Ecologia de uma assembléia de serpentes no semiárido neotropical

Texto

(1)UNIVERSIDADE FEDERAL DE SANTA MARIA CENTRO DE CIÊNCIAS NATURAIS E EXATAS PROGRAMA DE PÓS-GRADUAÇÃO EM BIODIVERSIDADE ANIMAL. ECOLOGIA DE UMA ASSEMBLÉIA DE SERPENTES NO SEMIÁRIDO NEOTROPICAL. TESE DE DOUTORADO. Paulo Cesar Mattos Dourado de Mesquita. Santa Maria, RS, Brasil 2013.

(2) PPGBA/UFSM,RS. MESQUITA, Paulo Cesar Mattos Dourado de. Doutor. 2013.

(3) ECOLOGIA DE UMA ASSEMBLÉIA DE SERPENTES NO SEMIÁRIDO NEOTROPICAL. Paulo Cesar Mattos Dourado de Mesquita. Tese apresentada ao Programa de Pós-Graduação em Biodiversidade Animal, da Universidade Federal de Santa Maria, como requisito parcial para obtenção do título de Doutor em Ciências Biológicas – Área Biodiversidade Animal.. Orientadora: Sonia Zanini Cechin. Santa Maria, RS, Brasil 2013.

(4)

(5) Universidade Federal de Santa Maria Centro de Ciências Naturais e Exatas Programa de Pós-Graduação em Biodiversidade Animal. A comissão examinadora, abaixo assinada, aprova a Tese de Doutorado: Ecologia de uma assembléia de serpentes no semiárido neotropical. Elaborada por Paulo Cesar Mattos Dourado de Mesquita como requisito para obtenção do título de Doutor em Ciências Biológicas – Área Biodiversidade Animal COMISSÃO EXAMINADORA:. Santa Maria, 18 de fevereiro de 2013.

(6) AGRADECIMENTOS Este trabalho é resultado da contribuição de muitas pessoas que de forma direta ou indireta contribuíram para meu crescimento profissional e pessoal. Por isso deixo meus sinceros agradecimentos: À minha querida Sherida, pelo amor, carinho, dedicação paciência e companheirismo durante todo o desenvolvimento do trabalho e durante todos os dias de convivência. Aos meus pais Paulo e Regina por serem o exemplo de retidão e honra que procuro seguir, por sempre me apoiarem em minhas decisões e por estarem sempre dispostos a ajudar nas situações difíceis, se mantendo por perto mesmo que geograficamente distantes. À minhas irmãs Sophia e Flora por porem em práticas os valores de uma família forte e unida. À minha orientadora Sonia Cechin pelo exemplo inspirador de ética científica, por ter acreditado em meu potencial, por ter confiado em meu trabalho e pelas ricas contribuições a esta obra. Aos amigos do laboratório Bruno, Victor, Carol, Daniel Cassiano, George, Miguel, Vinícius, Camila, Tailise, Leonan, Carlos, Samanta, Fran, Rubinho, Tiago, Débora, Juliano, Henrique, Maurício pela recepção amigável, convivência saudável e energia sempre ‘pra cima’! Mais uma vez à Fran, Samanta, Tiago e Daniel Cassiano pelas conversas, ideias e sugestões instigantes, inspiradoras e, por vezes, polêmicas que contribuíram muito com o resultado final desta tese e com meu crescimento como pesquisador. Mais uma vez à Carol Pietczak por apoiar minha curiosidade e fazer surgir trabalhos paralelos enriquecedores. Ao George Sá-Polidoro por ser um aluno dedicado e responsável em vários projetos paralaelos o que facilitou meu trabalho como coorientador. À Diva Borges-Nojosa, Daniel Passos, Castiele Bezerra, Fabrício Rodrigues, Wallony Brito e a toda equipe do NUROF, pela contribuição durante os campos, pelas conversas, risadas e todo o aprendizado que devo a vocês. Ao Célio, Seu Walmir e Dona Betina pela grande parceria em campo, receptividade o que tornou o trabalho muito mais fácil. Aos doutores Teresa Cristina Ávila-Pires, Maria da Graça Salomão, Ewerton Behr, Gisele Winck e Noeli Zanella pelas contribuições fundamentais ao primeiro capítulo desta tese durante qualificação e revisão de manuscrito em periódico. Ao doutor Luca Luiselli pelos importantes e positivos comentários que ajudaram a melhorar o terceiro capítulo desta tese. Aos meus amigos Tasso Junior, Simone Linhares, Matheus Rios e Marina Viana por sempre terem me mantido por perto mesmo quando eu estive distante. Aos meus professores: Sonia Cechin, Nilton Cáceres, Adriano Melo, Eduardo Paes, José Ricardo I. Ribeiro, Tiago G. Santos, Ronald Souza, Tatiana Kuplich que de forma direta ou indireta influenciaram minha forma de pensar através do conhecimento transmitido. Às serpentes pelo fascínio e mistério que parecem ser infinitos, apesar de todo estudo e conhecimento gerado... ... e tantas outras pessoas que estiveram ao meu lado ao longo desta caminhada. Certamente não lembrei todos que deveriam estar aqui, mas os que não foram citados nominalmente sintam-se incluídos no “e tantas outras pessoas”. Muito obrigado!.

(7) “O sertanejo é antes de tudo um forte” (Guimarães Rosa).

(8) RESUMO Neste trabalho apresentamos em quatro capítulos um estudo sobre a ecologia das serpentes de uma assembléia do semiárido brasileiro. O primeiro capítulo versa sobre a eficiência de quatro métodos tradicionais de amostragem de serpentes: procura visual limitada por tempo, encontros ocasionais, encontros ocasionais por terceiros e armadilhas de pitfall com cercasguia. Concluímos que a utilização concomitante dos métodos é eficiente e complementar em relação à determinação da riqueza de uma área, porém se o objetivo do estudo estiver relacionado à abundância ou estrutura de assembléia, os métodos podem ser sobrepostos e a utilização em conjunto deve ser cautelosa. No segundo capítulo apresentamos de forma descritiva as características de autoecologia de cada uma das 22 espécies de serpentes que foram registradas na área de estudo. Durante este estudo a maior parte dos indivíduos foi representada pelas espécies Oxybelis aeneus e Philodryas nattereri. O terceiro capítulo versa sobre os efeitos das interações interespecíficas sobre a estruturação da assembléia. Neste capítulo evidenciamos a existência de estruturas de guildas alimentares, espaciais e temporais através de uma abordagem de modelos nulos, sendo a guilda alimentar a mais importante na segregação de nichos entre as espécies da área. No quarto capítulo investigamos como variáveis climáticas e disponibilidade de presas afetam a estruturação da assembléia de serpentes. Evidenciamos que embora não haja um padrão global de resposta, variáveis relacionadas à temperatura e disponibilidade de presas, são as que influenciam um maior número de espécies de serpentes no semiárido do Brasil.. Palavras-chave: ecologia de comunidade, modelos nulos, interações, répteis.

(9) ABSTRACT Herein we present a four chapter study on the ecology of a snake assemblage from the Brazilian semi-arid. The first chapter is the comparison of the efficiency of four traditional methods used to sample snakes: time-constrained search, occasional encounters by the staff, occasional encounters by thirds and pitfall traps with drift-fences. We conclude that the concomitant use of these methods is effective and complementary to determine the species richness of an area, but if the objectives are related to species abundance or assemblage structure the methods may be overlaid and the use of these methods together should be cautious. In the second chapter we present a summarized descriptive autoecology of the 22 species of snakes found in the study area. During this study most individuals were represented by Oxybelis aeneus and Philodryas nattereri. The third chapter deals with the effects of interspecific interactions on the structure of the assemblage. In this chapter we indicate, through a null model approach, the existence of dietary, spatial and temporal guilds. The dietary guild seems to be the most important niche dimension segregated by the snakes in the area. The fourth chapter is an investigation on how climate and prey availability affect the structure of the snake assemblage. We show that although there is no overall pattern of response, predictors related to temperature and prey availability are those that influence a greater number of species in the area. Keywords: community, ecology, null models, interactions, reptiles.

