Jefter Barbosa Rodrigues 1, *, Samara Cíntia Alves Gama 2, Gentil Alves Pereira Filho 3, Frederico Gustavo Rodrigues França 4

(1)

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

Composition and Ecological Aspects of a Snake Assemblage on the Savanna

Enclave of the Atlantic Forest of the Guaribas Biological Reserve in

Northeastern Brazil

Author(s): Jefter Barbosa Rodrigues, Samara Cíntia Alves Gama, Gentil Alves Pereira Filho and

Frederico Gustavo Rodrigues França

Source: South American Journal of Herpetology, 10(3):1-8.

Published By: Brazilian Society of Herpetology

DOI: http://dx.doi.org/10.2994/SAJH-D-15-00016.1

URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-15-00016.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

(2)

Composition and Ecological Aspects of a Snake Assemblage

on the Savanna Enclave of the Atlantic Forest of the

Guaribas Biological Reserve in Northeastern Brazil

Jefter Barbosa Rodrigues1,_{*, Samara Cíntia Alves Gama}2_{, Gentil Alves Pereira Filho}3_, Frederico Gustavo Rodrigues França4

1_{Programa de Pós-Graduação em Ciências Biológicas, Zoologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba,}

Via Expressa Padre Zé, Cidade Universitária, s/n, Castelo Branco, CEP 58051-900, João Pessoa, Paraíba, Brazil.

2_{Programa de Pós-Graduação em Engenharia Ambiental, Centro de Tecnologia, Universidade Federal da Paraíba,}

Via Expressa Padre Zé, Cidade Universitária, s/n, Castelo Branco, CEP 58051-900, João Pessoa, Paraíba, Brazil.

3_{Museu de Zoologia da Universidade de São Paulo, Avenida Nazaré 481, CEP 04263-000, Ipiranga, São Paulo, São Paulo, Brazil.} 4_{Departamento de Engenharia e Meio Ambiente, Centro de Ciências Aplicadas e Educação, Universidade Federal da Paraíba,}

Rua da Mangueira, s/n, CEP 58297-000, Rio Tinto, Paraíba, Brazil. * Corresponding author. Email: rodrigues.herpeto@gmail.com

Abstract. We studied the composition, richness, abundance, and influence of abiotic factors on the seasonal activity of a snake assemblage

at a fragment of savanna enclave (tabuleiro forest) of the Atlantic Forest in northeastern Brazil. The sampling methods used were pitfall traps with drift fences, timed visual encounter survey, donations from local collectors, incidental encounters, and road sampling. We obtained a total of 164 individuals distributed across 29 snake species and six families over 2 years of study. The most frequently encountered species were the two blindsnakes Amerotyphlops paucisquamus and A. brongersmianus and the two false coral snakes Tantilla melanocephala and

Oxy-rhopus trigeminus. Monthly snake captures were significantly correlated only with the lowest temperatures. Our results show that the study

area has a rich diversity of snakes of similar composition to other Brazilian open areas with a dominance of fossorial and cryptozoic species.

Keywords. Abundance; Activity patterns; Ecology; Natural history; Reptile; Richness.

Resumo. Nós estudamos a composição, riqueza, abundância e a influência de fatores abióticos na atividade sazonal de uma taxocenose de

serpentes em um fragmento de enclave de cerrado (Floresta de tabuleiro) na Floresta Atlântica do nordeste do Brasil. Os métodos de amos-tragem foram armadilha de interceptação e queda com cercas-guia, procura visual cronometrada, coleta por terceiros, encontros ocasionais e procura de carro nas rodovias que margeiam a reserva. Durante dois anos de estudo, nós encontramos um total de 164 indivíduos distribuí-dos em 29 espécies de serpentes e seis famílias. As espécies mais frequentes foram Amerotyphlops paucisquamus, Amerotyphlops

brongersmia-nus, Tantilla melanocephala e Oxyrhopus trigeminus. A incidência mensal de captura das serpentes teve correlação significativa apenas com a

temperatura mínima. Os resultados indicam que a área de estudo comporta uma alta riqueza de serpentes e a composição é similar a outras áreas abertas do Brasil, com dominância de serpentes fossoriais e criptozóicas.

called Lowland Tabuleiro Forests (20–100 m elevation), and extend along the northeastern coast of Brazil (Thomas and Barbosa, 2008).

The herpetofauna is an important component of Brazilian biodiversity, playing a key role in the structure of ecological communities (Colli et al., 2002). The number of studies of snake assemblages in Brazil has increased in recent years, some of which have described the ecology of snake assemblages from Atlantic Forest of southern Brazil (Bérnils et al., 2001; Zanella and Cechin, 2006; Morato, 2005), southeastern Brazil (Sazima and Haddad, 1992; Marques and Sazima, 2004; Pontes et al., 2009; Costa et al., 2010), and northeastern Brazil (Argôlo, 2004; França et al., 2012). However, none of those studies were carried out specifically in the savanna enclaves of the Atlantic Forest. Herein, we present the results of a 2 year study on the snake assemblage of a tabuleiro patch in Guaribas Biological Reserve, one of the most important INTRODUCTION

The Atlantic Forest of Brazil is the second largest tropical rainforest of the Neotropics and one of the most biologically diverse regions in the world (Galindo-Leal and Câmara, 2003). However, the Atlantic Forest is also one of the most highly threatened, with only ca. 11% of its original cover remaining in different patch sizes and conservation levels (Tabarelli et al., 2005; Ribeiro et al., 2009).

