacalis, Rhinella granulosa, and pulse notes may be emitted prior to starting Scinax x–signatus calling in and around the same . The larvae of P. pocoto can be the three-pulsed note sequences, but these found along the margins of shallow semiper- and the four-pulsed note are rarely emitted. manent ponds (about 2–5 cm in depth) with Mean duration of each pulse is 5 6 1ms sparse vegetation and they hide in the mud (range ¼ 3–8 ms). Each pulse is followed by an when disturbed. The larvae of the previously interpulse interval of 111 6 21 ms (range ¼ mentioned species can also be found in the 43–166 ms). The average rate of emission is 13 same habitats as P. pocoto. 6 2 pulses/s (range ¼ 10–18) and 124 6 16 Advertisement call description.—We ana- notes/min (range ¼ 94–150). Mean dominant lyzed the advertisement calls of nine speci- frequency is 5636 6 300 Hz (range ¼ 5168– mens (15 notes per recording) of P. pocoto 6374 Hz). The call exhibits frequency modu- from five localities encompassing its entire lation, increasing from the first to the last known distribution (Table 1). All males were pulse in each note. A single note is emitted March 2014] HERPETOLOGICA 85

FIG. 5.—Schematic representation of Pseudopaludicola pocoto sp. nov. tadpole from Escola Agrıcola´ de Jundiaı,´ Macaıba´ Municipality, Rio Grande do Norte State, Brazil. (A) Lateral, dorsal, and ventral views; (B) detail of the oral disk. during a single airflow (personal observations Jaw sheaths are narrow with triangular serra- of FMM and AAG). tion; upper jaw sheath is arc-shaped and lower Description of larva.—Body is dorsoventral- jaw sheath v-shaped. In life, body and tail ly compressed with a globular appearance musculature are dark brown, and fins are (Fig. 5). Snout is rounded in all views. Eyes translucent with few scattered brown-pig- are small and positioned dorsally. Nares are mented blotches along its extension. oval and located closer to eyes than to snout, Remarks.—Pseudopaludicola pocoto is without projection on marginal rim. The widely distributed across the Caatinga and spiracle is sinistral, short and narrow, opening several populations were found within pro- on the middle third of the body bellow the tected and disturbed areas. Therefore, we lateral line with proximal wall fused to it. The consider the new species not endangered and cloacal tube is medial, narrow, and fused to recommend it be listed as Least Concern the fin. The dorsal fin slightly arched, following IUCN categories. Because we only emerging on the last third of the body; ventral collected the new species at sites within the fin with margin parallel to the longitudinal tail Caatinga or in ecotonal areas, it is likely axis; both fins are lower than body and similar endemic to this ecoregion, and thereby in height. The tail ends in a rounded tip. The provides additional evidence that the species oral disc is ventral and laterally emarginated; richness of this region is likely underestimat- single row of marginal papillae with a wide ed. gap on the anterior labium and two ventrolat- eral gaps on the posterior labium; submarginal DISCUSSION papillae absent. Labial tooth row formula: The conservative external morphology and 2(2)/2(1); A–1, A–2; P–1 with similar length small size of species of Pseudopaludicola whereas P–2 is slightly shorter; A–2 is widely hamper the assessment of species diversity interrupted and P–1 is narrowly interrupted. of the genus. Nevertheless, advertisement call 86 HERPETOLOGICA [Vol. 70, No. 1 parameters and tadpole morphology can aid in calls, and L.F. Toledo for information on Pseudopaludi- the comparison and delimitation of species in cola calls. R.A. Pyron and D.B. Shepard kindly revised the English. FMM and AAG thank the crew of Laboratorio´ de the genus. Indeed, several