(10) SUMÁRIO INTRODUÇÃO GERAL ................................................................................................ 11 Problemática regional .................................................................................................. 11 Problemática em métodos ecológicos ......................................................................... 12 Implicações conservacionistas .................................................................................... 13 Referências .................................................................................................................. 14. CAPÍTULO 1 - Efficiency of snake sampling methods in the Brazilian semiarid region17 Abstract .................................................................................................................... 19 Introduction.............................................................................................................. 20 Material and methods .............................................................................................. 22 Results...................................................................................................................... 25 Discussion ................................................................................................................ 28 Legends to the figures .............................................................................................. 35 Acknowledgments ................................................................................................... 36 Resumo .................................................................................................................... 37 References................................................................................................................ 38 Figures ..................................................................................................................... 45. CAPÍTULO 2 - Ecologia e história natural das serpentes de uma área de Caatinga no nordeste brasileiro ..................................................................................................................... 49 Abstract .................................................................................................................... 51 Resumo .................................................................................................................... 52 Introdução ................................................................................................................ 53 Material e métodos .................................................................................................. 53 Resultados ................................................................................................................ 57 Discussão ................................................................................................................. 74 Conclusões ............................................................................................................... 75 Agradecimentos ....................................................................................................... 75 Literatura Citada ...................................................................................................... 77 Tabelas ..................................................................................................................... 86 Figura ....................................................................................................................... 93.

(11) CAPÍTULO 3 – Do snake assemblages from semiarid Caatinga biome partition the available resource? .................................................................................................................... 97 Abstract ................................................................................................................... 99 Introduction ........................................................................................................... 100 Material and methods ............................................................................................ 101 Results ................................................................................................................... 105 Discussion ............................................................................................................. 107 Acknowledgements ............................................................................................... 111 References ............................................................................................................. 112 Figure 1 ................................................................................................................. 118 Supplementary materials ....................................................................................... 123. CAPÍTULO 4 – “Is temperature really unimportant for tropical snakes?” Effects of climate and prey availability in a snake assemblage in neotropical semiarid ...................... 125 Abstract ................................................................................................................. 127 Introduction ........................................................................................................... 128 Material and methods ............................................................................................ 131 Results ................................................................................................................... 134 Discussion ............................................................................................................. 136 Acknowledgements ............................................................................................... 140 References ............................................................................................................. 141 Figures ................................................................................................................... 148 Tables .................................................................................................................... 151. CONCLUSÃO GERAL ............................................................................................... 153.

(12)

(13) 11. INTRODUÇÃO GERAL. O termo comunidade biológica é utilizado para descrever um conjunto de organismos que coexistem em um local, em um dado tempo. Existem diferentes maneiras para realizar o estudo de comunidades, com base em três critérios principais: espaciais, tróficos e taxonômicos (UNDERWOOD, 1986). O critério espacial é o mais amplo e complexo dos três, pois pode incluir todos os organismos existentes em uma determinada área. O critério trófico inclui nos estudos somente as espécies que exploram de modo semelhante uma base comum de recursos alimentares, a despeito de haver ou não relação taxonômica entre elas. E o terceiro critério, o taxonômico, inclui nos estudos, entre todas as espécies de um determinado. local,. apenas. aquelas. que. são. taxonomicamente. relacionadas,. independentemente do modo como interagem entre si ou exploram os recursos disponíveis. Esta definição é também conhecida por taxocenose. As serpentes, por possuírem grande importância ecológica como predadoras (POUGH et al, 2003), e devido ao grupo apresentar grande plasticidade na ecologia e história natural, se mostram importantes objetos de estudo para ecologia de comunidades, podendo ser utilizadas como organismos modelo para o teste de diversas teorias ecológicas (SHINE & BONNET, 2000). Problemática regional O domínio Caatinga é um mosaico de arbustos espinhosos e florestas sazonalmente secas que, ao longo dos anos vem sofrendo impactos antrópicos especialmente pelo uso inadequado do solo (LEAL et al, 2005) gerando o processo de desertificação que é o principal processo responsável pela perda de biodiversidade neste bioma (TRIGUEIRO et al, 2009). Castelleti et al (2004) estimam que entre 30,4% e 51,7% do bioma já foi alterado por atividades antrópicas. Apesar destes números alarmantes, este bioma recebe pouco investimento em pesquisa e por este motivo ainda se mantém como o bioma menos estudado no Brasil e a maioria dos estudos estão concentrados em alguns poucos pontos dentro do bioma (SANTOS et al, 2011). Além disso, somente cerca de 2% da Caatinga está protegida em Unidades de Conservação, indicando que além de muito degradado é um bioma pouco protegido..

(14) 12. Vanzolini et al (1980) publicaram o livro “Répteis das Caatingas” registrando e caracterizando 43 espécies de Squamata e três Chelonia para o bioma. Segundo os autores, a herpetofauna seria composta por espécies de grande distribuição sem a existência de elementos endêmicos para o bioma. Porém, esta premissa tem sido negada por diversos autores com a freqüente descrição de novas espécies (e.g. HOGE & LIMA-VERDE, 1973; RODRIGUES & JUNCÁ, 2003; PASSOS et al, 2007; ALBUQUERQUE, 2008) e a realização de levantamentos mais detalhados tem apresentado novos registros e muitos casos de endemismo. Rodrigues (2003; 2004) apresenta a fauna de répteis da caatinga representada por 116 espécies, sendo 52 serpentes. Diversos registros de distribuição geográfica e descrição de novas espécies fazem com que este número, atualmente, seja ainda maior (e.g. BORGES-NOJOSA, 2006; BORGES-NOJOSA et al 2006; PASSOS et al, 2007; BORGESNOJOSA et al, 2008). Os estudos sobre ecologia de comunidades de serpentes na caatinga são raros. Apenas dois estudos abordam este tema no bioma Caatinga de maneira ampla. Vitt e Vangilder (1983) abordaram análise de guildas alimentares das espécies ocorrentes em Exú, Pernambuco e, Guedes (2006) em sua dissertação de mestrado discutiu sobre as serpentes do sertão do Seridó no Rio Grande do Norte, comparando a amplitude de nichos e avaliando possíveis segregações de nicho que permitam a coexistência. Ambos os estudos foram realizados em regiões de Caatinga com fisionomias abertas. Vitt e Vangilder (1983) estudaram uma área com predominância de afloramentos rochosos e Costa (2006) estudou uma área de fisionomia predominantemente de caatinga arbustivo-herbácea. Neste estudo analisamos uma área de Caatinga mais densa, predominantemente arbustivo-arbórea. Problemática em métodos ecológicos Uma questão fundamental em ecologia é se existem ou não processos que determinam a estruturação das comunidades biológicas. O efeito de interações interespecíficas e de fatores ambientais tem sido levantados como importantes no processo de estruturação das comunidades. O problema dos estudos sobre estruturação de comunidades biológicas no Brasil é que, em geral, os pesquisadores têm assumido a existência de processos estruturais para descrever seus objetos de estudo sem de fato testar se estes processos são aleatórios. Comunidades estruturadas através de interações interespecíficas e por influência de fatores ambientais já foram demonstradas para alguns grupos animais como aves (DIAMOND et al, 1975), peixes.

(15) 13. (JACKSON et al, 1992) e anfíbios (SANTOS et al., 2009). Porém assumir este conceito, sem testá-lo, parece ser inapropriado para alguns grupos, especialmente no caso de animais como serpentes, que apresentam particularidades fisiológicas, passando longos períodos de inatividade e alimentando-se em intervalos maiores de tempo. Implicações conservacionistas Em tempos de mudanças climáticas existem cada vez mais evidências de que as populações de répteis se encontram em declínio generalizado ao redor do mundo (Reading et al, 2010; Brito et al, 2011, Mesquita et al, no prelo). Especialmente por causa de limitações provenientes da ectotermia que exigem condições adequadas para a ocupação dos ambientes por este grupo. Sabe-se que os ambientes tropicais apresentam o maior número de espécies de serpentes e também as assembléias com maior riqueza de espécies. Por isto é surpreendente que poucos trabalhos sobre ecologia de comunidades tenham sido desenvolvidos nos trópicos (Luiselli, 2006) e especialmente em um país megadiverso como o Brasil. Assim, o conhecimento sobre técnicas de amostragem, sobre a autoecologia das espécies que compõem a assembléia e sobre padrões e processos de estruturação de assembléias de serpentes tropicais são cruciais para uma melhor argumentação para implantação de planos de conservação. Nesta tese, apresentamos, em quatro capítulos, os estudos realizados em uma área do semiárido brasileiro abordando aspectos importantes para compreensão da ecologia de assembléias de serpentes. Cada capítulo apresenta-se editado conforme as instruções aos autores dos periódicos pretendidos para publicação e contam com colaboração e coautoria de diferentes pesquisadores de instituições nacionais e internacionais.. REFERÊNCIAS ALBUQUERQUE, N.R. 2008. Revisão taxonômica das subespécies de Leptophis ahaetulla (Linnaeus, 1758) (Serpentes, Colubridae). (Tese de Doutorado). Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre.BORGES-NOJOSA, D.M. Diversidade de anfíbios e répteis da Serra de Baturité, Ceará, p-225-247. In: OLIVEIRA, T.S. de; ARAÚJO, F.S. de (org.), Diversidade e Conservação da Biota na Serra de Baturité, Ceará. Edições UFC; COELCE. Fortaleza: 445 pp. 2006. p-225-247.