The vegetation of the Atlantic Forest comprises principally tropical moist forests, but open physiognomies also appear along the coast (known as restingas) and in the interior (known as tabuleiros). These tabuleiros are natural savanna enclaves characterized by dense, tall, herbaceous vegetation with scattered trees (Oliveira-Filho and Carvalho, 1993). These open patches occur over faster-draining sand soils inside semidecidual forests,

South American Journal of Herpetology, 10(3), 2015, 1–8

Ralph A. Saporito

(3)

protected areas of the Atlantic Forest of northeastern Brazil. We focus on the composition, richness, abundance, and seasonal activity patterns of snake species to characterize the ecology of the assemblage.

MATERIALS AND METHODS Study area

The Guaribas Biological Reserve (06°44'25.93"S, 35°08'32.30"W) is located on the northern coast of Paraíba State in northeastern Brazil. The reserve is divided into three patches (called SEMAs I, II, and III) of 616 ha, 3,378 ha, and 327 ha, respectively. Two patches (SEMA I and II) are located in Mamanguape municipality and contain lowland tabuleiro forests with mainly savanna-like habitats called tabuleiros (Oliveira-Filho and Carvalho, 1993). The third patch (SEMA III) is adjacent to Rio Tinto and is characterized by forested habitat named Floresta Estacional Semidecidual (Radambrasil, 1981). In this work we focus on the snake diversity of a tabuleiro patch in SEMA II (Fig. 1).

The Guaribas Biological Reserve climate is type As’ in the Köppen classification, hot and humid, receiving annually 1,750–2,000 mm of seasonal precipitation between March and October and reaching its peak in June/July. Average temperatures range between 24°C in the rainy season during the autumn and winter and 26°C in the dry season of summer (Nimer, 1989).

Sampling methods

Snakes were collected between March 2010 and February 2012. When possible, for each snake found, we recorded date, time, substrate and if the snake was active. We follow the taxonomy presented by Grazziotin et al. (2012) and Bérnils and Costa (2014). For sampling we used pitfall traps with drift fences, timed visual encounter survey, road sampling, incidental encounters and donations from local collectors.

For pitfall traps, we established a linear set of 25 arrays (Fig. 1A), each consisting of a central 60 L plastic bucket sunk into the ground, three 5 m aluminum drift fences at angles of 120° from each other, and a 60 L bucket

Figure 1. Map of the study area showing (A) vegetation type and transects where pitfall traps were placed, (B) municipalities, (C) the country, and (D) the state of the study site.

Composition and Ecological Aspects of a Snake Assemblage on the Savanna Enclave of the Atlantic Forest of the Guaribas Biological Reserve in Northeastern Brazil

Jefter Barbosa Rodrigues, Samara Cíntia Alves Gama, Gentil Alves Pereira Filho, Frederico Gustavo Rodrigues França

2

(4)

at the end of each drift fence. Thus, each array had four bucket traps, totaling 100 traps. The arrays were evenly spaced along a 1,012.2 m transect. Traps were monitored once per week and remained active during the entire study, totaling 731 days and 17,544 hours of sampling. Although the traps were checked weekly, park rangers and other researchers working with lizards and mammals also checked the traps on other days of week, thus reducing animal mortality.

The timed visual encounter survey consisted of walking slowly in search of snakes in all visually accessible microhabitats (Sawaya et al., 2008). The surveys were conducted monthly between March 2010 and October 2011, except December 2010 and July 2011, in the same enclave of savanna type where the pitfall traps were placed (Fig. 1A). The total sampling effort was 174.10 h timed visual encounter survey, with 78.30 h during the day and 87.40 h at night. The same sampling effort was not applied to each month in timed visual encounter survey.

Road sampling was performed by sighting snakes by car, with speed of 40–50 km/h, on two paved roads, BR-101 and PB-071, surrounding the reserve. The circuit was 62 km long and was completed 63 times, with a frequency of two to three times per month, totaling 3,968 km of road sampling.

The local collectors method provided snakes that were captured by park rangers or other researches inside the reserve, as well as snakes captured during activities other than the intentional sampling methods (Sawaya et al., 2008).

Maximum and minimum ambient temperature, precipitation, and humidity data were collected during all months in the 2 year study from the nearest meteorological station, located approximately 18 km from study area, provided by Agência Executiva de Gestão das Águas do Estado da Paraíba (AESA).

Data analysis

We constructed a species accumulation curve for snakes in Guaribas Biological Reserve using the individual-based rarefaction method (with the nonparametric Mao Tau estimator) to evaluate the relationship between collection effort and species saturation in the assemblage (Gotelli and Colwell, 2001; Colwell et al., 2004). The function of richness (Mao Tau) was calculated as the accumulation function of species by the number of individuals collected. The species rarefaction curves were made without replacement using 1,000 randomizations. In addition, we used species richness estimators (with nonparametric incidence-based estimators: Bootstrap, Chao 2, ICE, Jacknife 1 and 2, and abundance-based data: ACE and Chao 1) to determine the expected richness of snakes in the area (Colwell and Coddington, 1994;

Colwell, 2009). The species rarefaction and richness estimates were performed with EstimateS 8.2.0 software (Colwell, 2009).

The correlation between the seasonal captures and abiotic factors was analyzed from the both monthly average of abiotic factors and incidence of monthly captured snakes, using Spearman’s rank correlation coefficient (rs; Zar, 1999; Winck et al., 2007). The test was

performed using R v.3.0.1 software (R Core Team, 2013) with a 5% of significance level.

