New records of Dispas albifrons (Serpentes, Dipsadidae) in the Atlantic Forest of Minas Gerais, Brazil, with morphological data

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1 Herpetology Notes, volume 11: (2018) (published online on 27 September 2018) New records of Dispas albifrons (Serpentes, Dipsadidae) in the Atlantic Forest of Minas Gerais, Brazil, with morphological data Adriano L. Silveira 1, *, Lucas S. V. B. Ribeiro 2, Tiago T. Dornas 2 and Taís N. Fernandes 3 Abstract. The snake Dipsas albifrons (Sauvage, 1884) is endemic to the Atlantic Forest in Brazil, occurring from the state of Bahia south to the state of Santa Catarina. Disjunct populations of the species are known, with a previous record for the state of Minas Gerais. New records are presented for Minas Gerais, with areas of the geographic distribution of D. albifrons occurring in the mountain complexes of the Planalto Meridional (Southern Plateau) of the Serra do Espinhaço and the Quadrilátero Ferrífero (Iron Quadrangle), as well as Vale do Rio Doce in the eastern part of the state. Morphometric and meristic data for specimens from Minas Gerais are presented. Keywords: Geographic distribution, Quadrilátero Ferrífero, Serra do Espinhaço, Vale do Rio Doce, pholidosis, morphometry Introduction Since its original description, the snake Dipsas albifrons (Sauvage, 1884) remained poorly known until the review by Passos et al. (2005), who defined its taxonomic identity and presented data on its morphological variation and geographic distribution. Dipsas albifrons occurs in the Atlantic Forest of southeastern and southern Brazil in the states of Espírito Santo, Rio de Janeiro, Paraná and Santa Catarina and on oceanic islands of the state of São Paulo (Passos et al., 2005), continental Sao Paulo (Sazima and Muscat, 2006), southern Bahia (Argolo, 2004), and Minas Gerais (Silveira et al., 2010), with an extensive gap in its distribution along the continental portion of the state of Sao Paulo. Most of the geographic distribution of Dispas albifrons (see Passos et al., 2005) corresponds to Ombrophilous Forest formations (IBGE, 2004). According to Silveira et al. (2010), it is probable that populations of D. albifrons isolated in Seasonal Semidecisuous Forest fragments of the region of Itabirito are subject to more local extinctions due to demographic, genetic and stochastic effects. The species is considered to be locally rare (Silveira et al., 2010). In the latest evaluation of the conservation status 1 Biótica Estudos Ambientais, Caixa Postal 2020, CEP , Belo Horizonte, Minas Gerais, Brazil 2 Amplo Engenharia e Gestão de Projetos Ltda., Rua Engenheiro Carlos Antonini 37, São Lucas, CEP , Belo Horizonte, Minas Gerais, Brazil 3 Vale S. A., Mina de Águas Claras, prédio 1, térreo, Avenida Doutor Marco Paulo Simon Jardim, CEP , Nova Lima, Minas Gerais, Brazil * Corresponding author. biosilveira@yahoo.com.br Figure 1. Dipsas albifrons ( 3636) in life, collected in Floresta Estadual do Uaimii, Ouro Preto, Minas Gerais. Photo by Adriano Silveira.

2 810 Adriano L. Silveira et al. Figure 2. Dipsas albifrons ( 3636) preserved in alcohol, collected in Floresta Estadual do Uaimii, Ouro Preto, Minas Gerais. Specimen in dorsal (A) and ventral (B) views; head in dorsal (C) and lateral (D) views. Photos by Adriano Silveira. of the reptiles of Minas Gerais, Dipsas albifrons was categorized as Data Deficient (DD) (Fundação Biodiversitas, 2007; Martins et al., 2008), which highlights the need for a better understanding of the species regional geographic distribution. The present work provides new records for D. albifrons from areas of Seasonal Semideciduous Forest in the Atlantic Forest of Minas Gerais. Materials and Methods Collected specimens were preserved following standard methods (Franco and Salomão, 2002) and deposited as voucher material in Coleção Científica de Serpentes of the Fundação Ezequiel Dias (). Collections were previously authorized by Instituto Chico Mendes de Conservação da Biodiversidade (authorization ) and by Instituto Estadual de Florestas MG (authorization 080/2016). The diagnosis of the taxon was based on the work of Passos et al. (2005). Scale counts followed the terminology of Peters (1964), with some adaptations, and the ventral scale counting method of Dowling (1951). Measurements were made with an analogue calliper to ± 0.02 mm, with the exception of snout-vent length, which was measured with a meter tape to ± 1 mm. For scale counts a slash (/) was used to separate counts on the left and right sides (L/R) and plus signs (+) were used to indicate temporal scales from anterior to posterior within a series. Specimen 4759 was not included in the analysis because it was badly damaged. The collections consulted were Coleção Científica de Serpentes of the Fundação Ezequiel Dias (), Coleção de Répteis of the Universidade Federal de Ouro Preto () and Coleção Herpetológica of the

