A New Account for the Endangered Cerrado Rocket Frog Allobates Goianus (Bokermann, 1975) (Anura: Aromobatidae), with Comments on Taxonomy and Conservation
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Acta Herpetologica 11(1): 21-30, 2016 DOI: 10.13128/Acta_Herpetol-17491 A new account for the endangered Cerrado Rocket Frog Allobates goianus (Bokermann, 1975) (Anura: Aromobatidae), with comments on taxonomy and conservation Thiago Ribeiro de Carvalho1,2,*, Lucas Borges Martins1,2, Ariovaldo Antonio Giaretta1 1 Laboratório de Taxonomia, Sistemática e Evolução de Anuros Neotropicais. Faculdade de Ciências Integradas do Pontal, Universidade Federal de Uberlândia (UFU), Rua 20, 1600, 38304-402, Ituiutaba, Minas Gerais, Brasil. 2 Programa de Pós-Graduação em Biologia Comparada, Universidade de São Paulo, Departamento de Biologia/FFCLRP. Avenida dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brasil. *Corresponding author. E-mail: [email protected] Submitted on 2015, 11th November; revised on 2016, 23rd March; accepted on 2016, 26th March Editor: Paolo Casale Abstract. We report a new distributional record of Allobates goianus in Niquelândia (Goiás State, Central Brazil), and its rediscovery in Minaçu since the creation of the Serra da Mesa dam lake in 1997. Moreover, we describe the species advertisement call from Niquelândia, reporting on a new calling emission pattern for the species, plus we provide the first comprehensive definition, diagnosis, and interspecific comparisons of A. goianus based on our two newly col- lected additional specimens since its original description in the mid-1970s. Allobates goianus is compared with the 22 Allobates species known to occur in Brazil due to geographic proximity. Morphological, color, and acoustic traits diagnose A. goianus from all analyzed congeners, except A. brunneus and A. olfersioides. Our study draws attention to the importance of rediscovering A. goianus at the type locality (Chapada dos Veadeiros) aiming to properly address the species limits of the three Brazilian Allobates species (A. brunneus, A. goianus, and A. olfersioides) that are indistin- guishable with regard to phenotypic traits. The conservation status of A. goianus, endemic to the Cerrado of Central Brazil, is discussed as its natural habitats are under increased pressure due to habitat fragmentation in the Cerrado. Keywords. Advertisement call, Allobates brunneus, Allobates olfersioides, habitat fragmentation, threatened species, type locality. INTRODUCTION restricted extent of occurrence. Besides the type local- ity, A. goianus has been reported from only two addi- The genus Allobates currently comprises 51 spe- tional localities, both in Goiás State: i) Floresta Nacional cies distributed along South America on both sides of de Silvânia, a federal protected area (Bastos et al., 2003), the Andes, and Central America (Grant et al., 2006; from where its advertisement call was recently described Frost, 2015). Allobates goianus (Bokermann, 1975) was by Bastos et al. (2011), and ii) Minaçu (Serra da Mesa described from Central Brazil (Alto Paraíso de Goiás, region), where it was recorded in 1996 by Brandão and Chapada dos Veadeiros, Goiás State) and is regarded as Araújo (2008), before the creation of the Serra da Mesa a Cerrado endemic species. The species was recently dam lake, supposedly flooding its habitats according to reported as endangered according to the latest Brazilian these authors. list of threatened species (ICMBio, 2014), due to habi- Recent faunal inventories failed to locate A. goianus, tat loss, the increasing fragmentation of habitats, and including in the areas reported here (see Oda et al., 2009; ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah 22 Thiago Ribeiro de Carvalho et alii Morais et al., 2012; Santoro and Brandão, 2014). Further- sion and follows Duellman (1970); relative finger lengths follow more, this species has not been reported from its type Grant et al. (2006). Morphological and color traits were assessed locality either since its original description in the mid under a stereomicroscope; finger lengths were measured with a 1970’s (Santoro and Brandão, 2014). micrometric piece coupled to a stereomicroscope. Calls were recorded using a Sennheiser K6/ME66 direc- The purposes of this study were to report a new dis- tional microphone and a M-Audio Microtrack-II digital record- tributional record of A. goianus in Central Brazil, based er, and K6/ME67 directional microphones and Marantz PMD on two male specimens and its rediscovery in Minaçu 670 or PMD 671 digital recorders. Both recorders were set at a since the creation of the Serra da Mesa dam lake in 1997, sampling rate of 48 kHz and a sample size of 16 bits. Calls were based on a call recording. Furthermore, we describe the analyzed with Raven Pro 32-bit 1.5 beta version (Bioacoustics advertisement call of A. goianus from Niquelândia based Research Program, 2012) with the following settings: window on a larger sample size, and report on a pattern of calling size = 256 samples; window type = Hann; 3dB filter bandwidth emission other than the previously