RESULTS

We recorded 164 individuals of 29 species from six families (Boidae Gray, 1825; Colubridae Oppel, 1811; Dipsadidae Bonaparte, 1840; Elapidae Boie, 1827; Typhlopidae Merrem, 1820 and Viperidae Oppel, 1811) from the tabuleiro area of the Guaribas Biological Reserve. Dipsadidae was the richest family with 15 species, while Viperidae had only one species. The most common species were Amerotyphlops paucisquamus (Dixon and Hendricks, 1979), Amerotyphlops brongersmianus (Vanzolini, 1976),

Tantilla melanocephala (Linnaeus, 1758), and Oxyrhopus trigeminus Duméril, Bibron and Duméril, 1854 that

represent together more than 50% of all individuals recorded. However, for most species (17) we found less than three individuals during the study (Table 1). The individual-based rarefaction curve (Mao Tau) did not reach stability and the species richness estimators produced estimates greater than the observed richness (34.22–47.87).

Considering the capture methods (Table 1), we recorded 133 individuals of 16 species in pitfall traps. The traps captured 81% of all records. Nine species were caught exclusively in pitfall traps. During the road sampling we found 21 individuals (13% of all individuals) of 16 species. Nine species were recorded only during road sampling and the encounter rate was 1 snake/27.60 km. Local collectors contributed three individuals (16.28%) of three species, and Bothrops leucurus Wagler in Spix, 1824 was only recorded by this method. Four snakes were found during the timed visual encounter survey. The encounter rate was one snake per 28.18 h of search effort. Finally, three snakes were recorded by incidental encounters.

The snakes showed a diversity of habits and activity (Table 2). Three species were fossorial (10%), six cryptozoic (21%), eight strictly terrestrial (28%), eleven utilized both terrestrial and arboreal habits (38%), and only Imantodes cenchoa (Linnaeus, 1758) was strictly arboreal (3%). Ten species were strictly nocturnal (34%), 12 were strictly diurnal (41%) and seven were active during both periods (24%).

Capture incidence of snakes in the Guaribas Biological Reserve was higher from December–May

(5)

(summer–early autumn) with peaks in April 2010, December 2010, and March 2011 (Fig. 2). There was a positive correlation between the capture incidence and the monthly low ambient temperature (S = 880.7058,

P = 0.0171), but there was no significant correlation with

monthly maximum ambient temperature (S = 1458.14;

P = 0.4316), precipitation (S = 1071.842, P = 0.06902), or

relative humidity (S = 1516.486, P = 0.5234). DISCUSSION

The snake fauna from tabuleiros of Guaribas Biological Reserve presented more species than other

snake assemblages from other protected areas of Atlantic Forest, including Núcleo Santa Virginia of Serra do Mar State Park, São Paulo, with 27 species (Hartmann et al., 2009a), Núcleo Picinguaba of Serra do Mar State Park, São Paulo, with 24 species (Hartmann et al., 2009b), Taquara Natural Municipal Park, Rio de Janeiro, with 21 species (Salles et al., 2010), Intervales State Park, São Paulo, with 19 species (Sazima, 2001) and Mata do Buraquinho Permanent Protect Area, Paraíba, with 18 species (Santana et al., 2008). However, the difference in richness was not large among the areas, and the richness of Atlantic Forest areas should be between 19 and 40 species (Pereira Filho, 2011). This richness per locality is lower than area in the Amazon (ca. 42–66 species;

Table 1. Abundance and relative abundance of each species recorded at the study site, as well as the sampling methods with which they were captured.

PT = pitfall traps with drift fences; RS = road sampling; LC = local collectors; TVES = timed visual encounter survey; IE = incidental encounters; ABUND = abundance; RELAT ABUND % = relative abundance.

FAMILY/SPECIES PT RS LC TVES IE ABUND RELAT ABUND % Typhlopidae Merrem, 1820

Amerotyphlops brongersmianus (Vanzolini, 1976) 27 27 16

Amerotyphlops paucisquamus (Dixon and Hendricks, 1979) 42 42 26

Boidae Gray, 1825

Boa constrictor Linnaeus, 1758 1 1 1

Epicrates assisi Machado, 1945 4 1 5 3

Colubridae

Chironius exoletus (Linnaeus, 1758) 3 3 2

Chironius flavolineatus (Jan, 1863) 1 1 1

Drymarchon corais (Boie, 1827) 1 1 1

Drymoluber dichrous (Peters, 1863) 3 1 4 2

Oxybelis aeneus (Wagler in Spix, 1824) 1 1 1

Spilotes pullatus (Linnaeus, 1758) 1 1 2 1

Tantilla melanocephala (Linnaeus, 1758) 24 1 25 15

Dipsadidae

Apostolepis cearensis Gomes, 1915 3 3 2

Boiruna sertaneja Zaher, 1996 1 1 1

Erythrolamprus taeniogaster (Jan, 1863) 2 2 1

Imantodes cenchoa (Linnaeus, 1758) 1 1 1

Oxyrhopus trigeminus Duméril, Bibron and Duméril, 1854 8 1 1 2 12 7

Philodryas nattereri Steindachner, 1870 1 1 1

Philodryas olfersii (Lichtenstein, 1823) 1 1 2 1

Phimophis guerini (Duméril, Bibron and Duméril, 1854) 1 1 1

Sibon nebulatus (Linnaeus, 1758) 1 2 1 4 2

Sibynomorphus mikanii (Schlegel,1837) 2 2 1

Siphlophis compressus (Daudin, 1803) 1 1 2 1

Taeniophallus affinis (Günther, 1858) 1 1 1

Taeniophallus occipitalis (Jan, 1863) 6 6 4

Thamnodynastes pallidus (Linnaeus, 1758) 1 1 1

Xenodon merremii (Wagler in Spix, 1824) 4 1 5 3

Elapidae

Micrurus aff. ibiboboca (Merrem, 1820) 6 6 4

Micrurus potyguara Pires, Silva, Feitosa, Prudente, Pereira

Filho and Zaher, 2014 1 1 1

Viperidae

Bothrops leucurus Wagler in Spix, 1824 1 1 1

TOTAL 133 21 3 4 3 164 100

4

(6)

