zootaxa

Zootaxa 1393: 19–26 (2007) www.mapress.com/ zootaxa/

ISSN 1175-5326 (print edition)

Copyright © 2007 · Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

A new species of Liotyphlops (Serpentes: Anomalepididae) from the Atlantic Rain Forest of Northeastern Brazil ELIZA MARIA XAVIER FREIRE1, ULISSES CARAMASCHI2 & ANTÔNIO JORGE SUZART ARGÔLO3 1 Departamento de Botânica, Ecologia e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário, 59072-970 Natal, RN, Brasil. E-mail: [email protected]. 2 Departamento de Vertebrados, Museu Nacional/UFRJ, Quinta da Boa Vista, 20940-040 Rio de Janeiro, RJ, Brasil. E-mail: ulisses @acd.ufrj.br 3 Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna Km 16, Salobrinho, 45650-000 Ilhéus, BA, Brasil. E-mail: [email protected]

Abstract A new species of the genus Liotyphlops, known from three localities in the states of Alagoas and Bahia, in the Atlantic Rain Forest of Northeastern Brazil, is described. Liotyphlops trefauti sp. nov. is distinguished from all other species of the genus by the following combination of characters: four scales contacting the posterior edge of prefrontal; one scale contacting the posterior edge of nasal, between the second supralabial and the frontal; five scales in the first vertical row of lateral head scales; 22-22-22 scales around body; 520–543 dorsal scales; 499–532 ventral scales; absence of eye spot; and dorsal and ventral color bright yellowish-brown to reddish-brown. Key words: Serpentes; Anomalepididae; Liotyphlops trefauti sp. nov.; Atlantic Rain Forest; Taxonomy

Resumo Descreve-se uma nova espécie do gênero Liotyphlops, conhecida de três localidades nos Estados de Alagoas e Bahia, na Floresta Atlântica do nordeste do Brasil. Liotyphlops trefauti sp. nov. é distingüida de todas as outras espécies do gênero pela seguinte combinação de caracteres: quatro escamas em contacto com a borda posterior da prefrontal; uma escama em contacto com a borda posterior da nasal, entre a segunda supralabial e a prefrontal; cinco escamas na primeira fileira vertical de escamas da lateral da cabeça; 22-22-22 escamas ao redor do corpo; 520–543 escamas dorsais; 499–532 escamas ventrais; mancha ocular ausente; colorido dorsal e ventral em brilhante marrom amarelado a marrom avermelhado. Palavras-chave: Serpentes; Anomalepididae; Liotyphlops trefauti sp. nov.; Floresta Atlântica; Taxonomia

Introduction The Brazilian Atlantic Rain Forests are among the most endangered biodiversity hotspots in the world (Mittermeyer et al. 1999; Myers et al. 2000); the remainder does not exceed 6% of its original area and most of this is located in southeastern Brazil. In northeastern Brazil the forest has been almost completely cleared for sugar cane farming and cattle ranching (Coimbra-Filho and Câmara 1996; Freire 2001). Nevertheless, several new species of reptiles and amphibians have been described from these areas (Cruz et al. 1999; Freire 1999; Ferrarezzi and Freire 2001; Peixoto et al. 2003; Rodrigues et al. 2005). Currently, the Anomalepididae, a primitive family of blind snakes, is composed of four genera (Anomale-

Accepted by P. David: 23 Nov 2006; published: 18 Jan. 2007

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pis Jan, 1860, Helminthophis Peters, 1860, Liotyphlops Peters, 1860, and Typhlophis Fitzinger, 1843) and encompasses 16 species (4 Anomalepis, 3 Helmintophis, 7 Liotyphlops, 2 Typhlophis; Uetz et al. 1995–2006), distributed from southern Middle America (Nicaragua, Costa Rica, and Panama), northwestern South America (Colombia, Equador, and Peru), and Brazil to Paraguay and northern Argentina. The genus Liotyphlops is the most speciose in the family and currently is composed by seven species: L. albirostris (Peters, 1857), L. anops (Cope, 1899), L. argaleus Dixon and Kofron, 1984, L. beui (Amaral, 1924), L. schubarti Vanzolini, 1948, L. ternetziii (Boulenger, 1896), and L. wilderi (Garman, 1883) (Dixon and Kofron 1984; McDiarmid et al. 1999). In this paper we describe a new species of Liotyphlops from the Atlantic Rain Forest of northeastern Brazil.

