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Species Zachaenus Carvalhoi Izecksohn, 1983 (Anura, Cycloramphidae): an Endemic Frog from the Atlantic Forest of Southeastern Brazil

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Species Zachaenus Carvalhoi Izecksohn, 1983 (Anura, Cycloramphidae): an Endemic Frog from the Atlantic Forest of Southeastern Brazil Herpetology Notes, volume 12: 113-204 (2019) (published online on 1 January 2019) Filling knowledge gaps about the ‘Data Deficient’ species Zachaenus carvalhoi Izecksohn, 1983 (Anura, Cycloramphidae): an endemic frog from the Atlantic Forest of southeastern Brazil Jhonny J. M. Guedes1,*, Clodoaldo L. de Assis1, Camila M. Novaes2, Jorge A. Dergam3, and Renato N. Feio1 Abstract. Zachaenus carvalhoi is an endemic frog from the Atlantic Forest of southeastern Brazil. It is considered a rare species, being currently classified as ‘Data Deficient’ by the IUCN due to the shortage of information about its natural history, ecological requirements, distribution and population trends. In the present study, we aim to fill gaps in the current knowledge of this species by: updating its altitudinal distribution range; describing its release call; providing new natural history data; and describing its karyotype. During fieldwork in the Municipality of Cataguases, Minas Gerais State, we recorded individuals of Z. carvalhoi in three small forest fragments, one of them at only 230 m a.s.l., which now represents the lowest known altitudinal record for this species. In all occasions, we only recorded this frog in calling activity during rainy days, suggesting an opportunistic breeding strategy. Moreover, the karyotype of Z. carvalhoi (2n = 26) is similar to those of other species of the family Cycloramphidae, but it differs remarkably in morphology and fundamental number. The advertisement call presented differences in the spectral structure in comparison to descriptions from other populations. In conclusion, Z. carvalhoi seems to be an explosive breeder occurring along a wide altitudinal range (low- and highland Atlantic Forest), and physical barriers such as mountain chains may not be a constraint to its dispersal. Furthermore, this species represents a promising subject for investigations over both bioacoustics and cytogenetic studies. Keywords. Altitudinal distribution, bioacoustics, karyotype, natural history Introduction human-related impacts we now face a global decline of amphibian species (Blaustein et al., 1994; Collins Every year, dozens of anuran species are described and Storfer, 2003; Grant et al., 2016), the lack of such worldwide (Glaw and Köhler, 1998; Pimm et al., data may imply in severe consequences to biodiversity 2010; Frost, 2018), and more than 7,800 species have conservation and species management because it may been formally described so far (Frost, 2018). However, hamper a broader application of these data in basic and for many of these taxa, basic information on natural applied research, leading to inefficient conservation history and ecology are still missing (see Oliveira et planning (Bury, 2006). Therefore, providing such kind al., 2017). In a rapidly changing world, where due to of information is fundamental in decreasing current shortcomings, besides contributing to solve taxonomic, phylogenetic, biogeographic and conservation issues. The genus Zachaenus Cope, 1866 is composed of small leaf-litter frogs endemic to the Brazilian Atlantic 1 Departamento de Biologia Animal, Museu de Zoologia João Forest (Verdade et al., 2009), and currently comprises Moojen, Universidade Federal de Viçosa, Viçosa, Minas two valid species: Zachaenus parvulus (Girard, 1853) Gerais 36570-900, Brazil. and Z. carvalhoi Izecksohn, 1983 (Frost, 2018). The 2 Departamento de Biologia Geral, Laboratório de Biologia former occurs throughout Rio de Janeiro State, the Molecular de Insetos, Universidade Federal de Viçosa, northern region of São Paulo State, and the south- Viçosa, Minas Gerais 36570-900, Brazil. central region of Espírito Santo State (Verdade et al., 3 Departamento de Biologia Animal, Laboratório de Sistemática Molecular-Beagle, Universidade Federal de Viçosa, Viçosa, 2009; Oliveira et al., 2012). The latter is known only Minas Gerais 36570-900, Brazil. from eight localities, occurring along highland areas in * Corresponding author. E-mail: [email protected] the Mantiqueira mountain range in the State of Minas 114 Jhonny J. M. Guedes et al. Gerais, and Cariacica and Santa Teresa (type-locality) classified as type Aw in Köppen’s system, with mean in the State of Espírito Santo (Mollo-Neto et al., 2016). annual temperature varying between 22 and 24° C, The available information regarding Zachaenus mean annual precipitation around 1,300 and 1,600 mm carvalhoi relies basically on anecdotal reports about its (Alvares et al., 2013), with a rainy season from October distribution, defensive behaviour, diet and advertisement to April and a dry season from May to September (Sá call (Dayrell et al., 2006; Verdade et al., 2009; Motta et Júnior et al., 2012). The region is part of the Atlantic al., 2010; Moura et al., 2010; Salles and Maciel, 2010; Forest biome (sensu IBGE and MMA 2004), and was Coelho-Augusto et al., 2013; Guimarães et al., 2013; originally covered by montane and submontane seasonal Zocca et al., 2014; Mollo-Neto et al., 2015). Only semideciduous forests (Veloso et al., 1991). Nowadays, recently a more comprehensive study was published it has less than 12% of forest cover remaining, mostly (Mollo-Neto et al., 2016), dealing with its reproduction distributed in small fragments of secondary forest (SOS and geographic variation. Furthermore, based on the Mata Atlântica and INPE, 2018). low densities at which individuals are known to occur, Fieldwork.