Martins and Oliveira, 1998; Bernarde and Abe, 2006; Prudente et al., 2010; Bernarde et al., 2011) and Cerrado (ca. 21–61 species; Carvalho and Nogueira, 1998; França et al., 2008; Sawaya et al., 2008; Araujo et al., 2010), but higher richness than areas in the Caatinga (ca. 13–22 species; Vitt and Vangilder, 1983; Costa, 2006; Mesquita et al., 2013). Moreover, these variations in number of species may be due to the differences in the size of areas, sampling effort, and habitat structure.

The abundance of species differs from others areas in the Atlantic Forest, mainly by the dominance of fossorial snakes. In other snake assemblages of Atlantic Forest in southeastern Brazil, the species with high abundance are terrestrial, such as the dipsadid Erythrolamprus miliaris (Linnaeus, 1758) and the vipers Bothrops jararaca (Wied,

Figure 2. Variation of the temperature and the number of snakes

col-lected during the study.

Table 2. Snake composition of the study area with information about habits (F: fossorial; T: terrestrial; C: cryptozoic; SAB: semi arboreal; AB: arboreal;

SAQ: semi aquatic), diel activity (N: nocturnal; D: diurnal; DN: diurnal and nocturnal), and reference where information was obtained.

FAMILY/SPECIES HABITS ACTIVITY REFERENCE Typhlopidae Merrem, 1820

Amerotyphlops brongersmianus (Vanzolini, 1976) F N (Zug et al., 2001)

Amerotyphlops paucisquamus (Dixon and Hendricks, 1979) F N (Zug et al., 2001)

Boidae Gray, 1825

Boa constrictor Linnaeus, 1758 SAB DN (Rocha and Prudente, 2010)

Epicrates assisi Machado, 1945 T N (França et al., 2012), this work

Colubridae

Chironius exoletus (Linnaeus, 1758) SAB D (Hartmann et al., 2009a)

Chironius flavolineatus (Jan, 1863) SAB D (Sawaya et al., 2008)

Drymarchon corais (Boie, 1827) T D (Strussmann and Sazima, 1993), this work

Drymoluber dichrous (Peters, 1863) T D (Bernarde and Abe, 2006), this work

Oxybelis aeneus (Wagler in Spix, 1824) SAB D (Vitt and Vangilder, 1983), this work

Spilotes pullatus (Linnaeus, 1758) SAB D (Hartmann et al., 2009b), this work

Tantilla melanocephala (Linnaeus, 1758) C DN (Sawaya et al., 2008)

Dipsadidae

Apostolepis cearensis Gomes, 1915 F DN (Rocha and Prudente, 2010; França et al., 2012)

Boiruna sertaneja Zaher, 1996 T N (Gaiarsa et al., 2013), this work

Erythrolamprus taeniogaster (Jan, 1863) SAQ D (França et al., 2012)

Imantodes cenchoa (Linnaeus, 1758) AB N (Hartmann et al., 2009b)

Oxyrhopus trigeminus Duméril, Bibron and Duméril, 1854 T DN (Rocha and Prudente, 2010), this work

Philodryas nattereri Steindachner, 1870 SAB D (Mesquita et al., 2013)

Philodryas olfersii (Lichtenstein, 1823) SAB D (Mesquita et al., 2013)

Phimophis guerini (Duméril, Bibron and Duméril, 1854) C N (Sawaya et al., 2008)

Sibon nebulatus (Linnaeus, 1758) SAB N This work

Sibynomorphus mikanii (Schlegel,1837) T N (Costa et al., 2010), this work

Siphlophis compressus (Daudin, 1803) SAB N (Bernarde and Abe, 2006), this work

Taeniophallus affinis (Günther, 1858) C D (Hartmann et al., 2009b)

Taeniophallus occipitalis (Jan, 1863) C D (Sawaya et al., 2008)

Thamnodynastes pallidus (Linnaeus, 1758) SAB N (Vitt and Vangilder, 1983), this work

Xenodon merremii (Wagler in Spix, 1824) T D (Rocha and Prudente, 2010), this work

Elapidae

Micrurus aff. Ibiboboca (Merrem, 1820) C DN (França et al., 2012), this work

Micrurus potyguara Pires, Silva, Feitosa, Prudente, Pereira Filho and Zaher, 2014 C DN (França et al., 2012), this work

Viperidae

(7)

1820) and Bothrops jararacussu Lacerda, 1884 (Hartmann et al., 2009a; Hartmann et al., 2009b; Pontes et al., 2009). Fossorial snakes, such as Liotyphlops ternetzii (Boulenger, 1893) in Distrito Federal (França et al., 2008), Trilepida

koppesi (Amaral, 1955) in Itirapina (Sawaya et al., 2008)

and Tantilla melanocephala, which is very common in many Cerrado snake assemblages (França et al., 2008; Sawaya et al., 2008; Araujo et al., 2010), are not abundant in most assemblages of Brazil except in Cerrado. The habitat structure of the tabuleiros with savanna-like vegetation, scattered trees, and sand soil, may be suitable for fossorial snakes. Therefore, the high number of fossorial snakes found in the tabuleiro can be associated with the savanna-like habitat structure. However, the three most abundant species in this study are also commonly found in forest fragments near Guaribas Reserve, indicating that these species are not exclusive to savanna-like habitats.