Materials and methods Specimens examined are deposited in the Museu de Zoologia, Universidade de São Paulo, São Paulo, SP, Brazil (MZUSP), Museu Nacional, Rio de Janeiro, RJ, Brazil (MNRJ), and Coleção Herpetológica of the Departamento de Botânica, Ecologia e Zoologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil (CHBEZ); specimens examined are referred in the Appendix I. Terminology of head scales and counts follow Amaral (1954) and Dixon and Kofron (1984).

Liotyphlops trefauti sp. nov. (Fig. 1 A–E) Holotype. MZUSP 12178, male, collected at Fazenda Bananeira, Municipality of Murici (9°14’S, 35°48’W, 640 m elevation), State of Alagoas, Brazil, on 04 November 1994 by E. M. X. Freire. Paratype. MZUSP 12179, female, collected at Regional Center of the CEPLAC (Comissão Executiva do Plano da Lavoura Cacaueira), Municipality of Ilhéus (14°46’S, 39°13’W; 50 m elevation), State of Bahia, Brazil, on 29 January 1992, by C. Jared, M. Antoniazzi, and L. Ferreira. Referred specimen. CHBEZ 649, young, collected at Mata da Cachoeira (09o00’S, 36o03’W; 437 m elevation), Usina Serra Grande, Municipality of São José da Lage, State of Alagoas, Brazil, on 25 October 2003, by E. M. X. Freire. Diagnosis. Liotyphlops trefauti sp. nov. is distinguished from all other species of the genus by the following combinations of characters: (1) four scales contacting the posterior edge of prefrontal; (2) one scale contacting the posterior edge of nasal, between the second supralabial and the prefrontal; (3) five scales in the first vertical row of lateral head scales; (4) 22-22-22 scales around body; (5) 520–543 dorsal scales; (6) 499– 532 ventral scales; (7) absence of eye spot; (8) dorsal and ventral color bright yellowish to reddish brown. Comparisons with other species. The presence of four scales contacting the posterior border of prefrontal approximates L .trefauti sp. nov. to the Colombian species L. anops and L. argaleus; however, L. trefauti sp. nov. presents one scale contacting the posterior border of nasal, between the second supralabial and the prefrontal (two scales in L. anops and L. argaleus) and 22-22-22 scales around the body (27-24-23 to 28-2424 in L. anops, 26-22-22 to 28-24-22 in L. argaleus; Dixon and Kofron, 1984; Table 1). Additionally, L. trefauti sp. nov. has dorsal and ventral color bright yellowish to reddish brown, while L. anops has all body scales pigmented although the brown pigment of each scale is confined to the posterior one third to one fourth of each scale and the rostral, nasal, and prefrontal areas, and the anal and caudal tip areas are whitish (Dixon and Kofron, 1984), and L. argaleus is uniform dark brown with the posterior one third of each scale with a transverse blackish brown spot, anterior two thirds of each scale dark gray, anal area and caudal spine whitish,

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and rostral and nasal areas pinkish white (Dixon and Kofron, 1984). Liotyphlops trefauti sp. nov. differs from L. albirostris, L. beui, L. schubarti, L. ternetzii, and L. wilderi by having four scales contacting the posterior border of prefrontal (three scales in those species) and higher number of dorsals scales, 520–543 (L. albirostris, 370–455; L. beui, 375–464; L. schubarti, 372–387; L. ternetzii, 463–510, and L. wilderi, 304–358; Dixon and Kofron, 1984; our data). TABLE 1. Comparative diagnostic characters for the species of Liotyphlops (Dixon and Kofron 1984; our data). L. argaleus