3 New records of Dispas albifrons in the Atlantic Forest of Minas Gerais, Brazil 811 Museu de História Natural of Pontifícia Universidade Católica de Minas Gerais (), all located in Belo Horizonte, Minas Gerais, Brazil. For the definition of mountain complexes in Minas Gerais, the Quadrilátero Ferrífero and Serra do Espinhaço are considered distinct relief units based on geomorphology (Dorr II, 1969; Saadi, 1995). Results and Discussion Figure 3. Dipsas albifrons ( 3651) in life, collected in RPPN Córrego Seco, Itabirito, Minas Gerais. Photo by Adriano Silveira. Two specimens of Dipsas albifrons were captured during field sampling in the Quadrilátero Ferrífero region. The first specimen ( 3636; Figs. 1 and 2) was collected in Floresta Estadual do Uaimii ( S; W; circa 1000 m elev.), in the district of São Bartolomeu, municipality of Ouro Preto, on 14 December 2016, by A. L. Silveira. It was traveling on the ground at night during rain, crossing a Figure 4. Habitat of Seasonal Semideciduous Forest at the collection sites of Dipsas albifrons. Uaimii in Ouro Preto; C and D RPPN Córrego Seco in Itabirito.

4 812 Adriano L. Silveira et al. Figure 5. Geographic distribution of Dipsas albifrons based on specimens in the present study (red circles), specimens examined by Passos et al. (2005) (blue circles) and other records from the literature (Argôlo, 2004, Bérnils et al., 2014, Ferreira & Silva- Soares, 2012, Gasparini, 2012, Instituto Ambiental do Paraná, 2012, Kunz & Ghizoni-Jr, 2008, Sazima & Muscat, 2016, Silva- Soares et al., 2011) (yellow circles). Records in Minas Gerais: 1 Floresta Estadual do Uaimii, Ouro Preto; 2 RPPN Córrego Seco e Sítio Irmãos Coragem, Itabirito; 3 Serra do Ouro Branco, Ouro Branco; 4 Caeté; 5 Sítio Primavera, Itaúna; 6 Serra do Sapo, Conceição do Mato Dentro, 7 Aimorés Hydroelectric Plant, Aimorés (see details in text). The green line delimits the Atlantic Forest biome. Table 1. Collection data for the analyzed specimens of Dipsas albifrons from Minas Gerais, Brazil. Specimen Municipality Locality Collection data Collector 3636 Ouro Preto Floresta Estadual do Uaimii 14/XII/2016 Silveira, A. L Itabirito RPPN Córrego Seco 16/XI/2017 Silveira, A. L. 65 Itabirito Sítio Irmãos Coragem 09/I/1988 Ramos, J Itaúna Sítio Primavera 03/II/1992 Unknown 659 S Ouro Branco 24/IV/2005 São-Pedro, V. A. 791 S Ouro Branco Serra do Ouro Branco 09/XII/2007 Gonçalves, L. M. 973 Caeté Caeté XI-XII/1991 Nascimento, L. B. & Feio, R. N Conceição do Serra do Sapo 15/XII/2014 Silva, A. L. Mato Dentro 4759 Aimorés Hydroelectric Plant Aimorés X/2004 Carvalho Jr., R. R.