(16) 14. BORGES-NOJOSA, D. M.; LOEBMANN, D. ; LIMA, D. C. ; MELO, J. C. L.; MAI, A. C. G. Reptilia, Colubridae, Pseutes sulphureus: distribution extension, new state record.. Check List, 2: 79-81, 2006. BORGES-NOJOSA, D.M.; MESQUITA, P.C.M.D.; FERNANDES-FERREIRA, H. Helicops angulatus (Water’s snake) Geographic distribution. Herpetological Review. 39:485. 2008. BRITO, J.C., S. FAHD, F.MARTÍNEZ-FREIRIA, P. TARROSO, S.LARBES, J.M. PLEGUEZUELOS & X. SANTOS. Climate change and peripheral populations: predictions for a relict Mediterranean viper. Acta Herpetologica 6(1): 105-118. 2008. DIAMOND, J.M. Assembly of species communities, p.342-444 in: M.L. CODY; J. M. DIAMOND (eds) Ecology and evolution of communities. Harvard University. Cambridge, Massachussets, USA. 1975. GUEDES, T. Estrutura da comunidade de Serpentes de uma área de Caatinga do Nordeste brasileiro. 2006. 74 f. Dissertação (Mestre em Ciências Biológicas), Universidade Federal do Rio Grande do Norte, RN, 2006. HOGE, A.R.; LIMA-VERDE, J.S., Liophis mossoroensis sp. nov. from Brazil. (Serpentes: Colubridae). Memórias do Instituto Butantan, 36: 215-220. 1973. JACKSON, D.A.; SOMERS, K.M.; HARVEY, H.H. Null models and fish communities: Evidence of nonrandom patterns. The American Naturalist, 139(5): 930-951. 1992. LEAL, I.; SILVA, J.M.C; TABARELLI, M.; LACHER Jr, T.E. Mudando o rumo da conservação da biodiversidade na Caatinga do Nordeste brasileiro. Megadiversidade. 1(1): 139-146. 2005. LUISELLI, L. Resource partitioning and interspecific competition in snakes : the search for general geographical and guild patterns. Oikos, 114(2): 193-211. 2006. MESQUITA, P.C.M.D.; PIETCZAK, C.; PINHEIRO-MESQUITA, S.F. Are common species endangered by climate change? Habitat suitability projections for the royal ground snake, Liophis reginae (Serpentes, Dipsadidae). North-Western Journal of Zoology (no prelo). PASSOS, P.; FERNANDES, R.; BORGES-NOJOSA, D.M. A New Species of Atractus (Serpentes: Dipsadinae) from a Relictual Forest in Northeastern Brazil. Copeia. 2007(4): 788– 797. 2007..

(17) 15. POUGH, H. F.; R. M. ANDREWS; J. E. CADLE; M. L. CRUMP; A. H. SAVITZKY; K. D. WELLS. Herpetology. 3.Ed. New Jersey. Pearson Prentice-Hall, 2003. 736p. READING, C. J., LUISELLI, L. M., AKANI, G. C., BONNET, X., AMORI, G., BALLOUARD, J. M., FILIPPI, E., NAULLEAU, G., PEARSON, D., AND RUGIERO, L. 2010. Are snake populations in widespread decline? Biology Letters 6(6):777-780. RODRIGUES, M.T. Herpetofauna da Caatinga. In: LEAL, I.R; TABARELLI, M.; SILVA, J.M.C. (Org.) Ecologia e Conservação da Caatinga. Recife, PE. Universidade Federal de Pernambuco, 2003. p.181-236. RODRIGUES, M.T. Fauna de répteis e anfíbios das caatingas. In: SILVA, J.M.C.; TABARELLI, M.; FONSECA, M.T.; LINS, L.V. (Org) Biodiversidade da caatinga: áreas e ações prioritárias para conservação. Brasília, DF. Ministério do Meio Ambiente, 2004, p.173180. RODRIGUES, M.T.; JUNCÁ, F.A. Herpetofauna of the quaternary sand dunes of the middle Rio São Francisco: Bahia: Brazil. Vii. Typhlops amoipira sp. Nov., a possible relative of Typhlops yonenagae (serpentes, typhlopidae). Papéis Avulsos de Zoologia.. São Paulo,. 42(13): 325-333. 2003. SANTOS, J.C., LEAL, I.R., ALMEIDA-CORTEZ, J.S., FERNANDES, G.W., TABARELLI, M. 2011.Caatinga: the scientific negligence experienced by a dry tropical forest. Tropical Conservation Science 4(3): 276-286 SANTOS, T. G.; VASCONCELOS, T. S.; ROSSA-FERES, D. C.; HADDAD, C. F. B. Anurans of a seasonally dry tropical forest: Morro do Diabo State Park, São Paulo state, Brazil. Journal of Natural History, v. 43, p. 973–993, 2009. SHINE, R.; BONNET, X. Snakes: a new 'model organism' in ecological research? Tree, 15(6): 221-222. 2000. UNDERWOOD, A.J. What is a community? In: D.M. RAUP AND D. JABLONSKI (Eds) Patterns and Processes in the History of Life. Springer-Verlag, Berlin, Germany. 1986. p 351367. VANZOLINI, P.E.; RAMOS-COSTA, A.M.; VITT, L.I. Répteis das Caatingas. Rio de Janeiro. Cerifa, 1980. 161p..

(18) 16. VITT, L. J.; L. D. VANGILDER. Ecology of a snake community in northeastern Brazil. Amphibia-Reptilia 4: 273-296. 1983..

(19) 17. CAPÍTULO 1 - Efficiency of snake sampling methods in the Brazilian semiarid region (submetido ao periódico: Anais da Academia Brasileira de Ciências).

(20) 18. Efficiency of snake sampling methods in the Brazilian semiarid region Paulo Cesar Mattos Dourado Mesquita1,2, Daniel Cunha Passos3 , Sonia Zanini Cechin2 1. 2. paulocmdm@gmail.com (corresponding author) Laboratório de Herpetologia, Departamento de Biologia, Universidade Federal de Santa. Maria. Avenida Roraima, 1000. CEP 97105-900, Santa Maria, Rio Grande do Sul, Brazil 3. Núcleo Regional de Ofiologia, Universidade Federal do Ceará (NUROF-UFC), Campus do. Pici, Centro de Ciências, Bloco 905, CEP: 60455-760, Fortaleza, Ceará, Brazil Keywords: Caatinga, comparison, pitfall traps, Squamata, techniques Short title: Methods to sample snakes in the Brazilian semiarid region Academy section: Biological Sciences Corresponding author: Paulo Cesar Mattos Dourado Mesquita. Address: Laboratório de Herpetologia, Departamento de Zoologia, Universidade Federal de Santa Maria. Avenida Roraima, 1000. CEP 97105-900, Santa Maria, Rio Grande do Sul, Brazil. Phone: 55 (55) 3026 4349. E-mail: paulocmdm@gmail.com.

