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Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3):241-253. Julho-Setembro de 2015 241

New records of Liotyphlops beui (Amaral, 1924) (Serpentes: ) and an updated distribution map

Henrique C. Costa1,*, Fidélis Júnio Marra Santos2 & Daniel Loebmann3

ABSTRACT: Data on distribution is basic information for many research fields, including assessment of conservation status. Usually, this issue is non-available or it is incomplete for fossorial species. Herein, we provide an updated map of distribution and new records of occurrence of the blind Liotyphlops beui. Although it is one of the most widely distributed Neotropical anomalepidids, we identify relevant gaps on species records of occurrence as well as dubious information about its most Austral distribution. A dataset with all recognized records which may be useful for other studies like distribution modeling is also provided. Key words: Blind ; gaps of distribution; Scolecophidia.

RESUMO: Novo registro de Liotyphlops beui (Amaral, 1924) (Serpentes: Anomalepididae) e uma atualização do mapa de distribuição. Dados sobre distribuição de espécies constituem uma informação básica para muitas linhas de pesquisa, incluindo a avaliação de estado de conservação. Geralmente, esses dados não estão disponíveis ou são incompletos para espécies fossoriais. Nós apresentamos um mapa de distribuição atualizado e novos registros de ocorrência da cobra-cega Liotyphlops beui. Embora seja uma das espécies de anomalepidídeos mais amplamente distribuída, identificamos importantes lacunas nos registros dessa espécie, assim como informações dúbias sobre sua distribuição austral. Uma base de dados com todos os registros identificados, a

1 Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Zoologia, Laboratório de Herpetologia. Avenida Antônio Carlos 6627, Pampulha, 31270-901, Belo Horizonte, MG, Brasil. 2 Pontifícia Universidade Católica do Rio Grande do Sul, Museu de Ciências e Tecnologia, Laboratório de Sistemática de Vertebrados, Setor de Herpetologia. Avenida Ipiranga, 6681, Partenon, 90619-900, Porto Alegre, RS, Brasil. 3 Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Laboratório de Vertebrados. Avenida Itália, km 8, Vila Carreiros, 96203-900, Rio Grande, RS, Brasil. * Corresponding author. [email protected] Recebido: 3 jun 2014 – Aceito: 3 fev 2015 242 Costa et al.: Geographic distribution of Liotyphlops beui qual pode ser útil para outros estudos como modelagem de distribuição também é apresentada. Palavras-chave: Cobras-cegas; lacunas de distribuição; Scolecophidia.

Anomalepididae Taylor, 1939 comprises four genera of blind snakes: Anomalepis Jan, 1860, Helminthophis Peters, 1860, Liotyphlops Peters, 1881, and Typhlophis Fitzinger, 1843 (McDiarmid et al., 1999). Liotyphlops is the richest , with 10 species current recognized, distributed from to Argentina (Dixon & Kofron, 1983; Haad et al., 2008; Centeno et al., 2010). In his Catalogue of the Snakes from the British Museum, Boulenger (1893) synonymized Liotyphlops with Helminthophis. Thirty years later, Amaral (1924) described Helminthophis beui, based on specimens from Butantan, São Paulo, Brazil, and the same author further synonymized H. beui with Helminthophis ternetzii Boulenger, 1896 (Amaral, 1929). Dunn (1932), removed Liotyphlops from the synonymy of Helminthophis, and only after the study by Dixon & Kofron (1983) L. beui was resurrected. Liotyphlops beui is diagnosed by having: three scales contacting posterior edge of prefrontal; two scales contacting posterior edge of nasal between second supralabial and prefrontal; five scales in the first vertical row of dorsals; four supralabials; four infralabials; 22–26 anterior scale rows; 20–24 midbody scale rows; 20 posterior scale rows; 384–464 dorsal scale rows (Centeno et al., 2010). Today, this species has one of the widest range among its congeners, occurring from Misiones in Argentina, northward to Goiás, in Brazil (Centeno et al., 2010). Recently, after examining anomalepidids deposited in some Brazilian collections, we found specimens from localities representing important records for the knowledge of the geographic distribution of Liotyphlops beui. These new records come from specimens in the collections of Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais, and Museu de Ciências e Tecnologia, PUC-RS (MCT), Porto Alegre, Rio Grande do Sul. Two specimens (UFMG 1906, 1907 [Figure 1]), from Pará de Minas (19.8600° S, 44.6078° W) represent the second known record from the state of Minas Gerais, filling a gap ofca. 800 km between Uberlândia and Colatina, the closest records (Centeno et al., 2010). In Figure 1 of Centeno et al. (2010), two locality records for L. beui are present in Minas Gerais: Uberlândia in the west and a second point in the southeast, which actually lies in the city of Viçosa, where L. wilderi, not L. beui occurs (F. C. Centeno, by e-mail to HCC; see also the appendix in Centeno et al. (2010), and Costa et al. (2010)). Other four new important records come from Bom Progresso (27.5439° S, 53.8658° W) (MCT 19086), Frederico Westphalen (27.3589° S, 53.3939° W) (MCT 4345), Frederico Westphalen, Colégio Agrícola (27.3916° S, 53.4307° Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3). 2015 243