The structure of savanna-like vegetation found in the study area may account for high diversity of terrestrial snake species, such as found in other snake assemblages in Cerrado core areas (França et al., 2008; Sawaya et al., 2008). Even colubrids that are mainly characterized by arboreal species (Cadle and Greene, 1993), in these open habitats they are represented by a high number of terrestrial species.

The two most effective methods of capturing snakes in Rebio Guaribas were pitfall traps and car searches, although other methods were important to contribute to species richness. Pitfall traps are responsible for 81% of all individuals collected, a result rather unusual, given that pitfall traps are a sampling method that often have collected fewest snakes in other studies (Hartmann et al., 2009b; Rocha and Prudente, 2010; Rodrigues and Prudente, 2011; Mesquita et al., 2013). However, this sampling method is highly effective for capturing fossorial and cryptozoic snakes (Cechin and Martins, 2000). Herein, the large number of individuals collected by pitfall traps can be due to the high abundance of fossorial snakes. We used 60 L buckets for pitfalls, which can capture even 1 m long snakes (Greenberg et al., 1994). Smaller buckets cannot maintain medium-size snakes, and larger buckets are difficult to inspect. We collected fossorial and terrestrial snakes, such as Amerotyphlops

brongersmianus and Xenodon merremii (Wagler in Spix,

1824), but also some semi-arboreal species, such as

Siphlophis compressus (Daudin, 1803), Sibon nebulatus

(Linnaeus, 1758), and Chironius flavolineatus (Jan, 1863). The car searches method was effective for collect larger and less abundant snakes, such as Boa constrictor Linnaeus, 1758, Epicrates assisi Machado, 1945, Drymarchon corais (Boie, 1827), and Boiruna sertaneja Zaher, 1996. This method is considered efficient for surveys because the continuous flow of cars struck many animals (Spellerberg, 2002). However, the results of this method can be difficult to compare with other studies because of differences in

sampling effort (length of roads, times of search per week), and lack of paved roads in many areas.

The relationship between activity and phylogeny is evident because almost all species that belong to the same family are active during the same time period (França et al., 2008). Even in the richest family, Dipsadidae, snakes share the same activity inside the tribes, such as Philodryadini Cope, 1886 (i.e., Philodryas Wagler, 1830 are all diurnal) and Pseudoboini Bailey, 1967 (i.e., Boiruna Zaher, 1996; Oxyrhopus Wagler, 1830; Phimophis Cope, 1860 and Siphlophis Fitzinger, 1843 are all nocturnal).

Finally, we found that minimum temperature was more important for seasonal activity of snakes in tabuleiros than other abiotic factors. Temperature is an important component that determines snake activity worldwide (Gibbons and Semlitsch, 1987). Other Brazilian snake assemblages are also influenced by temperature (Winck et al., 2007; Sawaya et al., 2008; Hartmann et al., 2009a; Hartmann et al., 2009b), principally because minimum temperatures can reduce the metabolic rates of the snake species (Lillywhite, 1987). Like temperature, precipitation usually has an important effect on communities of open areas such as the Cerrado and Caatinga biomes (França and Braz, 2013; Mesquita et al., 2013). However, our tabuleiro area shows a higher precipitation rate and less seasonality than Cerrado and Caatinga due to the influence of Atlantic Forest climate. This may be a major reason for the low influence of precipitation.

ACKNOWLEDGMENTS

We thank the research group of the Laboratory of Animal Ecology of Campus IV of UFPB for their support in data colletion, especially Rafaela Cândido de França, Ivan Lívio Rocha Sampaio, Diego Barros Pinheiro, Taíssa Regis, Anna Carolina Figueiredo de Albuquerque, Rafaela Amorim, Carlos Eduardo de Sousa Germano, Tamara Brito, Robério Júnior e Jonas Matias. FGRF thanks the financial support from the CNPq (Universal grant 474250/2010-5), GAPF is supported by a postdoctoral fellowship from FAPESP (2012/19753-6), and we also thank ICMBio/REBIO Guaribas for the usage of the study area and logistical support. Fieldwork was authorized by ICMBIO/SISBIO permits 22940-1 and 22940-2.

REFERENCES

Amaral A. 1955. Contribuição ao conhecimento dos ofidios

neotro-picos: XIV. Descrição de duas espécies novas de “cobra-cega” (fam. Leptotyphlopidae). Memórias do Instituto Butantan 26:203–205.

Araujo C.O., Corrêa Filho D.T., Sawaya R.J. 2010. Snake

assembla-ge of Estação Ecológica de Santa Bárbara, SP: A Cerrado remnant in Southeastern Brazil. Biota Neotropica 10:235–245. doi:10.1590/ S1676-06032010000200026

6

(8)

Argôlo A.J.S. 2004. As Serpentes dos Cacauais do Sudeste da Bahia.

Editus, Ilhéus.

Bailey J.R. 1967. The synthetic approach to colubrid classification.

Herpetologica 23:155–161.

Bernarde P.S., Abe A.S. 2006. A snake community at

Espigão do Oeste, Rodônia, southwestern Amazon, Brazil. South American Journal of Herpetology 1:102–113. doi:10.2994/1808-9798(2006)1[102:ASCAED]2.0.CO;2

Bernarde P.S., Machado R.A., Turci L.C.B. 2011. Herpetofauna da

área do Igarapé Esperança na Reserva Extrativista Riozinho da Li-berdade, Acre – Brasil. Biota Neotropica 11:117–144.