—We performed monthly surveys from threats imposed by habitat loss and fragmentation, and December 2012 to November 2013 in a locality called fast decline of habitat quality along the Atlantic Forest biome, Mollo-Neto et al. (2016) also suggested the Serra da Neblina/Sapecado (21.2091°S, 42.7558°W; reallocation of Z. carvalhoi to the ‘Near Threatened’ Datum WGS84; 912 m a.s.l.). Individuals of Z. category of the IUCN Red List, instead of the current carvalhoi were surveyed using five linear pitfall trap ‘Data Deficient’ status. In fact, threats such as habitat arrays (Ribeiro-Júnior et al., 2011), where each trap loss and fragmentation can severely reduce amphibian line was 50 m long, made of six 65 l buckets buried survival rates and result in population declines into the ground, set at 10 m intervals, and connected (Eterovick et al., 2005; Cushman, 2006; Tarvin et al., by a 50 cm tall drift fence of plastic canvas. The traps 2014), especially in forest dependent species. Therefore, remained active during five days in each month, and we the effects of such threats to amphibian conservation visited each trap line daily, during daytime. Moreover, should be carefully investigated. between 2013 and 2017, we randomly searched for So far, we are aware that Z. carvalhoi was not yet individuals by active search (Fitzgerald, 2012) in the studied cytogenetically, still lacks description of some surroundings of the area in which the traps were set, as parameters of its advertisement call, and its release well as in different forest fragments at the study site. call is unknown. Besides that, the lack of data about We conducted the searches during afternoon and night, distribution and/or abundance imposes especial issues through transects in the interior and border of such when determining in which category a species should fragments. be placed regarding its conservation framework (IUCN, Collected specimens (see Appendix I) were killed 2017). In this sense, herein we: (1) describe the release by intraperitoneal injection of Xylocaine® (lidocaine call of Z. carvalhoi; (2) update its altitudinal distribution hydrochloridae), tagged, and fixed in 10% formalin range; (3) provide new data about its natural history; before being transferred to a solution of 70% ethanol and (4) describe its karyotype. for storage. We identified the specimens as Z. carvalhoi based on the absence of dorsal folds and axillary Material and Methods patagium, as well as by the dark-brown coloration of its venter, with white dots of variable sizes (Izecksohn, Study site.—All data presented herein are based on 1983 “1982”). We deposited vouchers in the Museu specimens collected and/or observed during the course de Zoologia João Moojen (MZUFV), Universidade of a herpetological inventory in the Municipality of Federal de Viçosa, Viçosa Municipality, Minas Gerais Cataguases (21.3752ºS, 42.6855°W; Datum WGS84; State, Brazil. 179 m a.s.l.), Minas Gerais State, southeastern Brazil. For detailed information on the methodology used, as Acoustic analysis.—In the field, we recorded the well as other taxa recorded in the study site, see Guedes advertisement call of Z. carvalhoi using a Sony ICD et al. (2017) for lizards and amphisbaenians, and Assis PX721 digital recorder with an internal microphone and Feio (2017) for amphibians. (only the temporal parameters of these recordings were The study site varies in elevation from 170 to 1,200 used in further call analysis). To convert the calls from m, being drained by the Pomba river sub-basin, within MP3 to WAV format we used the software Adobe the Paraíba do Sul river basin. Climate is tropical, Audition CC 2018. In the laboratory, we simulated a Filling knowledge gaps about Zachaenus carvalhoi in Brazil 115 Figure 1. Individual Zachaenus carvalhoi collected in Cataguases Municipality, Minas Gerais State, southeastern Brazil (A) and giemsa-stained karyotype of the specimen (B). false axillary amplexus by gently pushing a collected spectral parameters we used: “Peak Frequency (Hz)”, specimen (MZUFV 18261; Fig. 1A), using thumb “Frequency 5% (Hz)”, and “Frequency 95% (Hz)”. and forefinger until a release call was emitted. In this Acoustic terminology follows Köhler et al. (2017). circumstance we used a Tascan DR-40 digital recorder We deposited all recordings at the Fonoteca Neotropical with an internal microphone, sampling rate of 48 kHz, Jacques Vielliard (FNJV) of the Universidade Estadual and resolution of 16 bits for recording. de Campinas, São Paulo, Brazil. We compared We measured spectral and temporal parameters using our recordings with other calls available in the Raven Pro 1.5 (Bioacoustics Research Program, 2014) literature, and their acronyms at FNJV are as follow: directly and respectively from the spectrogram and ZUFABC = Laboratório de Evolução e Diversidade oscillogram.
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