5 New records of Dispas albifrons in the Atlantic Forest of Minas Gerais, Brazil 813 Table 2. Counts of series of scales (pholidosis) and dorsal spots of the analyzed specimens of Dipsas albifrons from Minas Gerais, compared to the data reported by Passos et al. (2005). Characters 659 S 791 S 5857 Analyzed specimens Passos et al. (2005) Sex M M M M M F F F M and F Dorsals 15/15/15 15/15/15 15/15/15 15/15/15 15/15/15 15/15/15 15/15/17ˈ 15/15/15 15/15/15 Gulars Pre-ventrals Ventrals M: F: Cloacal Pairs of Subcaudals M: F: Supralabials (in contact with eye) Infralabials (in contact medially) (2/3) 12/11 (2) 7/8 (1/1)ˈ 12/12 7/7 (3/4) 11/11 (2) 13/11 7/7 11/12 10/10 11/10 (4) 11/ (2-4) 8-13 (1-4) Pre-oculars 3/3ˈ 2/2 2/2 2/2 1/2 1/1 2/2 2/2 0, 1, 2 Post-oculars 2/2 1/2 2/2 2/2 2/2 2/2 1/1 2/2 1, 2 Temporals (ant.+post.) 1+3/ / / / / /1+2+2ˈ 1+2/1*ˈ 1+2/1+1+2ˈ 1+1, 1+2, 2+1, 2+2, 2+3 Dorsal spots on the body 27/26 25/26 21/21 24/24 24/22 25/24 26/24 22/ Dorsal spots on the tail 16/15 17/17 12/12 16/16 14/15 14/16 13/13 19/16ˈ M: F: Sex: M male, F female * Fusion of the two series of temporals on the right side - Not reported ˈ Variation in relation to Passos et al. (2005) road that cuts through a forest remnant next to a swamp and a perennial stream. The second specimen ( 3651; Fig. 3) was collected in Reserva Particular do Patrimônio Natural (RPPN) Córrego Seco ( S; W; circa 1020 m elev.), in the municipality of Itabirito, on 16 November 2017, by A. L. Silveira. The specimen was moving at night over vegetation of the forest understory 80 cm above the ground next to a spring. Both collections occurred in remnants of Seasonal Semideciduous Forest undergoing secondary regeneration (Fig. 4). Seven additional specimens were located in scientific collections, including the Itabirito specimen examined by Silveira et al. (2010; Table 1). Six of the seven museum specimens were from Seasonal Semideciduous Forest formations within the western limits of the Atlantic Forest (IBGE, 2004), while the seventh specimen was from Vale do Rio Doce, within Seasonal Semideciduous Forest at its eastern border with Dense Ombrophilous Forest (IBGE, 2004). The new records presented here represent a significant expansion of the known geographic distribution of Dipsas albifrons in the Atlantic Forest of Minas Gerais, and allow the recognition of two geographical areas of the occurrence of the species (Fig. 5). The first area corresponds to the mountainous complexes of the Planalto Meridional of the Serra do Espinhaço (Conceição do Mato Dentro) and Quadrilátero Ferrífero and surroundings (Itabirito, Ouro Preto, Ouro Branco, Caté e Itaúna), while the second corresponds to Vale do Rio Doce (Aimorés) in the eastern part of the state contiguous with Região Serrana do Espírito Santo, where there are recorded localities of the species near Aimorés. The specimens analysed here were morphologically within the range reported for the species by Passos et al. (2005). Scale counts and dorsal spots were generally within the ranges previous reported (Table 2; Passos et al., 2005). The ventral (mean in males: 182.8; mean in females: 180.3) and subcaudal (mean in males: 89.4; mean in females: 82.0) scale counts of the specimens analyzed here were high relative to those reported by Passos et