Bérnils R., Batista M., Bertelli P. 2001. Cobras e lagartos do vale:

levan-tamento das espécies de Squamata (Reptilia, Lepidosauria) da bacia do rio Itajaí, Santa Catarina, Brasil. Revista de Estudos Ambientais 3:69–79.

Bérnils R.S., Costa H.C. 2014. Répteis brasileiros: Lista de espécies.

Herpetologia Brasileira 3:74–83

Boie F. 1827. Bemerkungen Über Merrem’s Versuch eines Systems der

Amphibien, 1. Lieferung: Ophidier. Isis van Oken 20:508–566.

Bonaparte C.L. 1840. A new systematic arrangement of vertebrated

animals. Transactions of the Linnean Society of London 18:247–304

Boulenger G.A. 1893. Catalogue of the Snakes in the British Museum

(Natural History). Taylor and Francis, London.

Cadle J.E., Greene H.W. 1993. Phylogenetic patterns, biogeography,

and the ecological structure of Neotropical snake assemblages. Pp. 281–293, in Ricklefs R.E., Schluter D. (Eds.), Species Diversity in Ecological Communities: Historical and Geographical Perspectives. University of Chicago Press, Chicago.

Carvalho M.A., Nogueira F. 1998. Serpentes da área urbana de

Cuia-bá, Mato Grosso: aspectos ecológicos e acidentes ofídicos associa-dos. Cadernos de Saúde Pública 14:753–763.

Cechin S., Martins M. 2000. Eficiência de armadilhas de

que-da (pitfall traps) em amostragens de anfíbios e répteis no Bra-sil. Revista Brasileira de Zoologia 17:729–740. doi:10.1590/ S0101-81752000000300017

Colli G.R., Bastos R.P., Araujo A.F. 2002. The character and dynamics

of the Cerrado herpetofauna. Pp. 223–241, in Oliveira P., Marquis R. (Eds.), The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York.

Colwell R. 2009. EstimateS: Statistical estimation of species richness

and shared species from samples, 8.2.0. Available from: http:// viceroy.eeb.uconn.edu/estimates.

Colwell R.K., Coddington J.A. 1994. Estimating terrestrial

biodiversity through extrapolation. Philosophical Transactions of the

Royal Society of London 345:101–118.

Colwell R.K., Mao C.X., Chang J. 2004. Interpolating, extrapolating,

and comparing incidence-based species accumulation curves.

Ecology 85:2717–2727. doi:10.1890/03-0557

Cope E.D. 1860. Catalogue of the Colubridae in the Museum of the

Academy of Natural Sciences of Philadelphia, with notes and descriptions of new species. Proceedings of the Academy of Natural

Sciences of Philadelphia 12:241–266.

Cope E.D. 1886. An analytical table of the genera of snakes. Proceedings

of the American Philosophical Society 23:479–499.

Costa H.C., Pantoja D.L., Pontes J.L., Feio R.N. 2010. Serpentes do

município de Viçosa, Mata Atlântica do Sudeste do Brasil. Biota

Ne-otropica 10:353–377.

Costa T.B.G. 2006. Estrutura da Comunidade de Serpentes de uma

Área de Caatinga do Nordeste Brasileiro. Masters Dissertation, Uni-versidade Federal do Rio Grande do Norte, Brazil.

Daudin F.M. 1803. Histoire Naturelle Generale et Particuliere des

Reptiles. F. Dufart, Paris.

Dixon J.R., Hendricks F.S. 1979. The wormsnakes (family

Typhlopidae) of the Neotropics, exclusive of the Antilles. Zoologisch

Verhandelingen 173 3–39.

Duméril A.M.C., Bibron G., Duméril A. 1854. Erpétologie Générale.

Roret, Paris.

Fitzinger L.J. 1843. Systema Reptilium. Braumüller et Seidel,

Vindobonae.

França F.G.R., Braz V.S. 2013. Diversity, activity patterns, and

habitat use of the snake fauna of Chapada dos Veadeiros National Park in Central Brazil. Biota Neotropica 13:74–84. doi:10.1590/ S1676-06032013000100008

França F.G.R., Mesquita D.O., Nogueira C.C., Araújo A.F. 2008.

Phylogeny and ecology determine morphological structure in a snake assemblage in the Central Brazilian Cerrado. Copeia 2008:23– 38. doi:10.1643/CH-05-034

França R.C., Germano C.E.S., França F.G.R. 2012. Composition of

a snake assemblage inhabiting an urbanized area in the Atlantic Forest of Paraíba State, Northeast Brazil. Biota Neotropica 12:1–13. doi:10.1590/S1676-06032012000300019

Gaiarsa M.P., Alencar L.R., Martins M. 2013. Natural history

of Pseudoboine snakes. Papéis Avulsos de Zoologia 53:261–283. doi:10.1590/S0031-10492013001900001

Galindo-Leal C., Câmara I.G. 2003. Atlantic Forest hotspot status:

an overview. Pp. 3–11, in Galindo-Leal C.,Câmara I.G. (Eds.), The Atlantic Forest of South America: Biodiversity Status, Threats and Outlook. Island Press, Washington.

Gibbons J.W., Semlitsch R.D. 1987. Activity patterns. Pp. 396–421,

in Seigel R.A., Collins J.T., Novak S.S. (Eds.), Snakes: Ecology and Evolutionary Biology. Macmillan, New York.

Gomes J.F. 1915. Contribution to the knowledge of Brazilian snakes.

Description of four new species and a new genus of opisthoglyphs.

Annais Paulista de Medicina e Cirurgia 4:121–129.

Gotelli N.J., Colwell R.K. 2001. Quantifying biodiversity: procedures

and pitfalls in the measurement and comparison of species richness.

