Herpetology Notes, volume 12: 675-679 (2019) (published online on 30 June 2019)

New record and geographic distribution of caramaschii Cruz, Nunes, and Juncá, 2012 in the state of Piauí, northeastern Brazil (Anura: )

Antonia Joyce S. Santos¹, Claylton A. Costa¹, Felipe P. Sena¹, Kássio C. Araújo², and Etielle B. Andrade1,*

The genus Proceratophrys Miranda-Ribeiro, 1920 The P. cristiceps group, characterized by the absence of currently comprises 41 species distributed throughout palpebral appendages, rostral or post-ocular elevations, South America (Frost, 2019). In Brazil, the genus has currently comprises 16 species (Frost, 2019): P. ararype a wide geographic distribution occurring in different Mângia, Koroiva, Nunes, Roberto, Ávila, Sant’Anna, phytophysiognomies, from open areas of the Caatinga Santana and Garda, 2018; P. aridus Cruz, Nunes and and Cerrado (e.g., Martins and Giaretta, 2011; 2013; Juncá, 2012; P. bagnoi Brandão, Caramaschi, Vaz-Silva Cruz et al., 2012; Brandão et al., 2013) to the forested and Campos, 2013; P. branti Brandão, Caramaschi, Vaz- areas of the Atlantic Forest and Amazon (e.g., Giaretta et Silva and Campos, 2013; P. caramaschii Cruz, Nunes al., 2000; Napoli et al., 2011; Dias et al., 2013; Mângia and Juncá, 2012; P. carranca Godinho, Moura, Lacerda et al., 2014; Barros et al., 2016). and Feio, 2013; P. concavitympanum Giaretta, Bernarde Most species of the genus Proceratophrys can be and Kokubum, 2000; P. cristiceps; P. cururu Eterovick clustered into four species groups — P. appendiculata and Sazima, 1998; P. dibernardoi Brandão, Caramaschi, (Günther, 1873), P. bigibbosa (Peters, 1872), P. boiei Vaz-Silva and Campos, 2013; P. goyana (Miranda- (Wied-Neuwied, 1824) and P. cristiceps (Müller, 1883) Ribeiro, 1937); P. huntingtoni Ávila, Pansonato and (Giaretta et al., 2000; Kwet and Faivovich, 2001; Strüssmann, 2012; P. moratoi (Jim and Caramaschi, Prado and Pombal, 2008; Cruz and Napoli, 2010; Dias 1980); P. rotundipalpebra Martins and Giaretta, 2013; et al., 2013) — but some species are not associated P. strussmannae Ávila, Kawashita-Ribeiro and Morais, with any of these groups (Frost, 2019): P. minuta 2011; and P. vielliardi Martins and Giaretta, 2011. Napoli, Cruz, Abreu and Del Grande, 2011; P. redacta Recently, morphological variations observed in Teixeira, Amaro, Recoder, Vechio and Rodrigues, Northeastern populations of Proceratophrys individuals 2012; and P. schirchi (Miranda-Ribeiro, 1937). Of the associated to P. cristiceps resulted in the description aforementioned species groups, only the P. bigibbosa of P. aridus and P. caramaschii (Cruz et al., 2012). group is considered monophyletic, being supported by Proceratophrys caramaschii differs morphologically molecular data (Pyron and Wiens, 2011; Teixeira Jr. et from P. cristiceps by the absence of tubercles on the al., 2012; Dias et al., 2013) and morphological characters snout and on the head, presence of one interocular (e.g., Kwet and Faivovich, 2001; Dias, 2018). transverse crest of tubercles, inner part of metacarpal tubercle bigger than the outer and the presence of several blotches on venter (Cruz et al., 2012). Proceratophrys caramaschii is registered only for the extreme north of 1 Grupo de Pesquisa em Biodiversidade e Biotecnologia do the Planalto da Ibiapaba and coastal region of the states Centro-Norte Piauiense (BIOTECPI), Instituto Federal do of Ceará (type locality in the city of Fortaleza) and Piauí, Piauí, Campus Pedro II, Rua Antonino Martins de Andrade Northeastern of Brazil (Roberto et al., 2013; Andrade et 750, Engenho Novo, Pedro II, Piauí 64255-000, Brazil. al., 2014; Nunes et al., 2015; Araújo et al., 2018), with 2 Programa de Pós-Graduação em Ecologia e Recursos Naturais, no record for other localities in the state of Piauí. Herein Bloco 902, Centro de Ciências, Universidade Federal do Ceará – UFC, Campus do PICI, Av. Humberto Monte, s/n, we report a new record of P. caramaschii for the central- 60455-760 Fortaleza, Ceará, Brazil. north region of the state of Piauí, Northeastern Brazil, * Corresponding author. E-mail: [email protected] updating the geographical distribution of the species. 676 Antonia Joyce S. Santos et al.

Figure 1. (A) lateral and (B) ventral views of Proceratophrys caramaschii (URCA 14205; SVL = 54.2 mm) recorded and collected in the municipality of Pedro II, state of Piauí, Northeastern Brazil, and (C) in which specimens were found.