L. anops

L. trefauti sp. nov. L. albirostris

Scales number contacting posterior edge of prefrontal

4

4

4

3

Scales number contacting posterior edge of nasal between second supralabial and prefrontal

2

2

1

1

Eye spot

little visible or ausent

absent

absent

little visible

Scales number in the first vertical row of dor- 5 sals

6

5

5

Scales rows around body

26–28/22–24/ 22

27–28/22–24/23– 24

22/22/22

24–26/22/22

Scales rows dorsals

351–533

548 or more

520–543

370–455

Total length (mm)

101–261

125–395

366–389

70–233

L. beui

L. schubarti

L. ternetzii

L. wilderi

Scales number contacting posterior edge of prefrontal

3

3

3

3

Scales number contacting posterior edge of nasal between second supralabial and prefrontal

2

2

2

1

Eye spot

little visible

little visible

evident

evident

Scales number in the first vertical row of dor- 5 sals

5

5

5

Scales rows around body

22/20/20

22/20/20

22/24/22

22/20/20

Scales rows dorsals

375–464

372–387

463–510

304–358

Total length (mm)

106–381

80–245

88–413

68–290

continued.

Description of the holotype. Rostral large, higher than wide, contacting anterolaterally nasals, laterally prefrontals, and posteriorly the single frontal, which prevents the prefrontals from contacting each other. Prefrontals pairs triangulars, bordered anteriorly and laterally by the rostral, ventrally by the large divided nasal, and dorsoposteriorly partially by the single frontal. Posterior edge of prefrontal passing in front of frontal. In lateral view, four scales contact posterior edge of prefrontal, including the frontal and three scales that lie between the frontal and the second supralabial. One scale bordering the posterior edge of nasal between second supralabial and prefrontal. Divided nasal scale bordered anteriorly by the rostral, dorsally by the prefrontal, ventrally by the first and second supralabials, and posteriorly by a scale that lie between the second supralabial and prefrontal. Five scales in the first vertical row of lateral head scales, consisting of the second supralabial, the frontal, and three scales one above the other in between, namely one supraocular, one ocular, and one subocular, respectively. Eye spot absent. Supralabials 4–4; infralabials 4–4. Dorsals, laterals, and ven-

A NEW SPECIES OF LIOTYPHLOPS (SERPENTES)

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trals scales of body and tail smooth; no enlarged ventral plates. Scales around body 22-22-22; dorsals 543; ventrals 531; subcaudals 8. In life, dorsal and ventral color uniform bright yellowish brown; in preservative, the color faded to uniform yellowish brown. Total length 362 mm; tail length 4 mm. Variation. The female paratype, in life, had dorsum and venter bright reddish brown (Fig. 2); dorsals 520; ventrals 499; total length 385 mm.

FIGURE 1. Liotyphlops trefauti sp. nov. (MZUSP 12178, holotype). (A) Dorsal view of head. (B) Lateral view of head. (C) Ventral view of head. (D) Ventral view of tail. (E) Lateral view of tail. Bar = 2 mm.

Habitat and habits. The holotype of L. trefauti sp. nov. was collected at Fazenda Bananeira, in Murici, Alagoas, where is located one of the biggest and currently the more significative remaining spot of the Atlantic Rain Forest in Northern and Northeastern Brazil. With about 1,200 hectares and 640 meters in elevation, it is covered by a dense forest with a canopy up to 40 meters high. The closed canopy maintains the shadow and humidity inside the forest. The low-growing layer is composed by plantules of the arboreal regeneration, some palms, and large number of lianes and epiphyte plants. The litter is thick and moist. Surrounding the Murici Forest are extensive sugar cane plantations and these isolate completely the forest island from all other similar forest spots. The specimen was collected at 12:30h. through active search inside the thick and moist litter around the trunk of a large tree in the forest.