Ecology Letters 4:379–391. doi:10.1046/j.1461-0248.2001.00230.x

Gray J.E. 1825. A synopsis of the genera of reptiles and Amphibia,

with a description of some new species. Annals of Philosophy 10:193–217.

Grazziotin F.G., Zaher H., Murphy R.W., Scrocchi G., Benavides M.A., Zhang Y.P., Bonatto S.L. 2012. Molecular phylogeny of

the new world dipsadidae (Serpentes: Colubroidea): a reappraisal.

Cladistics 28:437–459. doi:10.1111/j.1096-0031.2012.00393.x

Greenberg C.H., Neary D.G., Harris L.D. 1994. A comparison of

herpetofaunal sampling effectiveness of pitfall, single-ended, and double-ended funnel traps used with drift fences. Journal of

Herpetology 28:319–324.

Günther A. 1858. Catalogue of Colubrine Snakes of the British

Museum. London.

Hartmann P.A., Hartmann M.T., Martins M. 2009a. Ecologia e

história natural de uma taxocenose de serpentes no Núcleo Santa Virgínia do Parque Estadual da Serra do Mar no Sudeste do Brasil.

Biota Neotropica 9:1–12.

Hartmann P.A., Hartmann M.T., Martins M. 2009b. Ecology

of a snake assemblage in the Atlantic Forest of southeastern Brazil. Papéis Avulsos de Zoologia 49:343–360. doi:10.1590/ S0031-10492009002700001

Jan G. 1863. Elenco Sistematico degli Ofidi Descritti e Disegnati per

l’Iconografia Generale. Tipografia A. Lombardi, Milano.

Lacerda J.B. 1884. Leçons sur le Venin des Serpents du Brésil et sur la

Méthode de Traitement des Morsures Venimeuses par le Permanga-nate de Potasse. Lombaerts & C, Rio de Janeiro.

Lichtenstein H. 1823. Verzeichniss der Doubletten des Zoologischen

Museums der Königl. Universität zu Berlin: Nebst Beschreibung Vieler Bisher Unbekannter Arten von Säugethieren, Vögeln, Amphibien und Fischen/herausgegben von H. Lichtenstein. Commission bei T. Trautwein, Berlin.

Lillywhite H.B. 1987. Temperature, energetics, and physiological

ecology. Pp. 422–477, in Seigel R.A., Collins J.T., Novak S.S. (Eds.), Snakes: Ecology and Evolutionary Biology. Macmillan, New York.

Linnaeus C. 1758. Systema Naturæ. Regnum Animale. Sumptibus

Guilielmi Engelmann, Lipsiæ.

Machado O. 1945. Observações sobre ofídios do Brasil. Boletim do

Ins-tituto Vital Brazil 5:47–66.

Marques O.A.V., Sazima I. 2004. História natural dos répteis da

(9)

Duleba W. (Eds.), Estação Ecológica Juréia-Itatins: Ambiente Físico, Flora e Fauna. Holos, Ribeirão Preto.

Martins M., Oliveira M.E. 1998. Natural history of snakes in forests

of the Manaus region, Central Amazonia, Brazil. Herpetological

Na-tural History 6:78–150.

Merrem B. 1820. Versuch eines Systems der Amphibien I (Tentamen

Systematis Amphibiorum). J.C. Kriegeri, Marburg.

Mesquita P.C.M.D., Passos D.C., Borges-Nojosa D.M., Cechin S. 2013. Ecologia e história natural das serpentes de uma área de

Ca-atinga no nordeste brasileiro. Papéis Avulsos de Zoologia 53:99–113. doi:10.1590/S0031-10492013000800001

Morato S.A.A. 2005. Serpentes da Região Atlântica do Estado do

Para-ná, Brasil: Diversidade, Distribuição e Ecologia. Ph.D. Dissertation, Universidade Federal do Paraná, Brazil.

Nimer E. 1989. Climatologia do Brasil. Instituto Brasileiro de Geografia

e Estatística [IBGE], Rio de Janeiro.

Oliveira-Filho A., Carvalho D.A. 1993. Florística e fisionomia da

ve-getação no extremo norte do litoral da Paraíba. Revista Brasileira de

Botânica 16:115–130.

Oppel M. 1811. Die Ordnungen, Familien und Gattungen der Reptilien

als Prodrom einer Naturgeschichte Derselben. Von Michael Oppel. In commission bey J. Lindauer, München.

Pereira Filho G.A. 2011. Serpentes da Floresta Atlântica do estado da

Paraíba: Composição Faunística e Ecologia. Ph.D. Dissertation, Uni-versidade Federal da Paraíba, Brazil.

Peters W. 1863. Über einige neue oder weniger bekannte Schlangenarten

des zoologischen Museums zu Berlin. Monatsberichte der königlich

Akademie der Wissenschaften zu Berlin 29:272–289.

Pires M.G., Silva N.J. Jr., Feitosa D.T., Prudente A.L.C., Pereira Filho G.A., Zaher H. 2014. A new species of triadal coral snake

of the genus Micrurus Wagler, 1824 (Serpentes: Elapidae) from northeastern Brazil. Zootaxa 3811: 569–584. doi:10.11646/ zootaxa.3811.4.8

Pontes J.A.L., Pontes R.C., Rocha C.F.D. 2009. The snake community

of Serra do Mendanha, in Rio de Janeiro State, southeastern Brazil: composition, abundance, richness and diversity in areas with different conservation degrees. Brazilian Journal of Biology 69:795– 804. doi:10.1590/S1519-69842009000400006

Prudente A.L.C., Maschio G.F., Santos-Costa M.C., Feitosa D.T. 2010. Serpentes da Bacia Petrolífera de Urucu, Município de

Co-ari, Amazonas, Brasil. Acta Amazonica 40:381–386. doi:10.1590/ S0044-59672010000200016

R Core Team. 2013. R: A Language and Environment for Statistical

Computing. Available from: www.R-project.org

Radambrasil P. 1981. Levantamento Integrado dos Recursos Naturais

do Brasil. Folha Jaguaribe-Natal, Rio de Janeiro.