Figure 1. Live specimen of Liotyphlops beui (UFMG 1907, snout-vent length 282 mm), from Pará de Minas, state of Minas Gerais, Brazil. Photo by Henrique C. Costa.

W) (MCT 9494), and Porto Vera Cruz (27.7358° S, 54.9008° W) (MCT 11676). Lema (1994, 2002) cites L. beui for Rio Grande do Sul, but without voucher or detailed locality information. Although close to previous known localities in Argentina (Giraudo, 1994), our records of L. beui for Rio Grande do Sul can be considered the first with voucher specimens. With these new data, Liotyphlops beui is now known to occur from Porto Vera Cruz in Rio Grande do Sul, northward through Misiones (Argentina), Ciudad del Este (Paraguay) and the Brazilian states of Santa Catarina, Paraná, São Paulo, Mato Grosso do Sul, Mato Grosso (westernmost record in Barra do Bugres [15.0728° S, 57.1808° W]), Espírito Santo (easternmost record in Colatina [19.5400° S, 40.6300° W]), Minas Gerais and Goiás (northernmost record in Minaçu, UHE Cana Brava [13.4882° S, 48.1871° W]) (Table 1). Locality records lie in the terrestrial ecoregions (sensu Olson et al., 2001) of Alto Paraná Atlantic Forests (including a transition with the Southern Cone Mesopotamian Savanna), Araucaria Moist Forests, Serra do Mar Coastal Forests, Bahia Interior Forests, Cerrado, and Chiquitano Dry Forests (Figure 2). 244 Costa et al.: Geographic distribution of Liotyphlops beui

Liotyphlops beui inhabits environments varying from forests to open habitats, including urbanized areas (Barbo et al. 2011). Besides the new records here presented, many gaps remain in the knowledge of the geographic distribution of Liotyphlops beui. Probably, the examination of specimens from regional collections, and even more field work may help filling those gaps.

