Herpetology Notes, volume 13: 573-577 (2020) (published online on 26 July 2020)

Update on the geographic distribution of three poorly known species in the Mantiqueira mountain range

Edelcio Muscat¹, Daniel Stuginski¹, Ivan Nunes², Itamar Martins³, Guilherme Augusto-Alves4,5, Stenio Eder Vittorazzi6,7, Luís Felipe Toledo4, and Matheus de Toledo Moroti1,8,*

In megadiverse countries, such as , the species the most speciose mountain areas for anurans in South diversity (the Linnean shortfall), as well as their America (Silva et al., 2018). geographical distributions (the Wallacean shortfall), According to estimates, only 11-16% of the Atlantic remain poorly known for most taxa (Bini et al., 2006; Forest’s original coverage remains, composed mainly Andreone et al., 2008). There are more than 650 of small and isolated fragments (Ribeiro et al., 2009; species in the Atlantic Forest biome (LF Pompeu et al., 2018; Peixoto et al., 2020). In the Toledo, unpublished data). In the Mantiqueira mountain Monte Verde plateau of the Mantiqueira mountains, range alone, 234 species are recorded, corresponding the original vegetation was replaced by grazing land, to nearly ~37.5 % of the known for the monoculture reforestation and constructions, or has biome (Silva et al., 2018). Of these, 88 species are suffered intense logging (Golfari, 1975). This scenario endemic to this mountain range (Silva et al., 2018). The is even more worrisome as amphibians are considered high diversity and endemism make the Mantiqueira the most threatened vertebrates on the planet (Stuart et mountains a hotspot. They are also considered one of al., 2004). Factors such as fragmentation, habitat loss, climate change, diseases as chytridiomycosis, and the introduction of exotic species are the main causes of this decline (Stuart et al., 2004; Carvalho et al., 2017). Thus, there is an urgent need for monitoring amphibian 1 Projeto Dacnis, São Francisco Xavier, São Paulo, Brazil. populations, especially those data deficient species, 2 Laboratório de Herpetologia, Universidade Estadual since these could be threatened and not protected Paulista (UNESP), Campus do Litoral Paulista, Instituto de (Haddad, 2008). Biociências, São Vicente, São Paulo, Brazil. 3 Laboratório de Zoologia, Universidade de Taubaté (UNITAU), We present new records on the geographic distribution Taubaté, São Paulo, Brazil. of three poorly known, endemic anurans of the 4 Laboratório de História Natural de Anfíbios Brasileiros Mantiqueira mountain range: magalhaesi (LaHNAB), Departamento de Biologia , Instituto de (Bokermann, 1964); Proceratophrys itamari Mângia, Biologia, Universidade Estadual de Campinas (UNICAMP), Santana, Cruz and Feio, 2014; and Megaelosia Campinas, São Paulo, Brazil. boticariana Giaretta and Aguiar 1998. The new 5 Programa de Pós-Graduação em Ecologia, Instituto de records were made during herpetofauna monitoring, Biologia, Unicamp, Campinas, mostly by Projeto Dacnis researchers, in two forest São Paulo, 13083-862, Brazil. 6 Programa de Pós-Graduação em Genética, Departamento de fragments in the Mantiqueira mountain range: RPPN Genética, Universidade Federal do Paraná (UFPR), Centro Fazenda Renópolis, municipality of Santo Antônio Politécnico, Jardim das Américas, 81531-990, Curitiba, do Pinhal, state of São Paulo, Brazil (-22.805013, - Paraná, Brazil. 45.624407, WGS-84) and São Francisco Xavier (SFX), 7 Departamento de Ciências Biológicas, Faculdade de Ciências municipality of São José dos Campos, state of São Biológicas, Agrárias e da Saúde, Universidade do Estado de Paulo, Brazil (-22.903024, -46.018145, WGS-84). Mato Grosso, Tangará da Serra, MT, Brazil. The first area is a “Reserva Particular do Patrimônio 8 Laboratório de Síntese em Biodiversidade, Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Natural” (RPPN) that has submontane and montane Universidade Federal do Mato Grosso do Sul (UFMS), Atlantic forests, with rocky outcrops and plenty of Campo Grande, Mato Grosso do Sul, Brazil. streams. Its elevation ranges from 750 to 1800 m a.s.l. * Corresponding author. E-mail: [email protected] The area is inserted in the Campos do Jordão plateau. 574 Edelcio Muscat et al.

