Herpetology Notes, volume 14: 193-196 (2021) (published online on 26 January 2021)

New records of poorly known of the Apostolepis (Dipsadidae, Elapomorphini) in Central

Fábio Maffei1,* and Cristiano de Campos Nogueira2

Apostolepis is a genus endemic to Cis-Andean specimen on the margins of Taquaruçu River, Anastácio South America, currently comprising 37 species municipality (ca. 66 km from the type-locality) was (Entiauspe-Neto et al., 2020; Uetz et al., 2020). They described by Albuquerque and Lema (2012). Other two are fossorial snakes belonging to the Family Dipsadidae, specimens of , from Reserva Natural Laguna subfamily and tribe Elapomorphini, Blanca, Departamento de San Pedro are presented by with 32 species occurring in Brazil (Colli et al. 2019; Entiauspe-Neto et al. (2014). Another record based on a Nogueira et al., 2019; Entiauspe-Neto et al., 2020). field collected specimen is mentioned by Nogueira et al. However, many species in this genus are only known (2019) for Emas , Goiás, based on a field from their holotype or a few additional specimens, as record in Vadujo et al. (2009) as Apostolepis aff. lineata. the genus is poorly represented in collections (Nogueira Due to the low number of individuals collected for both et al. 2012). Apostolepis goiasensis Prado, 1943 is species, here we present new records for the endemic to Brazil, occurring in the Cerrado savannahs of of the state of do Sul, Central Brazil and Central Brazil (Nogueira et al., 2019). It was described update their range and meristic variation. from a specimen from Rio Verde, state of Goiás, Brazil, Data collection was carried during faunal monitoring lost during a fire at the Instituto Butantan (Lema 2015). at Fazenda Barra do Moeda, from 2007-2020. The area Lema (2003) redescribed the species based on a second is located in the municipality of Três Lagoas, in the state specimen from the municipality of Uberlândia, state of Mato Grosso do Sul, Central Brazil (-21.0064°S - of , Brazil. Subsequently, new data was 51.7969°W, WGS84). The farm is limited in its northeast published on individuals from , state part by the Moeda River, in the northwest by the MS- of Mato Grosso do Sul (Abes and Ferrarezzi, 2003); 395 state highway and in the southeast by the Paraná Luziânia, state of Goiás; Três Lagoas, state of Mato River. This river is one of the most important rivers in Grosso do Sul; and a specimen without known locality the region and divides the states of Mato Grosso do Sul (Loebmann and Lema, 2012; Lema 2015). Other three and São Paulo. The study area is a mosaic formed by records of the species are presented by Nogueira et al. different Cerrado savannah physiognomies, as well as (2019), for the Federal District (Brasília), state of Goiás deciduous and semi-deciduous in a matrix of (Uruaçu municipality) and state of São Paulo (Luiz Eucalyptus plantations. Semi-annual field campaigns Antônio municipality). were carried out from 2017 to 2018, using the methods Apostolepis intermedia Koslowsky, 1898 is known of active search and pitfall traps (15 lines with five 60 from Brazil and Paraguay. This species was described L buckets each) for five days per campaign. based on a single specimen collected in Miranda, were collected under the license SISBIO 58551-1/2 and state of Mato Grosso do Sul, Brazil, whose holotype were deposited in the Herpetological Collection of the was lost (Albuquerque and Lema 2012). One second Butantan Institute, São Paulo state, Brazil. In October 2017 (6-10) four individuals of Apostolepis were captured in pitfall traps: three A. intermedia and

1 Universidade Estadual Paulista, Faculdade de Ciências, one A. goiasensis. In April 2018, another individual of CEP17033-360, , São Paulo, Brazil. A. goiasensis was also captured in pitfall traps. Four 2 Universidade de São Paulo, Departamento de Ecologia, of these individuals (three A. intermedia and one A. Instituto de Biociências, CEP 05508‑090, São Paulo, São goiasensis) were captured in stands with eucalyptus Paulo, Brazil. plantations and the other individual from A. goiasensis * Corresponding author. E-mail:[email protected] was captured in an area of “Cerradão”, a woodland form © 2020 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. of dense Cerrado (Table 1). 194 Fábio Maffei & Cristiano de Campos Nogueira 1

Table 1. Individuals of Apostolepis collected in Três Lagoas, Mato Grosso do Sul state, Brazil. SVL: Snout-vent length; TL: Tail length.Table IBSP: 1. Individuals Butantan ofInstitute, Apostolepis São Paulo. collected in Três Lagoas, Mato Grosso do Sul state, Brazil. SVL: Snout-vent length; TL: Tail length. IBSP: Butantan Institute, São Paulo.