Figure 2. Geographic distribution of Liotyphlops beui. Red dots = literature records; yellow squares = new records. Terrestrial Ecoregions follow Olson et al. (2001). See text for details and Table 1 for the list of localities here represented. Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3). 2015 245 Voucher 431 CFA MACN 33040 231, 405 CFA MACN 3554 CIES 45, 53 CUNAM s/n 5255, 5256 MZUSP 4552 IBSP 15118 15117, MZUSP ? 44188 IBSP ? 11042–11043 MZUSP UFMG 1906, 1907 75588 IBSP 8882 IBSP ? ; 2009 (2010) (2010) (2010) (2010) (2009) (2009) (2009) (2009) et al. et al. et al. et al. et al. et al. et al. et al. et al. Source Giraudo (1994) Giraudo (1994) Giraudo (1994) Giraudo (1994) Giraudo (1994) Giraudo (1994) Dixon & Kofron (1983); Centeno Amaral (1954) Cintra Moreira Centeno Moreira Moreira Centeno This study Centeno Amaral (1954); Dixon & Kofron (1983) Silva Jr. : BM = British Museum. -53.67 -54.2820 -54.8333 -55.1221 -54.4645 -55.8833 -40.6300 -49.2898 -46.1736 -48.1871 -51.9624 -48.3373 -48.3100 -44.6078 -48.2769 -54.8600 -54.8278 Longitude 4.3089 -26.9305 -26.2664 -27.1000 -27.5140 -25.7037 -27.3833 -19.5400 -16.6721 -1 -13.4882 -18.3065 -16.3190 -13.9000 -19.8600 -18.9189 -20.4419 -17.6086 Latitude United Kingdom : CFA = Colección Felix de Azara; MACN = Museo Argentino de Ciencias Naturales de Ciencias Argentino Azara; MACN = Museo = Colección Felix de : CFA based on literature review and this study. Voucher information is based solely on its on solely based is information Voucher study. this and review on literature based : MZUSP = Museu de Zoologia, Universidade de São Paulo; IBSP = Instituto Butantan; = Instituto IBSP São Paulo; de Universidade Zoologia, = Museu de MZUSP : Localidade : CM = Carnegie Museum; MCZ = Museum of Comparative Zoology; DU = Duke University. University. Duke DU = Zoology; Comparative of Museum = MCZ Museum; Carnegie = CM : Argentina Brazil USA 1 PCH Santa Edwidges Campinas UHE Cana Brava Liotyphlops beui Liotyphlops Municipality/City, Municipality/City, 17 Km al sur de Fracrán por el camino que va hacia El Soberbio de Irigoyen de Bernardo 30 km al noreste Aristobolu del Valle Oberá Nacional Iguazú Parque Posadas Colatina Goiânia, Mambaí, Minaçu, Serranópolis UHE Corumbá IV UHE Serra da Mesa Pará de Minas Uberlândia Terenos UHE Ponte de Pedra : MNHG = Museum d’Histoire Naturelle, Geneve. State/Province Misiones Misiones Misiones Misiones Misiones Misiones ES GO GO GO GO GO GO MG MG MS MS / MT Locality records of records Locality Country Argentina Argentina Argentina Argentina Argentina Argentina Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Table 1. Table respective source. Collection acronyms: CUNAM de la Subtropicales; = Colección Ecológicas del Centro de Investigaciones CIES = Colección Rivadavia”; “Bernardino Misiones. de Nacional Universidad Museu = MCT Janeiro; de Rio do Federal Universidade Museu Nacional, MNRJ = Minas Gerais; de Federal Universidade UFMG = PUC-RS. Tecnologia, e Ciências de Switzerland 246 Costa et al.: Geographic distribution of Liotyphlops beui Table 1 (cont.) Table Voucher MNRJ 7854 6349 MZUSP 26467 IBSP 8163, 8164, 8884– IBSP 8889 10848, 10853–10855, MCT 10871, 10879 MCT 10880; MZUSP MCT 11544–11551 4086-4090, 15643 MZUSP 74097 IBSP 16363 MCT 16362 MCT MNRJ 383, 384 ? 68127 IBSP 2756-2757, 4098 MZUSP 10857-1059, 10862, MCT 10864, 10868 16360 MCT 73913 IBSP 19086 MCT

This et et al. (2010) (2010) (2010); (2010) (2010) (2007) (2007) (2008); Centeno (2008); Centeno (2008); Centeno et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. (2010) (2010) (2010)

(2008); Centeno Source Freire Dixon & Kofron (1983); Centeno Haad et al. Amaral (1954); Dixon & Kofron (1983); Haad al. (2010) This study Centeno study Dixon & Kofron (1983); Centeno Haad et al. This study This study Freire Bernarde & Machado (2002) Haad et al. Dixon & Kofron (1983); Centeno This study This study Centeno This study -57.1808 -55.7400 -50.2289 -49.4100 -53.4121 -53.0425 -49.2728 -49.2367 -49.2441 -49.2284 -54.5878 -51.1628 -50.1619 -51.3689 -53.2930 -51.0858 -44.7134 -53.8658 Longitude -25.4115 -15.0728 -15.4500 -23.0508 -25.5928 -25.4313 -25.5762 -25.4278 -25.3990 -25.4287 -25.5478 -23.3100 -25.0950 -23.3100 -25.5074 -26.2300 -23.2185 -27.5439 Latitude Flor da Serra Barra Bonita Foz do Chopim Localidade Bacacheri Cirsto Rei Social Jardim 1 Municipality/City, Municipality/City, Barra do Bugres Chapada dos Guimarães Andirá Araucaria Boa da Aparecida, Vista Cruzeiro do Iguaçu, Curitiba Curitiba, Curitiba, Curitiba, Foz do Iguaçu Londrina Ponta Grossa Rolândia Barras do Paraná, Tres União da Vitória Paraty Bom Progresso State/Province MT MT PR PR PR PR PR PR PR PR PR PR PR PR PR PR RJ RS Country Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3). 2015 247 Table 1 (cont.) Table 27588