(21) 19. ABSTRACT The choice of sampling methods is a crucial step in every field survey in herpetology. In countries where time and financial support are limited, the choice of the methods is critical. The methods used to sample snakes often lack objective criteria, and the traditional methods have apparently been more important when making the choice. Consequently research using not-standardized methods is frequently found in the literature. We compared four commonly used methods for sampling snake assemblages in a semiarid area in Brazil. We compared the efficacy of each method based on the cost-benefit regarding the number of individuals and species captured, time, and financial investment. We found that pitfall traps were the less effective method in all the aspects that we evaluated and it was not complementary to the other methods in terms of abundance of species. We conclude that methods can only be considered complementary if they are standardized to the objectives of the study. The use of pitfall traps in short-term surveys of the snake fauna in areas with shrubby vegetation and stony soil is not recommended. Keywords: Caatinga, comparison, pitfall traps, Squamata, techniques.

(22) 20. INTRODUCTION The choice of sampling methods of biodiversity should be the most cost-effective as possible in attending to the requirements of the research. In this perspective, several factors must be considered: the surveyed taxon, research objectives, environment studied, time available for the development of the field work, and availability of financial resources (Aurichio and Salomão 2002, Silveira et al. 2010, Spence-Bailey et al. 2010). Sampling methods for herpetofauna can be applied in the presence or absence of the researcher in the field (Heyer et al. 1994, Franco et al. 2002, Willson and Dorcas 2004, Silveira et al. 2010). The most used methods to capture snakes that require the presence of researchers in the field are: time-constrained search (TCS), transects and occasional encounters by the research staff (OE) (Franco et al. 2002). The OE method is often criticized because it is hard to standardize, as it is not subject to strict planning. Nevertheless, this sampling technique has been useful and has been used by a large number of researchers in different neotropical biomes (see Martins and Oliveira 1998, Bernarde and Abe 2006, Zanella and Cechin 2006, Winck et al. 2007, Sawaya et al. 2008, Hartmann et al. 2009a, Hartmann et al. 2009b, Araujo et al. 2010). Among the methods that do not require the constant presence of the researcher in the field, the most used methods are traps and occasional encounters by thirds (OET). Among the traps, the pitfall traps (PIT) are the most used in neotropical environments, while other techniques, such as “funnel traps”, “glue traps”, and artificial shelters are still rarely used possibly because of limited funding (Cechin and Martins 2000, Auricchio and Salomão 2002, Sawaya et al. 2008, Silveira et al. 2010). The literature on the methods of sampling snakes indicates a different efficiency for each method in different environments, and treats the snake fauna included in the studies of.

(23) 21. herpetofauna in general (Cechin and Martins 2000, Ribeiro-Júnior et al. 2008). Not specifying the methods for the group often leads to the snakes being subsampled (Greenberg et al. 1994, Parris 1999, Gardner et al. 2007, Garden et al. 2007, Ribeiro-Júnior et al. 2011). Unlike studies on many animal groups, including herpetology, where specific methods for the studied groups are developed, the methods for sampling snakes usually follow traditional methods for collecting general herpetofauna, rather than targeting the group itself (e.g. Vogt and Hine 1982, Jacobson 1984, Stubbs et al. 1984, Coyne 1994, Gascon 1994, Jones and Hayes-Odum 1994, McDiarmid and Altig 1999, Auricchio and Salomão 2002, Franco et al. 2002, Freilich et al. 2005, Willson and Dorcas 2004), despite the knowledge of the wide variety of shapes and habits that snakes may have (Cadle and Greene 1993). Studies that focus on snakes often rely on multiple methods to sample snakes in order to capture the highest number of individuals and thus obtaining a good representation of the assemblage richness (e.g. Bernarde and Abe 2006, Sawaya et al. 2008). The major problem of the simultaneous use of several methods is the difficulty in standardizing the samples of each method, making it difficult to compare the efficiency between these and adding sampling biases to the final results on the research (Silva 2010). Shine and Bonnet (2000) indicate that snakes are good model organisms for many ecological questions due to the natural history plasticity of the group and the authors showed that there is a growing trend in using snakes to test ecological theories. Nevertheless, the majority of studies on tropical snakes address species inventories and characteristics of the natural history of some species, rarely seeking the understanding of patterns and processes at the community level (but see Vitt and Vangilder 1983, Luiselli et al. 1998, Brown and Shine 2002, Luiselli 2006, Akani et al. 2007, Brooks et al. 2009). This is an issue that deserves more attention because it is known that most species of snakes and the richest assemblages occur in tropical environments (Vitt 1987, Greene 1997, Martins and Oliveira 1998)..

(24) 22. Herein we present a comparison between four of the most commonly used methods to sample snakes (TCS, OET, OE and PIT) in relation to the main limiting factors: capture rate over time; financial cost for each snake collected and environment while discussing the relationship and applicability in studies of species inventories and community ecology. MATERIAL AND METHODS Study area The study area was the experimental farm Vale do Curu (main entrance: 03º49’06.1’’S / 39º20’14.8’’W, GPS Datum: WGS 84) in Pentecoste Municipality, State of Ceará, Northeast Brazil. It is a semiarid region with an annual mean temperature of 26.8ºC, 73% relative humidity, and 723.3 mm of rainfall with a remarkable seasonality in the rainfall regime with a wet period from February to July and a dry period for the rest of the year (Barros et al. 2002, Leão et al. 2004). Between January 2008 and June 2010, we made monthly visits to the study area, in which each visit lasted approximately 90 hours. During the first six months we performed a pilot study to delineate the sampling methods and to train a local worker. We considered each method as follows: time-constrained search (TCS), occasional encounters by the staff (OE), occasional encounters by third (OET) and pitfall traps with drift-fences (PIT). TCS - consisted of the search for snakes on foot or by car (maximum speed of 25 km/h) carried out by three people at a slow pace in trails and roads within the area and surroundings. Each month we carried out a total of 24 hours of TCS, with 22 hours of TCS by foot and two hours by car. For logistical issues, we carried out 16 hours of diurnal TCS and eight hours of nocturnal TCS each month. For this method the initial investment was approximately $170.00.

(25) 23. (USD) (flashlight + hook for handling snakes + sampling bags + batteries). We did not include the expenses for the car fuel because the search by car occurred exclusively during the traveling from and to the original city in a vicinal road and a road within the study area. OE – consisted of the encounter of snakes during the field campaign when TCS was not being applied. We estimate the time that the staff was subject to OE in 46 hours per month (90 hours total, less 24 hours of TCS = 66 hours; less 20 hours of estimated period of inactivity of the researchers). There was no specific cost for the application of this method. PIT – consisted of three sets of traps installed in three different vegetation types (arboreal Caatinga, shrub Caatinga and river floodplain). Each set of traps was composed of 20 plastic containers (50 liters) buried in the soil in radial conformation interconnected by five meter long and 60 cm high drift fences (Mengak and Guynn-Jr 1987). A total of 60 containers were installed. Within each bucket, we placed litter and a sheet of Styrofoam to serve as shelter against the weather conditions for the captured animals. We chose not to follow the suggestion of Cechin and Martins (2000), of a linear conformation of the traps and 100 L buckets, because the stony soil and the shrubby vegetation make this alternative unfeasible. Each container was kept open for 60 hours. Considering the three sets of traps (60 buckets), we totalized 3,600 hours of PIT per month. The traps were checked every 20 hours during the field campaigns. For this method, the initial investment was approximately $1,260.00 (USD) (buckets + driftfences (including replacements) + payment for local workers that helped digging the soil for the installation of the traps). We did not include the costs of durable equipment that was easily obtained in rural areas such as shovels, crowbars, and pickaxes because most of them were provided by the local workers..

(26) 24. OET – to fit the legal requirements and to standardize the effort of OET, a single local worker was trained during the first six months of the pilot study for the techniques of handling and capturing snakes (training time was over 72 hours) and we requested him to capture only the snakes he encountered occasionally during his daily activities. The native collector was not paid to avoid the active sampling of animals. As snake encounters by this method are merely incidental, we considered the effort of OET as 540 monthly hours (720 h reduced by 180 h of the estimated inactivity of the collector). The cost of OET was nearly $20.00 (USD) (a handcrafted hook + plastic containers to store the snakes). Expenses with accommodation and transport for the study area were not included because these costs are not inherent to any particular method. Analysis – we compared the observed and estimated species richness (Sobs and Sest, respectively) using the first order Jackniffe estimator for each method using the software EstimateS 8.0 (Colwell 2005). For a better visual comparison, we built sample-based rarefaction curves for the richness estimated for each method and for all the methods together (Gotelli and Colwell 2001). We measured the snout-vent length (SVL) of captured snakes and compared by each method through the analysis of variance (ANOVA) and post hoc Tukey’s pairwise test to verify the differences in the size classes of the snakes captured. All analyses were performed with an alpha set at 0.05. The capture rate of the snakes was evaluated as a function of the monetary investment (in USD invested/snake captured) and the time spent (in hours of effort/snake captured). We also observed the presence or absence of untargeted species captured by each method. In order to access the suitability of using the combination of these methods in ecological studies, we compared the structures of the assemblage (composition, richness, and abundance).