recently described Anfıbios´ e Re´pteis–UFRN for help in fieldwork. FMM and revalidated species are diagnosed primar- thanks Capes for his Masters fellowship. Parts of this ily through advertisement calls (Carvalho, research were supported by two grants from CNPq to 2012; Pansonato et al., 2012; Andrade and AAG (552031/2011–9 and 558317/2009-0). CFBH is grateful for grant 2008/50928-1, Sa˜o Paulo Research Carvalho, 2013; Pansonato et al., 2013). Foundation (FAPESP), and the research fellowship of Despite the importance of advertisement CNPq. calls in the delimitation of species of Pseudo- paludicola, the terminology used for call LITERATURE CITED parameters in different studies is not always Altig, R., and R.W. McDiarmid. 1999. Body plan: compatible. For example, for P. saltica the Development and morphology. Pp. 24–51 in R.W. term note (Pansonato et al., 2013) was used to McDiarmid and R. Altig (Eds.), Tadpoles: The Biology refer to the same structure previously named of Anuran Larvae. The University of Chicago Press, pulse (Toledo, 2010), whereas the term call USA. Andrade, F.S., and T.R. Carvalho. 2013. A new species of (Pansonato et al., 2013) was applied to the Pseudopaludicola Miranda-Ribeiro (Leiuperinae: Lep- structure previously named note (Toledo, todactylidae: Anura) from the Cerrado of southeastern 2010). Likewise, the call of P. canga was Brazil. Zootaxa 3608:389–397. described as notes composed of one–nine Arias, F., C.M. Carvalho, M.T. Rodrigues, and H. Zaher. 2011a. Two new species of Cnemidophorus (Squamata: nonconcatenated pulses (Giaretta and Koku- Teiidae) from the Caatinga, Northwest Brazil. Zootaxa bum, 2003), and later considered as a series of 2787:37–54. single pulsed notes (Pansonato et al., 2012). Arias, F., C.M. Carvalho, M.T. Rodrigues, and H. Zaher. We recommend that authors consider a note 2011b. Two new species of Cnemidophorus (Squamata: as the sound emitted during a single airflow Teiidae) of the C. ocellifer group, from Bahia, Brazil. Zootaxa 3022:1–21. cycle (McLister et al., 1995). In Pseudopalu- Borges-Nojosa, D.M., and E.M. Santos. 2005. Herpeto- dicola this note may be formed by single fauna da Area´ de Betaniaˆ e Floresta, Pernambuco. Pp. pulses (P. canga, P. facureae, P. hyleaustralis, 275–289 in F.S. Araujo,´ M.J.N. Rodal, and M.R.V. P. giarettai, and P. parnaiba), by concatenated Barbosa (Eds.), Ana´lise das Varia¸coes˜ da Biodiversidade do Bioma Caatinga. Ministe´rio do Meio Ambiente, pulses (P. mystacalis and P. boliviana), or by Brazil. sets of nonconcatenated pulses (species in Cardozo, D., and P. Sua´rez. 2012. Osteological descrip- Table 3). tion of Pseudopaludicola canga with implications for the Ecological and behavioral characteristics taxonomic position of this taxon. Zootaxa 3515:75–82. Cardozo, D., and L.F. Toledo. 2013. Taxonomic status of can also help to distinguish syntopic species. Pseudopaludicola riopiedadensis Mercadal de Barrio For instance, we found P. pocoto in syntopy and Barrio, 1994 (Anura, Leptodactylidae, Leiuper- with P. mystacalis, and both species are inae). Zootaxa 3734:571–582. morphologically indistinguishable. Neverthe- Carvalho, T.R. 2012. A new species of Pseudopaludicola less, P. mystacalis calls mostly during the day, Miranda-Ribeiro (Leiuperinae: Leptodactylidae: Anu- ra) from the Cerrado of southeastern Brazil with a whereas P. pocoto calls mostly during the distinctive advertisement call pattern. Zootaxa 3328:47– night, and the advertisement calls are easily 54. distinguished. Other researchers have also Duellman, W.E. 1970. The hylid frogs of Middle America. found different species of Pseudopaludicola Monograph of the Museum of Natural History of the University of Kansas 1:1–753. calling during different hours of the day at Duellman, W.E., and L. Trueb. 