Scales Length (mm) Species Data Anal Subcaudal Dorsal Ventral SVL TL Sex Number (pairs) A. goiasensis 09/10/2017 Divided 27 15/15/15 214 375 39 M IBSP 90238 A. goiasensis 08/04/2018 Divided 28 15/15/15 220 445 45 F IBSP 90239 A. intermedia 06/10/2017 Entire 38 15/15/15 230 348 44 F IBSP 90237 A. intermedia 09/10/2017 ------not collected A. intermedia 09/10/2017 ------not collected

The specimens of A. goiasensis were identified (2003) (233-237). The number of subcaudals (27 and according to Lema (2003) and Loebmann and Lema 28) is within the reported range for the species (25-33). (2012), the latter allowing colour comparisons in life. The specimen collected from A. intermedia was The dorsum is salmon reddish with three narrow black identified according to Albuquerque and Lema (2012). longitudinal bands that disappear on the tail (Fig. 1A). The individual has five dark bands on the dorsal The vertebral stripe is the sharpest. The terminal portion region of the body, with the paravertebral bands being of the tail is black with a white tip. The belly is uniform narrower (Fig. 2A). Brown dorsum, not red as in A. (immaculate) white, except near the end of the tail dimidiata, and immaculate belly. The black caudal band which has black scales (Fig. 1B). The number of ventral completely covers the end of the tail, except for the scales (214 and 220) is below that presented by Lema cream terminal scale (Fig. 2B). The number of ventrals

Figure 1. Snakes of genus Apostolepis collected in Três Lagoas, Mato Grosso do Sul state, Brazil. (A) Male of A. goiasensis (IBSP 90238); (B) Ventral detail of head and tail of the specimen; (C) Female of A. intermedia (IBSP 90237); (D) Ventral detail of head and tail of the specimen. Photographs by Fábio Maffei. New records of poorly known snakes of the genus Apostolepis in Central Brazil 195

Figure 2. New records (squares) of Apostolepis in Três Lagoas, Mato Grosso do Sul state, Brazil. Literature records (circles) in the Cerrado biome (yellow polygon) and circle with dots the type-localities.

(230) is greater than the known variation (211-217; known distribution 400 km east from the closest know Albuquerque and Lema 2012) for males, and below that locality in the municipality of Anastácio (Fig. 2). presented by Entiauspe-Neto et al. (2014) for females The two species recorded here occur predominantly (241-242). The number of subcaudals (38) also differs in Cerrado areas. This biome is a biodiversity hotspot from the variation (33-37 for males; 28-31 for females). (Mittermeier et al. 2011) and is under strong anthropic For both species, the male’s total length is smaller than pressure, being the most threatened savannah in the the female, agreeing with the sexual dimorphism in (Strassburg et al., 2017). The rarity of records of Apostolepis (e.g. Lema and Renner, 1998). both species shows that we still know little about the Although the genus is widespread in Cis-andean South snake of central Brazil, and highlights the need America, most species inhabit open landscapes like the for new data from formations such as Cerradão. Cerrado, the Caatinga and the (Nogueira et al. 2019). The state of Mato Grosso do Sul (Central- Acknowledgements. Thanks to Suzano S.A. for supporting West Brazil) has 113 species of snakes, eight of them fieldwork; Filipe Serrano and Paulo R. Machado-Filho for of the genus Apostolepis: A. ambiniger (Peters, 1869), their support in tipping the material. Paulo Antas on behalf of FUNATURA for field logistics. A. assimilis (Reinhardt, 1861), A. cf. christineae, A. dimidiata (Jan, 1862), A. intermedia, A. goiasensis, A. References aff. nigroterminata 1 e A. aff. nigroterminata 2, these last two are still new to science in the process of description Abes, S.S., Ferrarezzi, H. (2003): Apostolepis goiasensis. Brazil: (Ferreira et al. 2017). Apostolepis goiasensis has already Mato Grosso do Sul. Herpetological Review 34: 167. been registered in Ribas do Rio Pardo and Três Lagoas Albuquerque, N.R., T. Lema. (2012): Description of the second known specimen of Apostolepis intermedia (Serpentes, (Abes and Ferrarezzi, 2003). Apostolepis intermedia , Xenodontinae). Zootaxa 3325: 53–58. has records in Miranda and Anastácio municipalities Colli, G.R., Barreto-Lima, A.F. Dantas, P.T., Morais, C.J.S., Pantoja, (Albuquerque and Lema, 2012). For this species, this D.L., Sena, A.D. Sousa, H.C. (2012): On the occurrence of present record fills a gap in the state and extends its Apostolepis phillipsi (Serpentes, Elapomorphini) in Brazil, with 196 Fábio Maffei & Cristiano de Campos Nogueira