Voucher 4345 MCT 9494 MCT 11676 MCT ? ? 55743 IBSP 67915 IBSP ? 7640 IBSP CM 39570, 39571; IBSP 16036, 75391; MCZ 142557 61758, MNRJ 8143 IBSP ? 23210 IBSP 62761, 75379; MNRJ IBSP 16361 10578; MCT 76279 IBSP 62751–62752 IBSP 70988, 71358 IBSP IBSP ? 44200, 61986–61988 IBSP

et al. Haad ; (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2001) (2010) (2007); (2007) (2008) et al. et al. et al. et al. et al. et al. et al. et al. This study et al. et al. ; et al. et al. et al. (2008); Centeno Source This study This study This study Bérnils Hartmann & Giasson (2008) Centeno Centeno Araújo & Almeida-Santos (2011) Amaral (1954); Dixon & Kofron (1983) Dixon & Kofron (1983) Freire Centeno Sazima & Manzani (1995) Forlani Freire et al. (2010) Haad Centeno Centeno Centeno Centeno Centeno -47.1167 -53.3939 -53.4307 -54.9008 -49.2201 -52.5332 -50.3500 -47.6544 -46.8758 -47.0608 -48.0333 -46.8358 -46.8410 -46.9189 -46.8524 -50.7384 -50.6434 -47.2234 Longitude -27.1170 -27.3589 -27.3916 -27.7358 -26.6618 -22.5500 -23.3856 -23.5108 -22.9058 -22.8167 -24.1000 -23.5228 -23.5675 -23.6039 -46.8524 -22.9035 -21.2615 -23.6565 Latitude 2

UHE Quebra Queixo Agricola Colegio Localidade 1 Parque Estadual Carlos Parque 1 Vila Cristina Vila 1 Mata de Santa Genebra 1 1 Estação Ecológica de Assis Estação Ecológica de 1 Municipality/City, Municipality/City, Westphalen Frederico Westphalen, Frederico Cruz Porto Vera altas da Bacia do Rio Itajaí Áreas Ipuaçu / São Domingos, Angatuba Araçariguama Assis, Bacaetava Barueri Campinas Campinas, Capão Bonito, Botelho Carapicuíba Carapicuíba, Cotia Embu das Artes Florínia Guararapes Ibiúna State/Province RS RS RS SC SC SP SP SP SP SP SP SP SP SP SP SP SP SP SP SP Country Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil 248 Costa et al.: Geographic distribution of Liotyphlops beui Table 1 (cont.) Table 67692, 67693

IBSP 69126 IBSP Voucher ? 7517 MZUSP ? 75958 IBSP 62642 IBSP MNRJ 8144–8146 26544-26545, 64196, IBSP 71725 44295 IBSP 30559, 42554 IBSP 68909 IBSP DU R 3974, 3975, 3977; IBSP6403–6404, 25288- 25289, 31879, 32677, 44235, 58709, 59055, 59187, 59964, 60481, 62141, 62802, 71915, 71929–71930; MZUSP 10661, 12092; MCZ 142576 6403– 6405 IBSP 73549 IBSP 72489 IBSP IBSP 55927 IBSP (2010)

(2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2010) (2007) et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. Centeno Source Centeno (Dixon & Kofron, 1983) Araújo Centeno Centeno Freire Centeno Centeno Centeno Centeno Dixon & Kofron (1983); Centeno Amaral (1954); Dixon & Kofron (1983) Centeno Centeno Centeno Centeno 6.9339 -47.5554 -49.5822 -48.7500 -46.8489 -4 -47.2989 -46.9028 -46.8839 -47.1828 -49.9464 -46.4608 -46.7919 -46.8083 -49.8708 -48.7234 -49.3844 -47.5239 Longitude -47.5554 -20.4733 -24.5333 -23.7169 -23.5489 -23.2639 -23.5278 -23.1858 -23.5458 -49.9464 -23.6678 -23.5328 -23.5250 -22.9678 -48.7234 -49.3844 -23.2150 Latitude Localidade 1 Parque Estadual Turístico do Alto do Estadual Turístico Parque Vila Quitaúna Vila 1 1 1 Marília Municipality/City, Municipality/City, Iguape Iporanga Iporanga, Ribeira Itapecerica da Serra Itapevi Itú Jandira Jundiaí Mairinque Mauá Osasco Osasco, Ourinhos Paranapanema Piraju Porto Feliz SP State/Province SP SP SP SP SP SP SP SP SP SP SP SP SP SP SP SP Brasil Country Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3). 2015 249 Table 1 (cont.) Table Voucher 17756 IBSP 55978 IBSP 42736 IBSP 41532 IBSP 63077 IBSP 43658 IBSP 16365 MCT DU R BM 1946.1.11.12; 13634, 3978, 3979; IBSP 17345, 17842, 18745, 19577, 20871, 22446, 23748, 26629, 27867, 30403, 32428, 32732, 34494, 42271,42422, 42709, 42886, 43817, 43881, 44091, 44348, 45317, 46102, 50044, 53395, 53639, 58948, 60557, 60929, 60940, 61935, 62010, 62027, 62099, 62662, 62676, 62705, 2859, 62944, 63017, 68356, 68682, 70206, 72649, 72797, 72924, 73342, 74105, 74185, 74477, 75354, 75355; MNRJ 10577; 2083, 2359, 6451, MZUSP 6613, 12393