The second area (SFX) is similar to RPPN Renópolis, according to the description of the species. The records also with many rocky outcrops, but its streams are for P. itamari (Fig. 1) in Santo Antônio do Pinhal extend larger, with stronger currents. It is in the Monte Verde the species’ range by approximately 9 km southeast plateau and has a fragmented landscape composed of of their type locality, Campos do Jordão, state of São primary and secondary forest fragments between 630 Paulo, Brazil (Mângia et al., 2014). SFX records extend and 2023 m a.s.l. Both areas are 42 km away from each the species range 59 km from the type locality and 42 other and are part of the southern Mantiqueira mountain km from the Santo Antônio do Pinhal record. In addition range complex. The voucher specimens were deposited to these locations, P. itamari has also been registered in in the scientific collections of Universidade Estadual de the municipality of , state of Campinas (ZUEC) municipality of Campinas, Coleção (Mângia et al., 2014), 61 km from its type locality. In Científica do Laboratório de Zoologia da Universidade addition to these locations, P. itamari has already been de Taubaté (CCLZU) municipality of Taubaté and found in the municipality of São Bento do Sapucaí (no Herpetology Collection (HCLP) of the Universidade voucher) and Parque Natural Municipal do Trabiju, Estadual Paulista, municipality of São Vicente, all in the municipality of (CCLZU-1482), state of São Paulo, Brazil. both in the state of São Paulo (I Martins, unpublished We found an individual of Proceratophrys itamari data). Proceratophrys itamari is commonly seen in SFX in RPPN Fazenda Renópolis (CCLZU-3437) in and RPPN Fazenda Renópolis. It has nocturnal habits November 2018. We recorded the same species in SFX and is found in forest areas above 1200m a.s.l. The in August 2019 (ZUEC-AMP 24829). We confirmed the species has an explosive reproduction and is apparently identification through the bioacoustic comparison of the not associated with rain. Tadpoles can be found in advertisement call and with the morphological diagnosis permanent and temporary streams.

Figure 1. Map of the known geographic distribution of Proceratophrys itamari Mângia, Santana, Cruz and Feio, 2014 in southeastern Brazil. Abbreviation of states: MG = Minas Gerais; SP = São Paulo. Update on the geographic distribution of three poorly known frog species 575

In November 2018, Itamar Martins also found a IUCN Red List of Threatened Species (Rocha et al., specimen of Hylodes magalhaesi in the RPPN Fazenda 2010) and receives the same status in the Red Book of Renópolis (CCLZU-3457). We recorded the same species Threatened Brazilian Fauna (ICMBio, 2018). Hylodes in SFX in July 2019 (HCLP-A123). We confirmed the magalhaesi is a seldom seen species and vocalizes identification through the bioacoustic comparison of the mainly during rainy season in SFX. Apparently, it is not advertisement call and with the morphological diagnosis an abundant species in SFX. Interestingly, species of according to the description of the species. The records Hylodes vocalize during the day, but in SFX we hear H. for H. magalhaesi (Fig. 2) in Santo Antônio do Pinhal magalhaesi vocalizing mostly at night, from under the extend the species’ range by approximately 9 km rocks in small streams. southeast of their type locality, Campos do Jordão, state In December 2018 we captured a Megaelosia of São Paulo, Brazil (Bokermann, 1964). SFX records boticariana tadpole in SFX (ZUEC-AMP 24587). The extend the species range 59 km from the type locality specimen was found in a small natural pool about 80 and 42 km from the Santo Antônio do Pinhal record. cm deep, formed along a rocky stream at approximately H. magalhaesi was recorded for the first time out of its 1200 m a.s.l. In December 2019, an adult was captured type locality in the district of Monte Verde, municipality on the rocks at the same stream’s bank. This specimen of Camanducaia, state of Minas Gerais, 48km from the was photographed and released in the same place. original site (Toledo et al., 2006). Our records represent The species identification of the tadpole was made two new localities within the state of São Paulo. They by genetic distancing (Kumar et al., 2018) using the are, respectively, the second and third most distant mitochondrial rRNA 16S gene (1434 bp; GenBank records away from the species’ type locality. Hylodes MT409034) extracted from the specimen ZUEC-AMP magalhaesi is classified as data deficient (DD) in the 24587 and compared to a sequence of M. boticariana