the description of a new specimen from Mato Grosso. Zootaxa Mittermeier, R.A., Turner, W.R., Larsen, F.W., Brooks, T.M., 4619(3): 580–588. Gascon, C. (2011): Global biodiversity conservation: the critical Entiauspe-Neto O.M., Lema T., Beconi H.E.C. (2014): Apostolepis role of hotspots. In: Biodiversity hotspots, p. 3-22. Zachos, F., intermedia Koslowsky, 1898 (Serpentes: Xenodontinae: Habel, J., Eds., Berlin, Germany, Springer-Verlag. Elapomorphini): first records for Paraguay. Check List 10: Nogueira, C., Barbo, F.E., Ferrarezzi, H. (2012): Redescription 600–601. of Apostolepis albicollaris Lema, 2002, with a key for the Entiauspe-Neto, O.M., Guedes, T.S.B., Loebmann, D., Lema, T. species groups of the genus Apostolepis (Serpentes: Dipsadidae: (2020): Taxonomic Status of Two Simultaneously Described Elapomorphini). South American Journal of Herpetology 7(3): Apostolepis Cope, 1862 Species (Dipsadidae: Elapomorphini) 213-225 from Caatinga Enclaves Moist Forests, Brazil. Journal of Nogueira, C.C. et al. (2019): Atlas of Brazilian Snakes: Verified Herpetology 54(2): 225–234. Point-Locality Maps to Mitigate the Wallacean Shortfall in Ferreira, V.L., Terra, J.S., Piatti, L., Delatorre, M., Strüssmann, C., a Megadiverse Snake Fauna. South American Journal of Béda, A.F., Kawashita-Ribeiro, R.A., Landgref-Filho, P., Aoki, Herpetology 14(Special Issue 1): 1–274. C., Campos, Z., Souza, F.L., Ávila, R.W., Duleba, S., Martins, Strassburg, B.B.N., Brooks, T., Feltran-Barbieri, R., Iribarrem, K.S., Rita, P.H.S., Albuquerque, N.R. (2017): Répteis do Mato A., Crouzeilles, R., Loyola, R., Latawiec, A.E., Oliveira-Filho, Grosso do Sul, Brasil. Iheringia. Série Zoologia 107(suppl.): F.J.B., Scaramuzza, C.A.M., Scarano, F.R., Soares-Filho, B., e2017153. Balmford, A. (2017): Moment of truth for the Cerrado hotspot. Lema, T. (2003): Reencontro de Apostolepis goiasensis Prado, 1942, Nature Ecology & Evolution 1(2017): 0099. com a redescrição da espécie (Serpentes: Elapomorphinae). Uetz, P., Freed, P. Hošek, J. (2020): Genus Apostolepis. The Comunicacoes do Museu de Ciencias e Tecnologia da PUCRS Database. Available at http://www.reptile-database.org. Série Zoologia 16: 199-209. Accessed on 20 August 2020. Lema, T. (2015): Remarks on Apostolepis goiasensis (Serpentes, Valdujo, P.H., Silvano, D.L., Colli, G., Martins, M. (2012): Anuran Xenodontinae), with presentation of the holotype. Cadernos de Species Composition and distribution patterns in Brazilian Pesquisa, série Biologia, 27: 20–27. Cerrado a Neotropical Hotspot. South American Journal of Lema, T. M.F. Renner. (1998): O status de Apostolepis Herpetology 7(2): 63–78. quinquelineata Boulenger, 1896, A. pymi Boulenger, 1903, e A. rondoni Amaral, 1925 (Serpentes: Colubride: Elapomorphinae). Biociências 6(1): 99-121. Loebmann, D., Lema, T. (2012): New data on the distribution of the rare and poorly known Apostolepis goiasensis Prado, 1943 (Serpentes, Xenodontinae, Elapomorphini) with remarks on morphology and colouration. Herpetology Notes 5: 523-525.

Accepted by Andrew Durso