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FIGURE 2. Liotyphlops trefauti sp. nov. (MZUSP 12179, paratype), in life.

The paratype was collected at the CEPLAC Regional Center in Ilhéus, Bahia, in a cocoa plantation shadowed by the former high Atlantic Rain Forest. The specimen was obtained also by active search in the thick and moist litter, at 10:00h. Another specimen was seen on the same day and in the same area, inside the nest of ants of the genus Acromyrmex (Hymenoptera, Formicidae), but the efforts to collect it failed. The very young and poorly preserved referred specimen was collected in the thick and moist litter of the Mata da Cachoeira, a secondary forest island of about 100 hectares and 437 meters in elevation inside a large matrix of sugar cane plantation. Geographical distribution. The species is known from three localities in the Atlantic Rain Forest of Northeastern Brazil, in the states of Alagoas (Murici and São José da Lage) and Bahia (Ilhéus), 50 –640 m elevation. Etymology. The specific name, a noun in the genitive case, honors Miguel Trefaut Rodrigues, by his extensive contribution to the knowledge of the Brazilian herpetology. We are very glad in to prive his pleasant and profitable friendship.

Discussion The genus Liotyphlops was divided by Dixon and Kofron (1984) in three morphological groups, based on overall similarities of head scales arrangements but without phylogenetic implications. The first group, composed by L. anops and L. argaleus, presents the character of four scales bordering the posterior edge of the prefrontal (against three scales in the other species groups). The second group, encompassing L. albirostris and L. wilderi, shares the character of one scale contacting the posterior edge of the nasal between the second



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supralabial and prefrontal, while the third group, composed by L. beui, L. schubarti, and L. ternetzii, has two scales (character also present in the species of the first group). The species of the first group are distributed in Colombia (L. anops known only from the vicinity of Villavicencio, in the Meta Province, and L. argaleus in La Selva, Cundinamarca); the species of the second group occur far disjunctly in southern Central America and northern South America (L. albirostris) and in southeastern Brazil, in the states of São Paulo and Rio de Janeiro, and Paraguay; and the species of the third group are distributed in central and southern Brazil, in the states of Paraná to Mato Grosso, Paraguay, and Argentina, in Corrientes and possibly Misiones (L. beui), in southeastern Brazil, in the State of São Paulo (L. schubarti), and central to southern Brazil, in the states of Pará, Goiás, Distrito Federal, Mato Grosso, and São Paulo, and Paraguay (L. ternetzii) (McDiarmid et al. 1999). Liotyphlops trefauti sp. nov. presents four scales bordering the posterior edge of the prefrontal, which is shared with the species of the first group, but also shows one scale contacting the posterior edge of the nasal between the second supralabial and prefrontal, a character of the second group. This demonstrates the weakness and artificiality of the groups proposed by Dixon and Kofron (1984), besides its utility in alpha taxonomy approaches. Regarding the geographical distribution, the new species extends the genus to northeastern Brazil, in the States of Alagoas and Bahia. To the present, it is the unique species of Liotyphlops in the Atlantic Rain Forest of that region.

Acknowledgments We thank Selma T. Silva, for her valuable help in the field. Carlos Jared, Marta Antoniazzi, and Luis Ferreira by collecting the paratype. Gabriel Skuk for the line drawings. Ronaldo Fernandes and Paulo Passos for reviewing the manuscript. UC and EMXF acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the fellowships and financial support.