1986. Biology of different sites (Loebmann and Haddad, 2010; . The Johns Hopkins University Press, USA. Pansonato et al., 2013). Finally, the use of Dure´, M.I., E.F. Schaefer, M.I. Hamann, and A. Kehr. molecular tools will be important for under- 2004. Consideraciones ecologicas´ sobre la dieta, la reproduccion´ y el parasitismo de Pseudopaludicola standing species diversity and evolutionary boliviana (Anura, Leptodactylidae) de Corrientes, relationships within the genus, as relatively Argentina. Phyllomedusa 3:121–131. few species have been included in previous Frost, D.R. 2013. Species of the World: An molecular phylogenetic analyses (e.g., Pyron Online Reference. Available at http://research.amnh. and Wiens, 2011). org/herpetology/amphibia/index.html. American Muse- um of Natural History, New York, USA. Archived by Acknowledgments.—We thank I. Joventino and R. Avila´ WebCite at http://www.webcitation.org/6Gntyhlze on for data on geographic distribution and advertisement 22 May 2013. March 2014] HERPETOLOGICA 87

Giaretta, A.A., and K.G. Facure. 2009. , egg-laying of the semitaeniatus group from a semiarid area in behaviour, eggs and tadpoles of four sympatric species Northeastern Brazil. Zootaxa 2930:60–68. of Pseudopaludicola (Anura, Leiuperidae). Journal of Pereira, M.G., and L.B. Nascimento. 2004. Descri¸ca˜oda Natural History 43:995–1009. vocaliza¸ca˜o e do girino de Giaretta, A.A., and M.N.C. Kokubum. 2003. A new Lobo, 1994, com notas sobre a morfologia de adultos species of Pseudopaludicola (Anura, Leptodactylidae) (Amphibia, Anura, Leptodactylidae). Arquivos do from northern Brazil. Zootaxa 383:1–8. Museu Nacional 62:233–240. Gosner, K.L. 1960. A simplified table for staging anuran Pombal, J.P., Jr., V.A. Menezes, A.F. Fontes, I. Nunes, embryo and larvae with notes on identification. C.F.D. Rocha, and M.V. Sluys. 2012. A second species Herpetologica 16:183–190. of the casque-headed frog genus Corythomantis Haddad, C.F.B., and A.J. Cardoso. 1987. Taxonomia de (Anura, Hylidae) from northeastern Brazil, the distri- tresˆ espe´cies de Pseudopaludicola (Anura, Leptodacty- bution of C. greeningi, and comments on the genus. lidae). Pape´is Avulsos de Zoologia 36:287–300. Boletim do Museu Nacional 530:1–14. Kehr, A.I., and E.F. Schaefer. 2005. Description of the Pyron, R.A., and J.J. Wiens. 2011. A large-scale phylogeny tadpole of Pseudopaludicola boliviana (Anura: Lepto- of Amphibia with over 2,800 species, and a revised dactylidae). Herpetological Review 36:250–252. classification of extant frogs, salamanders, and caeci- Laufer, G., and J.M. Barreneche. 2008. Re-description of lians. Molecular Phylogenetics and Evolution 61:543– the tadpole of Pseudopaludicola falcipes (Anura: 583. Leiuperidae), with comments on larval diversity of the Roberto, I.J., D. Cardozo, and R.W. Avila.´ 2013. A new genus. Zootaxa 1760:50–58. species of Pseudopaludicola (Anura, Leiuperidae) from Limbaugh, B.A., and E.P. Volpe. 1957. Early develop- western Piauiı` State, Northeast Brazil. Zootaxa ment of the Gulf Coast Toad, Bufo valliceps Wiegmann. 3636:348–360. American Museum Novitates 1842:1–32. Rodrigues, M.T. 2003. Herpetofauna da Caatinga. Pp. Lobo, F. 1994. Descripcion´ de una nueva especie de 181–236 in M. Tabarelli and J.M.C. Silva (Eds.), Pseudopaludicola (Anura: Leptodactylidae), re- Biodiversidade, Ecologia e Conserva¸ca˜o da Caatinga. descripcion´ de P. falcipes (Hensel, 1867) y P. saltica Universidade Federal de Pernambuco, Brazil. (Cope, 1887) y osteologıa´ de las tres especies. ´ Cuadernos de Herpetologia 8:177–199. Tabarelli, M., and J.M.C. Silva. 