Herpetology Notes, volume 12: 957-960 (2019) (published online on 10 October 2019)

A new state record of the glassfrog Vitreorana baliomma (Anura: Centrolenidae), with notes on its reproductive biology

Barnagleison S. Lisboa1,2,*, Willams Fagner Soares dos Santos2, Selma Torquato da Silva2, Miriam Camargo Guarnieri1, and Tamí Mott2,3

The Neotropical family Centrolenidae Taylor, 1951 clutches laid on the surface of leaves suspended on over is composed of 156 charismatic species, commonly water (Haddad and Prado, 2005; Gouveia et al., 2012; known as glassfrogs (Frost, 2019). The genus Vitreorana Pontes et al., 2014). According to Pontes et al. (2014), Guayasamin, Castroviejo-Fisher, Trueb, Ayarzagüena, this glassfrog was misidentified as V. eurygnatha, but Rada, Vilà, 2009 was proposed based on molecular differ morphologically from its congeners recorded in data, and currently includes ten valid species distributed the Atlantic Forest by having a thin layer of iridophores in Argentina, Brazil, Colombia, Ecuador, Guyana, covering the stomach and intestines; males with Paraguay, Peru, Surinam and Venezuela (Guayasamin rudimentary nuptial excrescences formed by glands on et al., 2009; Frost, 2019). In Brazil, there are six species the dorsomedial surface of finger I and some accessorial usually associated with forest streams with occurrence glands along its periphery; kidneys, urinary bladder, and in the Atlantic Forest and in the Amazon, as well as testes lacking iridophores layer; and iris pattern flecked in the Cerrado domain (Ab’Saber, 1977): Vitreorana by lavender star-shape melanophores. baliomma Pontes, Caramaschi and Pombal Jr., 2014, V. eurygnatha (Lutz, 1925), V. franciscana Santana, The holotype (adult male MNRJ 46857) of Vitreorana Barros, Pontes and Feio, 2015, V. parvula (Boulenger, baliomma was collected at Mata de Cabruca, Fazenda 1895), V. ritae (Lutz, 1952), and V. uranoscopa (Müller, Novo Pau, municipality of Itamaraju, state of 1924) (Guayasamin et al., 2009; Frost, 2019). Bahia, northeastern Brazil, region influenced for the Vitreorana baliomma (Figure 1) is a medium-size Jequitinhonha River. Paratypes are from two localities: species for the genus (SVL 16.4–21.2 mm), typically Fazenda Palmeiras, municipality of Itapebi, state of found inside ombrophilous forests in the Atlantic Forest Bahia, and National Park Serra de Itabaiana (NPSI), domain, from 98 to 620 meters above sea level, associated municipality of Areia Branca, state of Sergipe (Pontes et with marginal vegetation along streams, with their egg al., 2014). Posteriorly, Assis et al. (2016) also recorded the species in the southeast Brazil, in Fazenda Limoeiro, municipality of Almenara, state of Minas Gerais, ca. 170 km northwest from the type locality. Herein, we provide a new state record of V. baliomma, along with data on its reproductive biology. On 29 April 2013, during a monitoring project of the 1 Programa de Pós-Graduação em Biologia , herpetofauna at Murici Ecological Station (MES), a Departamento de Zoologia, Centro de Biociências, federal Conservation Unit, municipality of Murici, state Universidade Federal de Pernambuco. Av. Professor Moraes of Alagoas (-9.2088 S -35.8602 W; datumWGS84; 463 Rego, 1235, 50670-901, Recife, Pernambuco, Brazil. m a.s.l.), four adult individuals of V. baliomma were 2 Seção de Herpetologia, Museu de História Natural, observed and collected by BSL and colleagues. The Universidade Federal de Alagoas. Praça Afrânio Jorge, individuals were found at night perched on the upper 57010–020, Maceió, Alagoas, Brazil. surface of leaves in the marginal vegetation (height from 3 Laboratório de Biologia Integrativa, Setor de Biodiversidade, 0.5 to 3 meters) in a permanent stream located inside Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas. Av. Lourival Melo Mota, 57072–970, ombrophilous forest. They were reproductively active Maceió, Alagoas, Brazil. (between April to September; Figure 1), with presence * Corresponding author. E-mail: [email protected] of calling males, females with apparent mature oocytes, 958 Barnagleison S. Lisboa et al.