et al. (2008); Freire ; (2010) (2010) (2010) (2010) (2010) (2010); et al. (2011) et al. et al. et al. et al. et al. et al. Haad ; et al. Source (Dixon & Kofron, 1983) Centeno Centeno Centeno Centeno Centeno This study Amaral (1954); Dixon & Kofron (1983) (2007) Centeno Barbo -51.3889 -47.8417 -46.5275 -50.7224 -52.9556 -46.9229 -46.5508 -46.6358 Longitude -22.1258 -24.4962 -23.7808 -21.7265 -22.4672 -46.9229 -23.6228 -23.5478 Latitude 1 Localidade 3 1 Porto Primavera 1 Municipality/City, Municipality/City, Presidente Prudente Registro Riacho Grande Rinópolis Rosana, Santana do Parnaíba São Caetano do Sul São Paulo State/Province SP SP SP SP SP SP SP SP Country Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil 250 Costa et al.: Geographic distribution of Liotyphlops beui Table 1 (cont.) Table (2011) present (2011) et al. et Barbo 3 Voucher 282, 652, 1032, 1041, IBSP 1806, 3018–3020, 3024, 3025, 3289, 3799, 5120, 7533, 7568 17305 ISBP 4790 IBSP 17000 IBSP 16366 MCT 16368 MCT 16367 MCT 42515, 43618, 61946 IBSP 43618 IBSP 42318 ISBP 22416, 27646-27648, IBSP 42757, 44129, 44131, 44133, 44139, 44143 22377, 22712, 43664, IBSP 55334, 59335, 62943, 63599, 64468, 72517 MNHG (PE) 736 (2008); (2010) (2010) (2010) (2010) (2010) et al. (2008); Centeno et al. et al. et al. et al. et al. et al. (2010)

Proximate coordinates were used because the toponym the were used because coordinates Proximate 4 Source Amaral (1924); Amaral (1954); Haad Centeno Dixon & Kofron (1983) Amaral (1954); Dixon & Kofron (1983) Dixon & Kofron (1983) This study This study This study Centeno Centeno Centeno Centeno Haad et al. Dixon & Kofron (1983) -46.7192 -46.7168 -46.7506 -46.6869 -46.6404 -46.7192 -46.7327 -47.1350 -47.0399 -47.0604 -47.4578 -46.7528 -54.6035 Longitude -23.5678 -23.5840 -23.5442 -23.5750 -23.5533 -23.6007 -23.5785 -23.5289 -23.5374 -23.5778 -23.5019 -23.6019 -25.5099 Latitude 4

1 (2001), we used general coordinates for high elevation areas of the Itajaí river basin. river Itajaí of the areas elevation for high coordinates general (2001), we used Localidade et al. et Puente Stroessner São João Novo Grande, Fazenda Caitê Vargem Butantã Caxingui Jaguaré Paulistano Jardim Providência Jardim Morumbi Gomes Vila (2010) but not cited in their appendix. Specific informarion was given to us by F. C. Centeno and G. Puorto (Instituto Butantan). Butantan). (Instituto Puorto G. and Centeno C. F. by us to given was informarion Specific appendix. their in cited not but (2010) et al. was not found. Municipality/City, Municipality/City, São Paulo, São Paulo, São Paulo, São Paulo, São Paulo, São Paulo, São Paulo, São Roque São Roque, São Roque, Sorocaba da Serra Taboão Ciudad del Este, from several districts of the city of São Paulo, but no locality names were given. names but no locality of São Paulo, city of the districts from several L. beui State/Province SP SP SP SP SP SP SP SP SP SP SP SP Record mapped by Centeno 1

Country Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Brasil Paraguai Since no specific localities were given by Bérnils by given were localities specific no Since Notes: 2 a map with records of Grande, Fazenda Caitê Vargem Bol. Mus. Biol. Mello Leitão (N. Sér.) 37(3). 2015 251

Acknowledgements

To Fernanda C. Centeno for information about her data of Liotyphlops beui, and Giuseppe Puorto for collection numbers of some of Instituto Butantan’s specimens. To Gláucia M. F. Pontes (MCT) for access to specimens under her care. To Leonardo E. Lopes (Universidade Federal de Viçosa, Campus Florestal) for sending the specimens from Pará de Minas to HCC, and to Paulo C. A. Garcia (UFMG) for agreeing to deposit those snakes in the UFMG collection. We are also grateful to Roberta R. Pinto and one anonymous reviewer for comments on the manuscript.

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