2003. Areas e a¸coes˜ ´ Lobo, F. 1995. Ana´lisis filogene´tico del ge´nero Pseudo- prioritarias para a conserva¸ca˜o da Caatinga. Pp. 781– paludicola (Anura: Leptodactylidae). Cuadernos de 800 in I. Leal, J.M.C. Silva, and M. Tabarelli (Eds.), Herpetologia 9:21–43. Biodiversidade, Ecologia e Conserva¸ca˜o da Caatinga. Loebmann, D., and C.F.B. Haddad. 2010. Amphibians Universidade Federal de Pernambuco, Brazil. and reptiles from a highly diverse area of the Caatinga Toledo, L.F. 2010. Description of a new species of domain: Composition and conservation implications. Pseudopaludicola Miranda-Ribeiro, 1926 from the state Biota Neotropica 10:227–256. of Sa˜o Paulo, Southeastern Brazil (Anura, Leiuperidae). Lynch, J.D. 1989. A review of the leptodactylid frogs of Zootaxa 2681:47–56. the genus Pseudopaludicola in northern South America. Toledo, L.F., S. Siqueira, T.C. Duarte, A.C.P. Veiga- Copeia 1989:577–588. Menocello, S.M. Recco-Pimentel, and C.F.B. Haddad. Magalha˜es, F.M., A.K.B.P. Dantas, M.R.M. Brito, P.H.S. 2010. Description of a new species of Pseudopaludicola Medeiros, A.F. Oliveira, T.C.S.O. Pereira, M.H.C. Miranda-Ribeiro, 1926 from the state of Sa˜o Paulo, Queiroz, D.J. Santana, W.P. Silva, and A.A. Garda. Southeastern Brazil (Anura, Leiuperidae). Zootaxa 2013. Anurans from an Atlantic Forest-Caatinga 2496:38–48. ecotone in Rio Grande do Norte State, Brazil. Herpetology Notes 6:1–10. McLister, J.D., E.D. Stevens, and J. Bogart. 1995. Accepted: 26 October 2013 Comparative contractile dynamics of calling and Associate Editor: Christopher Raxworthy locomotor muscles in three hylid frogs. Journal of Experimental Biology 198:1527–1538. APPENDIX I Pansonato, A., D.H. Morais, R.W. Avila,´ R.A. Kawashita- Ribeiro, C. Strussmann, ¨ and I.A. Martins. 2012. A new Specimens Examined species of Pseudopaludicola Miranda-Ribeiro, 1926 ´ (Anura: Leiuperidae) from the state of Mato Grosso, Pseudopaludicola ameghini—BRAZIL: GOIAS: Baliza: Brazil, with comments on the geographic distribution of Fazenda Bandeirantes (CFBH 627; 643–647), MATO Pseudopaludicola canga Giaretta & Kokubum, 2003. GROSSO: Chapada dos Guimara˜es: Aldeia Velha (CFBH Zootaxa 3523:49–58. 114–117; 149–151), MATO GROSSO DO SUL: Nioaque Pansonato, A., C. Strussmann, J.R. Mudrek, and I.A. (CFBH 3431), Costa Rica: Corrego´ Morro Alto (CFBH Martins. 2013. Morphometric and bioacoustic data on 3476–3478; 3548–3550; 7281–7282), Bonito: Fazenda three species of Pseudopaludicola Miranda-Ribeiro, Paraıso´ (CFBH 5678), Paraıso´ (CFBH 7285), Inocencia:ˆ 1926 (Anura: Leptodactylidae: Leiuperinae) described Fazenda Lagoinha (CFBH 9449; 9452), Itaja´: Fazenda from Chapada dos Guimara˜es, Mato Grosso, Brazil, Lindos Campos (CFBH 9459). with the revalidation of Pseudopaludicola ameghini Pseudopaludicola canga—BRAZIL: PARA:´ Maraba´: (Cope, 1887). Zootaxa 3620:147–162. Serra dos Caraja´s (CFBH 157; 379–381). Passos, D.C., D.C. Lima, and D.M. Borges-Nojosa. 2011. Pseudopaludicola falcipes—BRAZIL: RIO GRANDE A new species of Tropidurus (Squamata, Tropiduridae) DO SUL: Sa˜o Sepe´: Granja das Capelas (CFBH 12026– 88 HERPETOLOGICA [Vol. 70, No. 1

12030; 12123–12133; 13137; 13150), Santa Vitoria´ do Pseudopaludicola pocoto—BRAZIL: RIO GRANDE Palmar: Praia do Cassino (CFBH 14056–14057). DO NORTE: Macaıba:´ Escola Agrıcola´ de Jundiaı´ Pseudopaludicola mineira—BRAZIL: MINAS GER- (AAGARDA 1065; 5584–5597; 8965). BRAZIL: PARA- AIS: Santana do Riacho: Serra do Cipo´ (CFBH 285; BA: Patos (LHUFCG 0072–0081). BRAZIL: PARAIBA:´ 9262–9267; 30894–30895). Aguiar: Serra de Santa Catarina (LHUFCG 0300–0305). Pseudopaludicola murundu—BRAZIL: SAO˜ PAULO: BRAZIL: CEARA:´ Jati: Sıtio´ Ba´lsamo (MNRJ 55887; Rio Claro: Itape´ (CFBH 8235–8243). Pseudopaludicola mystacalis—BRAZIL: CEARA:´ Uba- 55893). jara: Neblina (CFBH 15855–15856; 15915–15916), Vi¸cosa —BRAZIL: MATO GROSSO: do Ceara´:Sıtio´ Santo Mano (CFBH 20298–20300; 20303). Chapada dos Guimara˜es (CFBH 170–172; 14372–14378).