(27) 25. indicated by each method by building diagrams of the distribution of abundances for each method and by a cluster analysis UPGMA (Unweighted Pair Group method with Mean Arithmetic) using Euclidean distances as a measure of similarity between the structures resulted from each method. RESULTS Number of individuals and species richness – After 24 months of samplings, we recorded 620 snakes through the four evaluated methods. TCS responded for 55.8% (n=346) of the captures, followed by OET with 37.1% (n=230), PIT (n=23), and OE (n=21) that contributed less than 4% each (Table 1). All methods together captured 22 species of snakes. OET was the method that captured the highest number of species (n=20), followed by TCS (n=19), OE (n=10) and PIT (n=7). The first order Jackniffe estimator of richness predicted an assemblage composed of 22 (Sobs) to 26 species (Sest = 25.83) based on all the methods together. The same estimator predicts a richness of 23 species for OET (estimated value = 22.88), 22 species for TCS (estimated value = 21.88), 18 species for OE (estimated value = 17.67) and 11 species for PIT (estimated value = 10.83). Observing the rarefaction curves, the methods of OE and PIT were far from reaching the plateau, in spite of the relatively high effort (especially for PIT). TCS and OET showed similar patterns in their curves, after a fast growth in the early samples both maintained a slow and steady growth until the end of the study, while OE and PIT showed a slow and continuous growth since the first samples (Figure 1).. (Figure 1 may be included here.).

(28) 26. Differences in the sizes of snakes captured – TCS captured snakes between 98 and 1210 mm SVL (mean = 623.22 ± SD 243.27), OET captured snakes between 125 and 2300 mm (mean = 575.40 ± SD 313.90), OE between 169 and 1250 mm (mean = 531.05 ± SD 267.14) and PIT captured individuals between 186 and 580 mm (mean = 322.35 ± SD 83.41). The results from the ANOVA (F=8.19; p=0.0001) and the Tukey’s pair-wise comparison indicated that only snakes captured by PIT presented the shorter amplitude of sizes and were significantly smaller than those captured by TCS (q=6.76; p<0.01) and OET (q=5.60; p<0.01) (Figure 2).. (Figure 2 may be included here) Financial costs – One snake was captured for every $ 0.49 USD invested in TCS, $ 0.09 USD in OET, no specific cost was estimated for OE, and one snake for every $ 54.78 USD invested in PIT. Time costs – TCS was the method with the highest rate of capture at nearly 0.6 snakes per hour, or approximately one snake every 1 hour and 40 minutes of effort. The methods of OET and OE showed similar encounter rates of 0.018 snake/hour (OET) and 0.019 snake/hour (OE), or approximately one snake every 55 hours and 30 minutes of effort in OET and one snake every 52 hours and 40 minutes in OE. PIT presented the lowest capture rate with 0.0053 snakes/hour (considering one set of traps, i.e. 20 buckets) or one snake every 187 hours and 40 minutes. If we consider the three sets of traps, the success rate falls to 0.0018 snakes/hour and considering each bucket individually the capture rate is 0.00026 snakes/hour, or one snake for every 3,756 hours and 30 minutes of effort in PIT. Assemblage structure – Three species were registered exclusively by OET (Apostolepis cearensis (n=2), Liophis mossoroensis (n=1) and Mastigodryas bifossatus (n=1)), two only by.

(29) 27. TCS (Crotalus durissus (n=1) and Thamnodynastes cf. strigilis (n=1)) and no exclusive species were captured by OE or PIT (Figure 3). The diagrams of distribution of abundances represent the importance of each component of the assemblage indicated by each method; we observed that PIT is the only method with a strong trend toward a single species (Figure 3). Regarding the assemblage structure (species composition, richness, and abundance) that is indicated by each method, the UPGMA formed a group including TCS, OET, and OE, whereas PIT did not cluster (Figure 4).. (Figures 3 and 4 may be included here) DISCUSSION TCS and OET were the most efficient methods in terms of representation of the richness of the area because the rarefaction curves for those methods were within the range of 95% of the sample-based rarefaction curves of all methods together. Although the rarefaction curves of TCS and OET nearly reached the plateau at the end of the samplings, we observed that the sample-based curves did not reach a steady plateau for any of the methods, which is expected because it is virtually impossible to sample all the species from any biological community (Gotelli and Colwell 2001). TCS was the method with the highest rate of captures, and it resulted in a good representation of the richness because the estimated richness for this method was the same as the total number of species known for the area, observed including all the methods. Overall, the financial costs of TCS are low, but the results depend on the experience of the researchers involved in the work (Silveira et al. 2010, Ribeiro-Júnior et al. 2008, Garden et al. 2007). TCS has the disadvantage of being very physically demanding and requires prior training and good.

(30) 28. fitness of the field staff. It has the advantage of being the most efficient method in relation to the capture rate of snakes over time, and presents a relatively low maintenance cost (basically the replacement of batteries) and a reasonable rate of catch per monetary unit invested ($ 0.49 USD per snake). Another advantage of TCS is that there is no mortality or capture of untargeted species. In addition to that, because it is a method specifically directed to the capture of snakes, it allows field observations of the activity and behavior of the snakes, providing valuable information on ecology and natural history of many species. Our TCS results support the option made by Brown and Shine (2002) that used TCS exclusively in their study on ecological patterns in a tropical snake assemblage. OET was a good representative of the snake assemblage in the area; the estimated richness by this method was only one species higher than what is known to the area. Although there is a slow addition of individuals per hour, this addition is constant throughout the study period, which increases the probability of success of the method. The three species captured exclusively by this method clearly show the importance of OET in studies with snakes in semi-arid environments. OET has a disadvantage because it may be biased by the day to day work areas and schedule of the local collector, for example if the collector works in crops with seasonal harvest and, therefore, information about the seasonal activity of the captured snakes should be discarded because of the periods that the collector stays longer in field. Sometimes it is argued that one cannot rely on the information given by locals, but this problem can be mitigated by decreasing the number of collectors and training them appropriately, thus valuing the quality of the information rather than a greater amount (Dorcas and Willson 2009). Another disadvantage of this method is the time required for training the collectors. OET is a method recognized as controversial and rarely the authority responsible for environmental permits authorizes its use, because it allegedly encourages the killing of.

(31) 29. snakes (Akani et al. 2007). During our study, no snakes were killed by the trained collector, although he did occasionally collect some animals that were roadkill or killed by other locals. OET is advantageous because it requires almost no maintenance and - at least initially - local people from the study area tend to see more animals than recently arrived researchers and it also enables the researcher to collect information throughout the study period, even without the presence of researchers in the field (FitzGibbon and Jones 2006, Franco et al. 2002). Those are important reasons for the participation of local helpers in field research that requires snake sampling, as long as they are not paid and receive previous training in all aspects of this method (e.g. human and animal safety). OE was not efficient regarding the number of individuals in this study because of the relatively short time of possible encounters by OE. The method presents a slow rate of addition of new species, but the capture rate in hours of application is very similar to that of OET. Zanella and Cechin (2006) intuitively named this method as “Occasional Encounters by Thirds”, which is consistent with our results. Because, similarly to OE, every snake encounter by OET are merely incidental and should obviously have the same probability of occurrence in the absence of observer bias. Another advantage of OE is that there are no specific financial costs involved. PIT was the least efficient method in all aspects evaluated in this study. It is the least representative of the observed richness, did not capture any exclusive species, has the lowest capture rate, and the highest financial investment by snake captured (more than 100 times higher than TCS). Gibbons and Semlitsch (1982) suggest that PIT presents problems due to the variable efficiency in sampling different species. We found that, from 23 PIT-trapped individuals, 60.86% (n=14) belonged to a single small-sized species (Liophis viridis) and it was the only method with a significant difference in the size class of the sampled snakes,.