6 814 Adriano L. Silveira et al. Table 3. Morphometry of the analyzed specimens of Dipsas albifrons from Minas Gerais, compared with the data reported by Passos et al. (2005). Medidas (mm) 659 S 791 S 5857 Analyzed specimens Passos et al. (2005) Sex M M M M M F F F M and F Snout-vent length M: F: 390*, + Caudal length M: 215 F: 139*, + Head length F: 15.3* Head width F: 8.4* Head height Sex: M male, F female * Measurements of lectotype + Measures of the largest specimen - Not reported al. (2005). These results follow the pattern of increased ventral and subcaudal counts in more northern populations (Passos et al., 2005). Acknowledgements. We thank the company Vale S. A. for financial support and for authorizing the research at RPPN Córrego Seco; the business Amplo Engenharia e Gestão de Projetos for logistic support; the Instituto Estadual de Florestas MG for authorizing the research in Floresta Estadual do Uaimii; José Janderson F. Rocha and Leonardo Augusto C. Fonseca for assistance with field activities; Erik R. Wild, for translating the English version of the manuscript; and the anonymous reviewers for their corrections and suggestions. References Argôlo, A.J.S. (2004): As Serpentes dos Cacauais do Sudeste da Bahia. Ilhéus, Editus. Bérnils, R.S., Almeida, A.P., Gasparini, J.L., Srbek-Araujo, A.C., Rocha, C.F.D., Rodrigues, M.T. (2014): Répteis na Reserva Natural Vale, Linhares, Espírito Santo, Brasil. Ciência & Ambiente 49: Dorr II, J.V.N. (1969): Phyysiographic, stratigraphic and structural development of the Quadrilatero Ferrifero Minas Gerais, Brazil. Geological Survey Professional Paper 641(A): I-V+A1 A110. Dowling, H.G. (1951): A proposed standard system of counting ventrals in snakes. British Journal of Herpetology 1(5): Ferreira, R.B., Silva-Soares, T. (2012): Road mortality of snakes at the Parque Estadual da Fonte Grande, an urban forest of Southeastern Brazil. Boletim do Museu de Biologia Mello Leitão, Nova Séria 29: Franco, F.L., Salomão, M.G. (2002): Répteis. In: Técnicas de Coleta e Preparação de Vertebrados para Fins Científicos e Didáticos, p Auricchio, P., Salomão, M.G., Org., São Paulo, Instituto Pau Brasil de História Natural. Fundação Biodiversitas (2007): Revisão das listas das espécies da flora e da fauna ameaçadas de extinção do Estado de Minas Gerais. Relatório Final, Volume 3 (Resultados: Lista Vermelha da Fauna de Minas Gerais). Belo Horizonte, Fundação Biodiversitas. Gasparini, J.L. (2012): Anfíbios & Répteis: Vitória e Grande Vitória, Espírito Santo. Vitória, GSA. IBGE (2004): Mapa de Vegetação do Brasil. 3. ed. [S.l.], Instituto Brasileiro de Geografia e Estatística. Scale 1: Instituto Ambiental do Paraná (2012): Plano de Manejo do Parque Estadual da Ilha do Mel. Curitiba, Instituto Ambiental do Paraná. Kunz, T.S., Ghizoni-Jr, I.R. (2008): Serpentes encontradas mortas em rodovias do estado de Santa Catarina, Brasil. Biotemas 22(2): Martins, M., Bérnils, R.S., Silveira, A.L., Sousa, B.M., Drummond, G.M., Coutinho, M.E., Cotta, G.A., Barbosa, V., Fernandes, R., Marques, O.A.V., Mello, H.E.S. (2008): Répteis ameaçados de extinção em Minas Gerais. In: Listas Vermelhas das Espécies da Fauna e da Flora Ameaçadas de Extinção em Minas Gerais, digital media. Drummond, G.M., Machado, A.B.M., Martins, C.S., Mendonça,.M.P, Stehmann, J.R., Eds., Belo Horizonte, Fundação Biodiversitas. Passos, P., Fernandes, R., Porto, M. (2005): Geographical variation and taxonomy of the snail-eating snake Dipsas albifrons (Sauvage, 1884), with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge, 1950 (Serpentes: Colubridae: Dipsadinae). Zootaxa 1013: Peters, J.A. (1964): Dictionary of Herpetology: a brief and meaningful definition of words and terms used in herpetology. New York and London, Hefner Publishing.

7 New records of Dispas albifrons in the Atlantic Forest of Minas Gerais, Brazil 815 Saadi, A. (1995): A geomorfologia da Serra do Espinhaço em Minas Gerais e de suas margens. Geonomos 3(1): Sazima, I., Muscat, E. (2016): Shelled baby food: Newly hatched goo eating snakes of the genus Dipsas (Squamata: Dipsadidae) prey on snails in nature. Herpetologia Brasileira 5: Silva-Soares, T., Ferreira, R.B., Salles, R.O.L., Rocha, C.F.D. (2011): Continental, insular and coastal marine reptiles from the municipality of Vitória, state of Espírito Santo, southeastern Brazil. Check List 7: Silveira, A.L., Pires, M.R.S., Cotta, G.A. (2010): Serpentes de uma área de transição entre o Cerrado e a Mata Atlântica no Sudeste do Brasil. Arquivos do Museu Nacional 68(1 2): Accepted by Andrew Durso