described by Bastos et = 270 Hz; overlap = 85%; hop size = 0.79 ms; DFT size = 1024 al. (2011); Also, we provide the first comprehensive defi- samples; grid spacing = 46.9 Hz. Temporal traits were measured from the oscillogram and spectral traits from the spectrogram. nition, diagnosis, and interspecific comparisons of A. goi- Dominant frequency was determined from the entire call using anus based on our two newly collected specimens since the “Peak Frequency” measurement function. Sound figures its original description by Bokermann (1975). were generated with Seewave package version 1.7.3 (Sueur et al., 2008) on R platform version 3.1.0 (R Core Team, 2014) with the following settings: window type = Hanning; window length MATERIALS AND METHODS = 512 samples (FFT); overlap = 85%. Definitions of call traits follow those of Cocroft and Ryan (1995) in most cases with ter- Fieldwork was conducted from November to December minological modifications in Carvalho et al. (2015). Note rate is 2014 in the Serra da Mesa region, municipalities of Niquelân- expressed in notes/sec, call rate in calls/min. See Appendix 1 for dia (14°21’50’’S, 48°30’17’’W; ca. 710 m a.s.l.) and Minaçu information about sound recordings and voucher specimens. (13°45’35’’S, 48°18’31’’W; ca. 900 m a.s.l.), Goiás State, Central Brazil (Fig. 1). These localities lie 110 km southwest and 95 km northwest from the type locality of A. goianus, respectively. Giv- RESULTS en that A. goianus is a Brazilian Cerrado endemic species, inter- specific comparisons were restricted to Allobates species occur- New distributional record ring in Brazil due to geographic proximity, i.e. the 18 species listed in the latest Brazilian amphibian list (Segalla et al., 2014): Our new distributional record of A. goianus in A. brunneus (Cope, 1887), A. caeruleodactylus (Lima and Cald- Niquelândia is located approximately 110 km southwest- well, 2001), A. conspicuus (Morales, 2002), A. crombiei (Morales, 2002), A. femoralis (Boulenger, 1884), A. flaviventris Melo-Sam- ward from its type locality, whereas the site where we paio, Sousa and Peloso, 2013, A. fuscellus (Morales, 2002), A. rediscovered the species in Minaçu is located approximate- gasconi (Morales, 2002), A. grilissimilis Simões, Sturaro, Peloso ly 95 km northwestward from the type locality (Fig. 1). and Lima, 2013, A. hodli Simões, Lima and Farias, 2010, A. marchesianus (Melin, 1941), A. masniger (Morales, 2002), A. nidicola (Caldwell and Lima, 2003), A. olfersioides (Lutz, 1925), Morphology and color patterns A. paleovarzensis Lima, Caldwell, Biavati and Montanarin, 2010, A. subfolionidificans (Lima, Sanchez and Souza, 2007), A. sum- The type series of A. goianus is composed of three tuosus (Morales, 2002), A. vanzolinius (Morales, 2002), with specimens: the holotype (MZUSP 76652, an adult female the addition of A. bacurau Simões, 2016, A. magnussoni Lima, with SVL 17.4 mm); and two paratypes (MZUSP 73706, a Simões and Kaefer, 2014, A. myersi (Pyburn, 1981), and A. juvenile with SVL 12.8 mm; and MZUSP 76651, probably tapajos Lima, Simões and Kaefer, 2015, which were not includ- a sub-adult with SVL 14.7 mm). Due to poor preserva- ed in this species list. New specimens are deposited in the Col- tion conditions, we decided not to seek for further evi- lection of Amphibians of the Museu de Biodiversidade do Cer- rado at the Universidade Federal de Uberlândia (AAG-UFU) dence for sexing these specimens (vocal slits or internal under the following accession numbers: AAG-UFU 5064–5065. morphology). Color of the holotype was fainted so that The type series of A. goianus is deposited at the Museu de Zoo- coloration comparisons were restricted to general colora- logia da Universidade de São Paulo (MZUSP) under the follow- tion of dorsum. Dorsal blotch was barely discernible and ing accession numbers: MZUSP 76652 (holotype), and MZUSP ill-outlined, but even so this color trait could be associ- 73706, 76651 (paratypes). ated with a lanceolate or hourglass-shaped blotch. Morphological and coloration characters follow the diag- Morphological features and size of our newly two col- nostic traits listed in Kok et al. (2013). Definitions and termi- lected adult male specimens from Niquelândia essentially nology are according to Grant et al. (2006). Snout-vent length matched the holotype description of A. goianus (Boker- (SVL) was measured with digital calipers of 0.01 mm preci- A new account for Allobates goianus 23 Fig. 1. Distribution map of Allobates goianus (circles) and A. brunneus (triangles) in the Brazilian Cerrado. Circles: (1) Alto Paraíso de Goiás, Chapada dos Veadeiros (type locality); (2) Minaçu (Brandão and Araújo, 2008; present study); (3) Niquelândia (present study); (4) Silvânia (Bastos et al., 2003); Triangles: (1) Chapada dos Guimarães [collection sites 1–3 in Lima et al. (2009)], presumably the type locality [a site that lies approximately 30 miles northeast from Cuiabá according to the original description: Cope (1887)]; (2) Other record sites in Chapada dos Guimarães [collection sites 4–9 in Lima et al. (2009)]. Brazilian state abbreviations: GO (Goiás), MT (Mato Grosso).