(32) 30. tending to catch smaller snakes and in a smaller size range. There is evidence that the size of the containers influences the capture rate and size of the snakes caught, so the constraint observed in our studies may be due to the size of the buckets we used (Cechin and Martins 2000, Todd et al. 2007). However, with the impossibility of using larger containers in stony soils as those of many areas of the Brazilian Caatinga, this method is not advantageous in this type of environment. Considering the financial expenses of PIT, it is recommended in studies where it is expected that a large number of terrestrial, fossorial, and cryptozoic snakes, in long-term studies and at sites that are relatively plain and with sandy soils (Enge 2001, Rueda-Almonacid et al. 2006). Among the methods evaluated, PIT is also the method that requires the greatest time and financial investment in maintenance due to damage to the drift-fences caused by intense solar radiation, low humidity, and animal or human action. Furthermore, the installation period is physically demanding because of the stony ground and high temperatures, requiring a large number of field-assistants (in our study, ten assistants) resulting in higher financial expenses. Ribeiro-Júnior et al. (2008) suggest that PIT is a cost-effective method for sampling lizards, amphibians, and small mammals. In this study, we demonstrate that the same cannot be said about snakes in the semi-arid regions in Brazil. This is consistent with the results in other areas that also captured a low number of snakes, even using larger containers than those used in our study (Ribeiro-Júnior et al. 2011). As found by Garden et al. (2007) and Enge (2001), the number of untargeted groups, such as invertebrates, frogs, lizards, and small mammals, captured by PIT is high, which makes the method advantageous for general faunistic inventories, but not to studies that target snakes specifically. Moreover, it was the only method where the mortality of the untargeted species was observed even though the mortality rate has not been quantified..

(33) 31. It is difficult to compare the eficiency of PIT in different biomes, because, each study use slightly different delineation to apply this method. Nevertheless the capture rate of snakes per container per month was much lower than the rates for other regions of Brazil even considering studies that used smaller containers (Cechin and Martins 2000). Although pragmatically, this relationship is not the most appropriate, because containers connected by drift-fences should not be considered as independent units, but we chose to discuss this in order to be able to compare the available information. The most obvious advantages of PIT is that, after installation and proper maintenance, the sampling is passive and does not require a constant presence in the field for long periods, it is not biased by the researcher experience, and it allows some extent of quantification of prey availability. Our results are consistent with Silveira et al. (2010), Garden et al. (2007), and Enge (2001) that PIT sample small and medium-sized animals or juveniles of larger animals, with terrestrial or fossorial habits. While active methods are usually more general, and record a wide variety of species. Campbell and Christman (1982) suggest that PIT capture animals rarely found by visual encounters, which was not corroborated for snakes in this semi-arid area, but it has been demonstrated for other tropical biomes (e.g. Zanella and Cechin 2006, Sawaya et al. 2008). We showed that TCS, OET, and OE are grouped and could be compared regarding the structure of the assemblage while the results obtained by PIT are inappropriate for comparisons in studies that are based on abundances or assemblage structure at least in semiarid regions. PIT resulted in a very different assemblage structure compared to the other methods due to the strong tendency to capture only a small group of species, being unable to capture even some of the most abundant species..

(34) 32. The study area should also be considered for the methods to be cost-effective. Our results indicate that in semi-arid areas with stony soil, the most cost-effective set of sampling methods tested is of TCS, OET, and OE. We suggest the non-application of PIT under the given conditions, and research of tropical areas should also consider other sampling methods not tested here, such as box and funnel traps that have been successfully used in many extratropical environments (Kjoss and Litvaitis 2001). The choice of methods should be made carefully in relation to the study objectives and methods should be adapted to the reality of each location (Silveira et al. 2010). When the objective is to identify the species richness in a particular area or to investigate aspects of natural history and the autoecology of certain species of snakes it is accepted and recommended to use as many methods as possible, because some methods may capture species that are difficult to be registered by other methods and it may increase the number of individuals sampled from the target group. In these cases, the use of multiple methods can be considered as complementary (Magurran 2004, Prudente et al. 2010, Silva 2010). However, if the objective of the study is related to patterns of population dynamics, abundance, or assemblage structure we suggest great care in selecting the sampling methods. Because in these cases, some methods cannot be regarded as complementary, because they may add overlapping information that may distort rather than reveal natural patterns. This approach was already considered in research on more easily sampled taxa. In those studies the sampling delineation is directed to obtain very consistent data, even reducing (and often excluding) the number of records of some species that could be captured by some different methods (see Heyer et al. 1994, Huang and Hou 2004, Gardner et al. 2007(b), Dixo and Martins 2008, Siqueira et al. 2009). In conclusion, although it is one of the most efficient methods to sample other groups of herpetofauna, and thus extremely useful in faunistic inventories, PIT was ineffective in.

(35) 33. catching snakes in the Brazilian semiarid region. Considering the difficult to sample snakes in the field (Reinert 1993), the limited time and funding, we suggest that the time and funds usually invested in PIT should be invested in other methods that are more cost-effective and are truly complementary, especially in shrubby environments with stony soils. Furthermore, we suggest that when there is the simultaneous use of different methods, the sampling effort should be standardized (in hours of effort, for example) to allow comparisons between different methods and studies (Ribeiro-Júnior et al. 2011). We agree with Silveira et al. (2010) that the methods should be used, focusing neither on convenience nor tradition, but rather fundamentally to obtain quality data that provide results that fulfill the objectives of the study (Measey 2006, Garden et al. 2007, Ribeiro-Junior et al. 2008, Dorcas and Willson 2009, Spence-Bailey et al. 2010).. (Table 1 may be included here).

(36) 34. LEGENDS TO THE FIGURES Figure 1. Sample-based rarefaction curves for all sampling methods. Confidence interval is shown only for all methods together. TCS – Time-constrained survey, OET – Occasional encounters by thirds, PIT – Pitfall traps, OES – Occasional encounters by the field staff. Figure 2. Non-outlier relation between size and sampling method for snakes in the study area. Time constrained search (TCS), Occasional encounters by thirds (OET), Occasional encounter (OE) and Pitfalls (PIT). Figure 3. Diagrams of distributions of abundances of the species registered by each method. Ace (Apostolepis cearensis), Bco (Boa constrictor), Bse (Boiruna sertaneja), Cdu (Crotalus durissus) Eas (Epicrates assisi), Lah (Leptophis ahaetulla), Lan (Leptodeira annulata), Ldi (Liophis dilepis), Lmo (Liophis mossoroensis), Lpo (Liophis poecilogyrus), Lvi (Liophis viridis), Mbi (Mastigodryas bifossatus), Mib (Micrurus ibiboboca), Oan (Oxybelis aeneus), Otr (Oxyrhopus trigeminus), Pjo (Psomophis joberti), Pna (Philodryas nattereri), Pni (Pseudoboa nigra), Pol (Philodryas olfersii), Tme (Tantilla melanocephala), Tst (Thamnodynastes cf. strigilis), Xme (Xenodon merremii). Figure 4. UPGMA dendrogram representing the similarities among the assemblage structure obtained by each sampling methods (r = 0.99). Table 1. Number of individuals of the species captured by each method at Pentecoste municipality, Northeast Brazil..

(37) 35. ACKNOWLEDGMENTS We would like to thank Dr. Teresa Cristina Sauer Ávila-Pires, Dr. Noeli Zanella, Dr. Maria da Graça Salomão, and Dr. Everton Behr for their valuable suggestions on the first versions of the manuscript. Dr. Diva Maria Borges-Nojosa and the staff of the Núcleo Regional de Ofiologia/Universidade Federal do Ceará for material and logistic support. ICMbio for the license code: SISBIO/18596-1. CAPES for the financial support, and SZC thanks CNPq for the research funding (protocol 303359/2009-9)..