Literature cited Amaral, A. (1954) Contribuição ao conhecimento dos ofidios do Brasil. 12. Notas a respeito de Helminthophis ternetzii Boulenger, 1896. Memórias do Instituto Butantan, 26, 191–195. Coimbra-Filho, A.F. & Câmara, I.G. (1996) Os limites originais do Bioma Mata Atlântica na Região Nordeste do Brasil. Rio de Janeiro: Fundação Brasileira para a Conservação da Natureza. 86 pp. Cruz, C.A.G., Caramaschi, U. & Freire, E.M.X. (1999) Occurrence of the genus Chiasmocleis (Anura: Microhylidae) in the State of Alagoas, north-eastern Brazil, with a description of a new species. Journal of Zoology, 249, 123–126. Dixon, J.R. & Kofron, C.P. (1984 [1983]) The Central and South American anomalepid snakes of the genus Liotyphlops. Amphibia-Reptilia, 4, 241–264. Ferrarezzi, H. & Freire, E.M.X. (2001) New species of Bothrops Wagler, 1824 from the Atlantic Forest of Northeastern Brazil (Serpentes, Viperidae, Crotalinae). Boletim do Museu Nacional, Nova Série, Zoologia, 440, 1–10. Freire, E.M.X. (1999) Espécie nova de Coleodactylus Parker, 1926 das dunas de Natal, Rio Grande do Norte, Brasil, com notas sobre suas relações e dicromatismo sexual no gênero (Squamata, Gekkonidae). Boletim do Museu Nacional, Nova Série, Zoologia, 399, 1–14. Freire, E.M.X. (2001) Composição, taxonomia, diversidade e considerações zoogeográficas sobre a fauna de lagartos e serpentes de remanescentes da Mata Atlântica do Estado de Alagoas, Brasil. Unpubl. PhD Thesis. Programa de Pósgraduação em Zoologia, Museu Nacional, UFRJ, Rio de Janeiro. 96 pp. McDiarmid, R.W., Campbell, J.A. & Touré, T’S.A. (1999) Snake Species of the World. A Taxonomic and Geographic Reference. Volume 1. The Herpetologists’ League, Washington, xii+511 pp. Mittermeyer, R.A., Myers, N., Robles, P. & Mittermeyer, C.G. (1999) Hotspots: Earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX - Agrupación Sierra Madre, Mexico City. Myers, N., Mittermeyer, R.A., Mittermeyer, C.G., Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. Peixoto, O.L., Caramaschi, U. & Freire, E.M.X. (2003) Two new species of Phyllodytes (Anura, Hylidae) from the State


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of Alagoas, Northeastern Brazil. Herpetologica, 59, 235–246. Rodrigues, M.T., Freire, E.M.X., Pellegrino, K.C.M. & Sites, Jr., J.W. (2005) Phylogenetic relationships of a new genus and species of microteiid lizard from the Atlantic forest of north-eastern Brazil (Squamata, Gymnophtalmidae). Zoological Journal of the Linnean Society, 144, 543–557. Uetz, P., Etzold, T. & Chenna, R. (1995–2006) The EMBL Reptile Database. Available from: www.embl-heidelberg.de/ ~uetz/LivingReptiles.html. Access on 14 November 2006.



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Appendix 1. Specimens examined Liotyphlops albirostris. VENEZUELA: Caracas (MNRJ 3172). Liotyphlops beui. BRAZIL: State of Mato Grosso do Sul: Barra do Bugres (MNRJ 7854). State of São Paulo: Campinas (MNRJ 8143); Carapicuíba (MNRJ 10578); Itú (MNRJ 8144–8146); São Paulo (MNRJ 10577). State of Paraná: Foz do Iguaçu (MNRJ 383, 384). Liotyphlops schubarti. BRAZIL: State of São Paulo: Pirassununga, Cachoeira de Emas (MZUSP 2595, holotype). Liotyphlops ternetzii. BRAZIL: Distrito Federal: Brasília (MZUSP 6461). State of Minas Gerais: João Pinheiro (MNRJ 11329); Nova Ponte, UHE Miranda (MNRJ 8147); Rio Preto, UHE Queimado (MNRJ 10032–10033). Liotyphlops wilderi. BRAZIL: State of Minas Gerais: Caeté, Alto da Serra da Piedade (MZUSP 3842). State of Rio de Janeiro: Angra dos Reis, Ilha Grande (MNRJ 7853); Paraty (MNRJ 1814).


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