Figure 1. Vitreorana baliomma in Murici Ecological Station, municipality of Murici, state of Alagoas, Brazil. (A) Male calling, (B) female with apparent mature oocytes, (C) amplectant pair, (D) egg clutch with embryos deposited on the upper (E) and underside leaf face (F). White arrow indicates one fossorial tadpole of the species in burial behaviour at substrate. (G) Habitat where the glassfrog was found. Photos by W.F.S.Santos (A and G) and B.S.Lisboa (B-F). A new state record of the glassfrog Vitreorana baliomma 959 amplectant pairs in axillary amplexus, and two egg on the original description of Pontes et al. (2014), clutches deposited in the upper and lower side of leaves which mentioned the species ooccurring in NPSI (see (height from 0.5 to 2.0 m; Figure 1D, E). Parental care appendix 1). behaviour was not observed. On 06 September 2013 we Vitreorana baliomma from Murici Ecological Station collected one egg clutch of V. baliomma deposited on represents the northernmost record in the distribution of the upper side of a leave (height of 0.7 meters above the species, extending approximately 237 km northeast water level) with 16 embryos in advanced stages of from the municipality of Areia Branca, Sergipe state, the development. Hatching tadpoles are fossorial, exhibiting nearest locality to the state of Alagoas, and ca. 955 km the behaviour of burring into the substrate (Figure 1F), as northeast of the municipality of Itamaraju, state of Bahia recorded for other Vitreorana species (e.g. Heyer, 1985; (type locality), the southernmost limit of the distribution Menin et al., 2009). The stream had rocky outcrops, known for this species (Figure 2). The presence of V. sandy substrate, and decaying leaves (water depth 0.10 baliomma in MES is the first record of the family – 0.27 m). Other anurans also were found using the Centrolenidae to the Pernambuco Center of Endemism, same stream: Aplastodiscus sp., granulosa, the most deforested and least known region of the Proceratophrys renalis, and Rhinella hoogmoedi. Atlantic Forest domain, located in the north portion of Vouchers were deposited in the Herpetological São Francisco river and including Alagoas, Pernambuco, Collection in the Museu de História Natural − Paraíba and Rio Grande do Norte states (Tabarelli Universidade Federal de Alagoas, Maceió, Brazil et al., 2006). Additionally, the Murici Ecological (adults MUFAL 11066-67, 11069-70; lot of tadpoles Station maintain endemic and threatened anurans (e.g. MUFAL 12049; ICMBio/SISBIO collection permit Crossodactylus dantei, Hylomantis granulosa, Ololygon #33507-1). The adult specimens were identified based muriciensis, and gyrinaethes) reinforcing its relevance for the conservation of in the Brazilian Atlantic Forest.

Acknowledgements. We thank José Neto, Ingrid Tiburcio, Gustavo Fajardo, Flávia Magalhães, Lahert Lobo, Cícero Côca and Junior Côca for assistance in the fieldwork; to Filipe Nascimento for valuable suggestions to manuscript and providing a pre-peer review. Also we thank Nelma Mendonça (IBAMA) and Jailton Fernandes (ICMBio) for their permission and fieldwork support for conducting this research. BSL thanks CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for scholar grant (132436/2012-4). TM thanks CNPq fellowship (309904/2015-3).

References

Ab’Saber, A.N. (1977): Domínios morfoclimáticos na América do Sul: primeira aproximação. Geomorfologia 52: 1–21. Frost, D.R. (2019): Species of the World: an Online Reference. Version 6.0. Available at: http://research.amnh.org/ herpetology/amphibia/index.html. Accessed on 25 April 2019. American Museum of Natural History, New York, USA. Gouveia, S.F., Faria, R.G., Rocha, P.A. (2012): Local distribution and notes on reproduction of Vitreorana aff. eurygnatha (Anura: Centrolenidae) from Sergipe, northeastern Brazil. Herpetological Bulletin 120: 16–21. Figure 2. Geographic distribution map of Vitreorana Guayasamin, J.M., Castroviejo-Fisher, S., Trueb, L., Ayarzagüena, baliomma. (BA): 1 – Fazenda Novo Pau Brasil, municipality J., Rada, M., Vilà, C. (2009): Phylogenetic systematics of of Itamaraju; 2 – Fazenda Palmeiras, municipality of Itapebi. glassfrogs (Amphibia: Centrolenidae) and their sister taxon (SE): 3 – National Park Serra de Itabaiana, municipality of Allophryne ruthveni. Zootaxa 2100: 1−97. Areia Branca. (MG): 4 – Fazenda Limoeiro, municipality of Haddad, C.F.B., Prado, C.P.A. (2005): Reproductive modes in Almenara. (AL): 5 – Murici Ecological Station, municipality and their unexpected diversity in the Atlantic forest of of Murici. Brazil. BioScience 55: 207−217. 960 Barnagleison S. Lisboa et al.

Heyer, W.R. (1985): Taxonomic and natural history notes of frogs Appendix 1 of the genus Centrolenella (Amphibia: Centrolenidae) from southeastern Brasil and adjacent Argentina. Papéis Avulsos de Material examined: Vitreorana baliomma from Zoologia 36: 1−21. the National Park Serra de Itabaiana, Areia Branca Menin, M., Lima, A.P., Rodriguez, D.J. (2009): The tadpole of municipality, Sergipe state, Brazil: MUFAL 12590; Vitreorana oyampiensis (Anura, Centrolenidae) in central MUFAL 12614; MUFAL 12641; MUFAL 12651; Amazonia, Brazil. Zootaxa 2203: 65−68. MUFAL 12655; MUFAL 12672; MUFAL 12678; Pontes, R.C., Caramaschi, U., Pombal, Jr., J.P. (2014): A remarkable MUFAL 12684; MUFAL 12829. new glass (Centrolenidae: Vitreorana) from the northeast Atlantic forest, Brazil. Herpetologica 70: 298–308. Tabarelli, M., Siqueira-Filho, J.A., Santos, A.M.M. (2006): A Floresta ao norte do rio São Francisco. In: Diversidade biológica e conservação da floresta Atlântica ao norte do rio São Francisco, p. 40−48. Pôrto, K.C., Cortez, J.A., Tabarelli, M., Ed., Brasília, Brasil, Ministério do Meio Ambiente.

Accepted by Diego Santana