(38) 36. RESUMO A escolha de métodos de amostragem é um passo crucial em todas as pesquisas de campo em herpetologia. Em países onde há frequentemente limitações de tempo e apoio financeiro a escolha dos métodos é ainda mais crítica. Os métodos utilizados para amostrar as serpentes muitas vezes carecem de critérios objetivos e aparentemente a tradição tem sido mais importante para a escolha. Essa é a razão pela qual pesquisas usando métodos não padronizados são frequentemente encontradas na literatura. Neste estudo fazemos uma comparação entre quatro métodos comumente utilizados para a amostragem taxocenoses de serpentes em uma área semiárida no Brasil. Comparamos a eficácia de cada método baseado no custo benefício em relação ao número de indivíduos e espécies registradas, investimento de tempo e financeiro. Constatamos que armadilhas de “pitfall” foi o método com pior custobenefício em todos os aspectos avaliados além de não ter sido complementar aos outros métodos, em relação à abundância das espécies e estrutura da assembleia. Concluímos que os métodos podem ser considerados complementares apenas se padronizados para os objetivos do estudo. O uso de armadilhas de queda em levantamentos da fauna de serpentes não é recomendado em áreas arbustivas e de solo pedregoso. Palavras-chave: Caatinga, comparação, armadilhas pitfall, procura visual, técnicas..

(39) 37. REFERENCES. AKANI GC, EBERE N, LUISELLI L AND ENIANG EA. 2007. Community structure and ecology of snakes in fields of oil palm trees (Elaeis guineensis) in the Niger Delta, southern Nigeria. Afr J Ecol 46: 500-506. AURICHIO P AND SALOMÃO MG. 2002. Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos. São Paulo: Instituto Pau Brasil de História Natural. 348 p. ARAUJO CO, CORRÊA-FILHO DT AND SAWAYA R J. 2010. Snake assemblage of Estação Ecológica de Santa Bárbara, SP: A Cerrado remnant in southeastern Brazil. Biota Neotrop 10(2): 235-245. BARROS VS, COSTA RNT AND AGUIAR JV. 2002. Função de produção da cultura do melão para níveis de água e adubação nitrogenada no Vale do Curu - CE. Irriga 7(2): 98-105. BERNARDE PS AND ABE AS. 2006. A snake community at Espigão Oeste, Rondônia, Southwestern Amazon, Brazil. South Am J Herpetol 1(2): 102-113. BROOKS SE, ALLISON EH, GILL, JA AND REYNOLDS JD. 2009. Reproductive and trophic ecology of an assemblage of aquatic and semi-aquatic snakes in Tonle Sap, Cambodia. Copeia 2009(1): 7-20. BROWN GP AND SHINE R. 2002. Influence of weather conditions on activity of tropical snakes. Austral Ecol 27: 596-605. CADLE JE AND GREENE HW. 1993. Phylogenetic patterns, biogeography, and the ecological structure of Neotropical snake assemblages. In: RICKLEFS RE AND SCHLUTER D (Eds), Species diversity in ecological communities: historical and geographical perspectives, Chicago: University of Chicago Press, pp. 281-293..

(40) 38. CAMPBELL HW AND CHRISTMAN SP. 1982. Field techniques for herpetofaunal community analysis. In: Scott Jr NJ (Ed), Herpetological Communities. Washington: Society for the Study of Amphibians and Reptiles and Herpetologists’ League. pp. 193-200. CECHIN SZ AND MARTINS M. 2000. Eficiência de armadilhas de queda (pitfall traps) em amostragem de répteis e anfíbios no Brasil. Rev Bras Zool 17(3): 729-740. COLWELL RK. 2005. EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5. User’s Guide and application (http://purl.oclc.org/estimates). COYNE MS. 1994. Feeding ecology of subadult green sea turtles in south Texas waters. Thesis, Master of Science, Texas A&M University. 86p. DIXO M AND MARTINS M. 2008. Are leaf-litter frogs and lizards affected by edge effects due to forest fragmentation in Brazilian Atlantic forest? J Trop Ecol 24: 551-554. DORCAS M AND WILLSON JD. 2009. Innovative methods for studies of snake ecology and conservation. In: Mullin SJ and Seigel RA (Eds), Snakes: Ecology and Conservation Ithaca, Cornell University Press, pp. 5-37. ENGE KM. 2001. The pitfalls of pitfall traps. J Herpetol 35(3): 467-478. FITZGIBBON S AND JONES D. 2006. A community-based wildlife survey: the knowledge and attitudes of residents of suburban Brisbane, with a focus on bandicoots. Wildlife Res 33: 233241. FRANCO FL, SALOMÃO MG AND AURICHIO P. 2002. Répteis. In: Aurichio P and Salomão MG (Eds), Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos. São Paulo: Instituto Pau Brasil de História Natural. pp. 75-125. FREILICH JE, CAMP RJ, DUDA JJ AND KARL AE. 2005. Problems with Sampling Desert Tortoises: A Simulation Analysis Based on Field Data. J Wildlife Manage 69(1): 45-56..

(41) 39. GARDEN JG, MCALPINE CA, POSSINGHAM HP AND JONES DN. 2007. Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and costefficient combinations? Wildlife Res 34: 218–227. GARDNER TA, BARLOW J AND PERES CA. 2007. Paradox, presumption and pitfalls in conservation biology: The importance of habitat change for amphibians and reptiles. Biol Conserv 138: 166-179. GARDNER TA, FITZHERBERT EB, DREWERS RC, HOWELL KM AND CARO T. 2007. Spatial and temporal patterns of abundance and diversity of an East African leaf litter amphibian fauna. Biotropica 39(1): 105-113. GASCON C. 1994. Bottom-nets as a new method for quantitatively sampling tadpole populations (Amphibia, Anura). Rev Bras Zool 11(2): 355-359. GIBBONS JW AND SEMLITSCH RD. 1982. Terrestrial drift fences with pitfall traps: an effective technique for quantitative sampling of animal populations. Brimleyana 1982: 1-16. GOTELLI NJ AND COLWELL RK. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4: 379-391. GREENBERG CH, NEARY DG AND HARRIS LD. 1994. A comparison of herpetofaunal sampling effectiveness of pitfall, single-ended, and double-ended funnel traps used with drift fences. J Herpetol 28(3): 319-324. GREENE HW. 1997. Snakes: the evolution of mystery in nature. Berkeley: University of California Press. 351 p. HARTMANN PA, HARTMANN MT AND MARTINS, M. 2009a. Ecology of a snake assemblage in the Atlantic forest of southeastern Brazil. Pap Avulsos Zool 49(27): 343-360. HARTMANN PA, HARTMANN MT AND MARTINS M. 2009b. Ecologia e história natural de serpentes no Núcleo Santa Virgínia do Parque Estadual da Serra do Mar, no sudeste do Brasil. Biota Neotrop 9(3): 173-184..

(42) 40. HEYER WR, DONNELLY MA, MCDIARMID RW, HAYEK LC AND FOSTER MS. 1994. Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Washington: Smithsonian Institution Press. 384p. HUANG C AND HOU PL. 2004. Density and diversity of litter amphibians in a monsoon forest of Southern Taiwan. Zool Stud 43(4): 795-802. JACOBSON ER. 1984. Immobilization, Blood Sampling, Necropsy Techniques and Diseases of Crocodilians: A Review. J Zoo Anim Med 15(1): 38-45. JONES D AND HAYES-ODUM L. 1994. A method for the restraint and transport of crocodilians. Herpetol Rev 25: 14-15. KJOSS VA AND LITVAITIS JA. 2001. Comparison of 2 methods to sample snake communities in earlu successional habitats. Wildlife Soc B 29(1): 153-157. LEÃO RAO, TEIXEIRA AS, ANDRADE EM AND OLIVEIRA F. 2004. Automatic delimitation and characterization of a catchment located at the Fazenda Experimental do Vale do Curu in Pentecoste County – Brazil. Rev Ciênc Agron 35(1): 26-35. LUISELLI L. 2006. Resource partitioning and interspecific competition in snakes: the search for general geographical and guild patterns. Oikos 114: 193-211. LUISELLI L, AKANI GC AND CAPIZZI D. 1998. Food resource partitioning of a community of snakes in a swamp rainforest of south-eastern Nigeria. J Zool 246: 125-133. MAGURRAN AE. 2004. Measuring Biologial Diversity. Oxford: Blackwell Science. 264p. MARTINS M AND OLIVEIRA ME. 1998. Natural history of snakes in forests of Manaus region, Central Amazonia, Brazil. Herpetol Nat Hist 6(2): 78-150. MCDIARMID RW AND ALTIG R. 1999. Tadpoles: The Biology of anuran larvae. Chicago: University of Chicago Press. 458p. MEASEY GJ. 2006. Surveying biodiversity of soil herpetofauna: towards a standard quantitative methodology. Eur J Soil Biol 42(2006): 103-110..