Figure 2. Map of the known geographic distribution of Hylodes magalhaesi (Bokermann 1964) in southeastern Brazil. Abbreviation of states: MG = Minas Gerais; SP = São Paulo. 576 Edelcio Muscat et al. from the type locality. The genetic distance between The state of São Paulo concentrates Brazil’s greatest these two specimens was 0.006%, which indicates number of amphibian studies, and new efforts in this that they are representatives for the same species. This region have been revealing important finds, such as record extends the distribution of M. boticariana by species that have not yet been described, distribution around 62 km to the northeast of the type locality in the extensions (Martins, 2010; Moroti et al., 2019), and Itapetininga Forest Park, municipality of Atibaia, state the presence of species that are still largely unknown to of São Paulo (Giaretta and Aguiar, 1998). It is the first science (Rotenberg et al., in press). Peixoto et al. (2020) record away from the type locality (Fig. 3). Megaelosia state that the Poços de Caldas, Campos de Jordão, boticariana is classified as data deficient (DD) in the and Boa Vista plateau ranges are priority areas for Serra IUCN Red List of Threatened Species (Cruz and da Mantiqueira conservation. The Monte Verde plateau, Telles, 2010) and receives the same status in the Red however, is still an area that needs to be sampled further. Book of Threatened Brazilian Fauna (ICMBio, 2018). We suggest that this region should also be considered Megaelosia species can be considered one of the most strategic to conservation and that the levels of protection enigmatic species that occur in Mantiqueira mountains. it receives be increased. Tadpoles of M. boticariana are commonly found in These three anuran species require attention in relation backwaters of lotic environments in high areas, depths to their conservation due to their high habitat specificity ranging from 10cm to 80cm. So far, we have only seen (preserved highland streams). The projections for four adult individuals. All individuals were found at habitat loss in the Mantiqueira biogeographical units are approximately 19:00 h, on top of rocks near or at the concerning because they point to a high probability of edge of streams. a marked increase in the number of threatened species over a short period of time, since the area’s current

Figure 3. Map of the known geographic distribution of Megaelosia boticariana Giaretta and Aguiar 1998 in southeastern Brazil. Abbreviation of states: MG = Minas Gerais; SP = São Paulo. Update on the geographic distribution of three poorly known frog species 577 protection systems are ineffective (Peixoto et al., 2020). icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/ Future studies that focus on understanding the population publicacoes135diversas/livro_vermelho_2018_vol1.pdf. dynamics and respective distributions of these poorly Accessed on 25 February 2020. Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K. (2018): known species will be key for elaborating conservation MEGA X: Molecular Evolutionary Genetics Analysis across strategies for the anurans of the Mantiqueira mountain computing platforms. Molecular Biology and Evolution 35: range. 1547–1549. Mângia, S., Santana D.J., Cruz, C.A.G., Feio, R.N. (2014): Acknowledgments. The authors thank Projeto Dacnis for its Taxonomic review of Proceratophrys melanopogon (Miranda- support. We thank the owners Renata de Albuquerque Pinheiro Ribeiro, 1926) with description of four new species (Amphibia, and Patrícia Pupo do Prado for allowing us to study at the private Anura, Odontophrynidae). Boletim do Museu Nacional 531: property in SFX (Reserva das Araucárias) and for encouraging 1–33. studies in the area. This study was registered at Sistema Nacional Martins, I.A. (2010): Natural history of luederwaldti de Gestão do Patrimônio Genético e do Conhecimento Tradicional (Amphibia: Strabomantidae: Holoadeninae) in southeastern of Associado (SisGen # A345A1D). We thank ICMBio for the Brazil. Zoologia-Curitiba 27(1): 40–46. licenses granted (27745-19; 72484). MTM is grateful to CAPES Moroti, M.T., Pedrozo, M., Ceron, K., Soares, C.P., Machado, for its scholarship. Financial support to LFT and GAA was I.F. (2019): Composition of anuran species in Parque Natural provided by grants from the São Paulo State Research Foundation Municipal Augusto Ruschi in Paraíba Valley, São Paulo, Brazil. (FAPESP #2016/25358-3; #2019/03170-0) and the National Herpetology Notes 12: 291–303. Council for Scientific and Technological Development (CNPq Peixoto, M.A., Guedes, T.B., Silva, E.T., Feio R.N., Romano, P.S.R. #300896/2016-6). IAM received grants (FAPESP #2013/50741-7 (2020): Biogeographic tools help to assess the effectiveness and # 2018/00694-6). of protected areas for the conservation of anurans in the Mantiqueira mountain range, Southeastern Brazil. Journal for References Nature Conservation 54: 125799. Pompeu, P.V., Fontes, M.A.L, Mulligan, M., Bueno, I.T., Siqueira, Andreone, F., Cox, N.A., Glaw, F., Köhler, J., Rabibisoa, N.H., M.F., Acerbi Jr, F.W., Kamino, L.H.Y., Waterloo, M.J., Randriamahazo H., Raxworthy, C., Stuart, S.N., Vences, M. Bruijnzeel, L.A. 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