Materials and Methods m above sea level, in the Serra dos Matões, presenting a dry and mild climate compared to other municipalities Fieldwork was conducted on the 5th of March 2018 in of Piauí (Milanez and Puppim, 2009). It is a semiarid temporary ponds along the highway PI-216, municipality region with transitional areas between the Cerrado and of Pedro II, state of Piauí (4.4808º S, 41.4131º W; the Caatinga biomes, with the predominance of species Datum WGS84; 520 m elevation). The municipality typical of the Cerrado (Barros et al., 2014). of Pedro II is located in the central-north region of the Six males of P. caramaschii were collected and are state of Piauí, Northeastearn Brazil, approximately 600 housed in the Coleção Biológica do Instituto Federal New record and geographic distribution of Proceratophrys caramaschii 677

far from the temporary ponds formed by the rainwater (Figure 1C). Our data corroborate the results of Nunes et al. (2015), who affirm that the reproduction of this species is mainly associated to the rainy season in the region (January to May). Data on the reproductive biology of P. caramaschii are scarce and tadpoles are currently undergoing description (in prep.). The advertisement call of P. caramaschii is composed by one multipulsed note with 39–51 pulses (44 ± 3.55; 7 calls) and dominant frequency of 0.947 kHz (no variation found; 7 calls), emitted in series of 5–7 calls. Call duration varied from 496 to 559.20 milliseconds (ms) (516.79 ± 23.31 ms; 7 calls) with call intervals from 447.70 to 611.20 ms (525.98 ± 70.57 ms; 6 intervals). Rate of pulse emission varied from 39 to 51 pulses/ second (44.43 ± 3.55; 7 calls), with pulse duration of 4.20–9 ms (7.01 ± 0.86 ms; 7 calls; 316 pulses) and pulse interval of 1.90–5.90 ms (3.99 ± 0.80 ms; 7 calls, Figure 2. Oscillogram with detail in some pulses (A), 312 pulse intervals). Bioacoustic data presented here spectrogram (B) and power spectrum (C) of the advertisement (Figure 2) are similar to those reported by Nunes et al. call of Proceratophrys caramaschii (URCA 14205; SVL = (2015) for the populations of P. caramaschii recorded in 54.2 mm), recorded in the municipality of Pedro II, state of the municipalities of Ubajara and Viçosa do Ceará, both Piauí, northeastern Brazil. in the state of Ceará. We recorded P. caramaschii about 330 km in a straight line southwest from the type locality (Figure 3), the municipality of Fortaleza (Nunes et al., 2015), do Piauí, Campus Pedro II (CBPII 001–004) and in the increasing the distribution of the species about 90 km Coleção Herpetológica da Universidade Regional do in a straight line southwest from its nearest previous Cariri (URCA 14205–14206), municipality of Crato, state of Ceará. The specimens were identified according to the morphological characteristics listed by Cruz et al. (2012) and characters related to the eyelids according to Brandão et al. (2013). The advertisement call of one of the specimens (URCA 14205) was recorded with a Tascam DR-05 digital recorder coupled to a CSR HT-81 directional microphone, at a sample rate of 44.1 kHz and sample size of 16 bits. The call was analysed using the software SoundRuler, version 0.9.6 (Bee, 2004; Gridi-Papp, 2004), with Fast Fourier Transform length (FFT) of 256 points, Hanning window, and 90% of overlap. Quantitative features are given as range followed by mean, standard deviation, and sample size in parenthesis. The snout-vent length (SVL) of this specimen was taken with a digital calliper with 0.1 mm precision. Figure 3. Geographic distribution of Proceratophrys caramaschii in the northeastern region of Brazil. Circle = Results and Discussion municipality of Fortaleza, state of Ceará (type locality of the species); Triangle = municipality of Ubajara, state of Ceará Males of P. caramaschii (Figure 1A–B) vocalized in (region of the Planalto da Ibiapina); Square = municipality great numbers emitting antiphonal calls (call/response), of Ilha Grande (coastal region of the state of Piauí); Star = especially after rain. The individuals were found calling municipality of Pedro II, central region of the state of Piauí among the vegetation, on the wet soil, about two meters (new record). 678 Antonia Joyce S. Santos et al. record in the municipality of Ubajara (Nunes et al., Odontophrynidae), with description of two new species without 2015), both in the state of Ceará, and about 175 km in eyelid appendages from northeastern Brazil. South American a straight line southward from the coastal region of the Journal of Herpetology 7(2): 110–122. Dias, P.H.S. (2018). The tadpole of state of Piauí (Roberto et al., 2013; Andrade et al., 2014; (Peters, 1872) (Anura: Odontophrynidae), with a description Nunes et al., 2015; Araújo et al., 2018). This new record of its buccopharyngeal morphology and proposal of novel corresponds to the southernmost known occurrence synapomorphies for the P. bigibbosa species group. Copeia 106: of the species. The present record reveals the need to 86–93. conduct fauna surveys, especially for , given Dias, P.H.S., Amaro, R.C., Carvalho-e-Silva, A.M.P.T., Rodrigues, that there is no information on the species in the region. M.T. (2013): Two new species of Proceratophrys Miranda- The municipality of Pedro II is considered a touristic Ribeiro, 1920 (Anura; Odontophrynidae) from the Atlantic forest, with taxonomic remarks on the genus. Zootaxa 3682: route, mainly by the formation of waterfalls during 277–-304. the rainy season, and a region quite exploited by the Frost, D.R. 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Accepted by Pedro Pinna