(43) 41. MENGAK MT AND GUYNN-JR DC. 1987. Pitfalls and snap traps for sampling small mammals and herpetofauna. Am Mid Nat 118(2): 284-288. PARRIS KM. 1999. Review: amphibian surveys in forests and woodlands. Contemp Herpetol. 1999: 1-14. PRUDENTE ALC, MASCHIO GF, SANTOS-COSTA MC, FEITOSA DT. 2010. Serpentes da bacia petrolífera de Urucu, Município de Coari, Amazonas, Brasil. Acta Amazo 40(2): 381-386. REINERT HK. 1993. Habitat selection in snakes. In: Seigel RA and Collins JT (Eds), Snakes: Ecology and Behavior. New York: McGraw-Hill. pp. 201-240. RIBEIRO-JÚNIOR MA, GARDNER TA AND ÁVILA-PIRES TCS. 2008. Evaluating the Effectiveness of Herpetofaunal Sampling Techniques across a Gradient of Habitat Change in a Tropical Forest Landscape. J Herpetol 42(4): 733-749. RIBEIRO-JÚNIOR MA, ROSSI RV, MIRANDA CL AND ÁVILA-PIRES TCS. 2011. Influence of pitfall trap size and design on herpetofauna and small mammal studies in Neotropical Forest. Zoologia 28(1): 80-91. RUEDA-ALMONACID JV, CASTRO F AND CORTEZ C. 2006. Técnicas para el inventario y muestreo de anfibios: Una compilación. In: ANGULO A. ET AL. (Eds.), Técnicas de Inventario y Monitoreo para los Anfibios de la Región Tropical Andina. Bogotá: Conservación Internacional. pp. 135–71. SAWAYA RJ, MARQUES OAV AND MARTINS M. 2008. Composição e história natural das serpentes de Cerrado de Itirapina, São Paulo, sudeste do Brasil. Biota Neotrop 8(2): 127-148. SHINE R AND BONNET X. 2000. Snakes: a new ‘model organism’ in ecological research? Trends Ecol Evol 15: 221-222. SILVA FR. 2010. Evaluation of survey methods for sampling anuran species richness in the Neotropics. S Am J Herpetol 5(3): 212-220..

(44) 42. SILVEIRA LF, BEISIEGEL BM, CURCIO FF, VALDUJO PH, DIXO M, VERDADE VK, MATTOX GMT AND CUNNINGHAM PTM. 2010. Para que servem os inventários de fauna? Estud Av 24(68): 173-207. SIQUEIRA CC, VRCIBRADIC D, ALMEIDA-GOMES M, BORGES-JUNIOR VNT, ALMEIDA-SANTOS P, ALMEIDA-SANTOS M, ARIANI CV, GUEDES DM, GOYANNES-ARAÚJO P, DORIGO TA, VAN SLUYS M AND ROCHA CFD. 2009. Density and richness of leaf litter frogs (Amphibia: Anura) of an Atlantic Rainforest area in the Serra dos Orgãos, Rio de Janeiro State, Brazil. Zoologia 26: 97-102. SPENCE-BAILEY LM, NIMMO DG, KELLY LT, BENNETT AF AND CLARKE MF. 2010. Maximising trapping efficiency in reptile surveys: the role of seasonality, weather conditions and moon phase on capture success. Wildlife Res 37: 104–115. STUBBS D, HAILEY A, PULFORD E AND TYLER W. 1984. Population Ecology of European Tortoises: Review of Field Techniques. Amphibia-Reptilia 5(1): 57-68. TODD BD, WINNE CT, WILLSON JD AND GIBBONS JW. 2007. Getting the Drift: Examining the Effects of Timing, Trap Type and Taxon on Herpetofaunal Drift Fence Surveys. Am Mid Nat 158: 292-305. VITT LJ AND VANGILDER LD. 1983. Ecology of a snake community in Northeastern Brazil. Amphibia-Reptilia 4: 273-296. VITT LJ. 1987. Communities. In: SEIGEL JT ET AL. (Eds), Snakes: ecology and evolutionary biology. New York: McGraw-Hill. pp. 335-365. VOGT RC AND HINE RL. 1982. Evaluation of techniques for assessment of amphibian and reptile populations in Wisconsin. In: SCOTT JR NJ (Ed.), Herpetological Communities. Washington: Society for the Study of Amphibians and Reptiles and Herpetologists’ League. pp. 201-217..

(45) 43. WINCK GR, SANTOS TG AND CECHIN SZ 2007. Snake assemblage in a disturbed grassland environment in Rio Grande do Sul state, southern Brazil: population fluctuations of Liophis poecilogyrus and Pseudablabes agassizii. Ann Zool Fenn 44: 321-332. WILLSON JD AND DORCAS ME. 2004. A comparison of aquatic drift fence with traditional funnel trapping as a quantitative method for sampling amphibians. Herpetol Rev 35(2): 148150. ZANELLA N AND CECHIN SZ. 2006. Taxocenose de serpentes no planalto médio do Rio Grande do Sul, Brasil. Rev Bras Zool 23(1): 211-217..

(46) 44. Figure 1. Figure 2.

(47) 45. Figure 3.

(48) 46. Figure 4.

(49) 47. Table 1.

(50) 48.

(51) 49. CAPÍTULO 2 - Ecologia e história natural das serpentes de uma área de Caatinga no nordeste brasileiro (submetido ao periódico: Papéis Avulsos de Zoologia).

(52) 50. Ecologia e história natural das serpentes de uma área de Caatinga no nordeste brasileiro Titulo curto: “História natural de serpentes em uma área de Caatinga” Paulo C. M. D. Mesquita1,3, Daniel C. Passos2, Diva M. Borges-Nojosa2, Sonia Z. Cechin1 1. Laboratório de Herpetologia, Departamento de Biologia, Universidade Federal de Santa Maria. Avenida Roraima, 1000. CEP 97105-900, Santa Maria, RS, Brazil 2. Núcleo Regional de Ofiologia, Universidade Federal do Ceará. Campus do Pici, Bloco 905, CEP 60.455-760, Fortaleza, Ceará, Brasil 3. Autor para correspondência: paulocmdm@gmail.com.

(53) 51. ABSTRACT The snake fauna from the Brazilian Caatinga is poorly studied. We studied a snake assemblage from an area of Caatinga with shrub and tree vegetation type to describe the natural history of the snake species found. A total of 636 individuals of 22 species from four families were recorded.. The species abundances distribution is log-normal and the. composition presents species typical from the Caatinga with Oxybelis aeneus (Wagler, 1824) and Philodryas nattereri Steindachner, 1870 being the most common. The natural history of each species is described based on information on activity patterns, diet, habitat use, reproduction, and defensive repertoire obtained during the study and on information available in literature. The study area is located in a priority region for conservation and our results emphasize that conservation policies should be implemented in the region. KEYWORDS: Community; Assemblage; Diet; Behavior; Activity..

(54) 52. RESUMO A fauna de serpentes do bioma Caatinga é uma das menos estudadas do Brasil. Estudamos a assembléia de serpentes de uma área de Caatinga arbustivo-arbórea a fim de descrever a história natural das espécies ocorrentes na região. Um total de 636 indivíduos de 22 espécies de quatro famílias foi registrado. A distribuição das abundâncias das espécies na área é lognormal e a composição apresenta serpentes típicas de Caatinga sendo Oxybelis aeneus (Wagler, 1824) e Philodryas nattereri Steindachner, 1870, as espécies mais comuns. A história natural de cada espécie é descrita a partir das informações sobre padrões de atividade, dieta, uso do ambiente, reprodução e repertório defensivo, obtidas durante o estudo e de informações disponíveis na literatura. A área de estudo está em uma área prioritária para conservação e os resultados reforçam que políticas conservacionistas sejam aplicadas na região. PALAVRAS-CHAVE: Comunidade; Assembléia; Dieta; Comportamento; Atividade..