Ribeiro M.C., Metzger J.P., Martensen A.C., Ponzoni F.J., Hi-rota M.M. 2009. The Brazilian Atlantic Forest: How much is

left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142:1141–1153. doi:10.1016/j.biocon.2009.02.021

Rocha W.A., Prudente A.L.C. 2010. The snake assemblage of Parque

Nacional de Sete Cidades, state of Piauí, Brazil. South American

Journal of Herpetology 5:132–142. doi:10.2994/057.005.0207

Rodrigues F.S., Prudente A.L.C. 2011. The snake assemblage

(Squamata: Serpentes) of a Cerrado-Caatinga transition area in Castelo do Piauí, state of Piauí, Brazil. Zoologia 28:440–448. doi:10.1590/s1984-46702011000400005

Salles R.O.L., Weber L.N., Silva-Soares T. 2010. Reptiles,

Squama-ta, Parque Natural Municipal da Taquara, municipality of Duque de Caxias, state of Rio de Janeiro, southeastern Brazil. Check List 6:280–286.

Santana G.G., Vieira W.L., Pereira Filho G.A., Delfim F.R., Lima Y.C., Vieira K.S. 2008. Herpetofauna em um fragmento de

Floresta Atlântica no estado da Paraíba, Região Nordeste do Brasil.

Biotemas 21:75–84. doi:10.5007/2175-7925.2008v21n1p75

Sawaya R.J., Marques O.A.V., Martins M. 2008. Composição e

história natural das serpentes de Cerrado de Itirapina, São Pau-lo, sudeste do Brasil. Biota Neotropica 8:127–149. doi:10.1590/ S1676-06032008000200015

Sazima I. 2001. Répteis. Pp. 148–158, in Leonel C. (Eds.), Intervales:

Fundação para a Conservação e Produção Florestal do Estado de São Paulo. Fundação Florestal, São Paulo.

Sazima I., Haddad C.F.B. 1992. Répteis da Serra do Japi: notas sobre

história natural. Pp. 212–236, in Morellato L.P.C. (Eds.), História Natural da Serra do Japi: Ecologia e Preservação de uma Área Flo-restal no Sudeste do Brasil. Editora da Universidade Estadual de Campinas/Fundação de Apoio à Pesquisa do Estado de São Paulo, Campinas.

Schlegel H. 1837. Essai sur la Physionomie des Serpens/par H.

Schle-gel. Schonekat, Amsterdam.

Spellerberg I.F. 2002. Ecological Effects of Roads. Science Publishers,

Enfield.

Steindachner F. 1870. Herpetologische Notizen (II). Sitzungsberichte

der Kaiserlichen Akademie der Wissenschaften 62:326–350.

Strussmann C., Sazima I. 1993. The snake assemblage of the

Pantanal at Poconé, western Brazil: faunal composition and ecological summary. Studies on Neotropical Fauna and Environment 28:157–168.

Tabarelli M., Pinto L.P., Silva J., Hirota M., Bede L. 2005.

Challenges and opportunities for biodiversity conservation in the Brazilian Atlantic Forest. Conservation Biology 19:695–700. doi:10.1111/j.1523-1739.2005.00694.x

Thomas W.W., Barbosa M.R. 2008. Natural vegetation types in the

Atlantic Forest of northeastern Brazil. Pp. 6–20, in Thomas W.W. (Eds.), The Atlantic Coastal Forests of Northeastern Brazil. NYBG Press, New York.

Vanzolini P.E. 1976. Typhlops brongersmianus, a new name for

Typhlops brongersmai Vanzolini, 1972, preoccupied (serpents, typhlopidae). Papéis Avulsos de Zoologia 29:247.

Vitt L.J., Vangilder L.D. 1983. Ecology of a snake community in

northeastern Brazil. Amphibia–Reptilia 4:273–296.

Wagler J. 1824. Serpentum Brasiliensium Species Novae, ou Histoire

Naturelle des Espèces Nouvelles de Serpents, Recueillies et Obser-vées Pendant la Voyage dans l’interieur du Brésil Dans les Années 1817, 1818, 1819, 1820, Executé par Ordre de Sa Majesté le Roi de Bavière, Publiée par Jean de Spix. Typis Franc. Seraph. Hübschman-ni, Monaco.

Wagler J. 1830. Natürliches System der Amphibien: mit

Vorangehen-der Classification Vorangehen-der Säugethiere und Vögel: ein Beitrag zur ver-gleichenden Zoologie. J.G. Cotta’scchen Buchhandlung, München.

Wied N.M. 1820. Abbildungen zur Naturgeschichte Brasiliens. Isis von

Oken 15:1103.

Winck G.R., Santos T.d., Cechin S.Z. 2007. Snake assemblage in

a disturbed grassland environment in Rio Grande do Sul State, southern Brazil: population fluctuations of Liophis poecilogyrus and

Pseudablabes agassizii. Annales Zoologici Fennici 44:321–332.

Zaher H. 1996. A new genus and species of pseudoboine snake, with a

revision of the genus Clelia (Serpentes, Xenodontinae). Bollettino del

Museo Regionale di Scienze Naturali 14:289–337.

Zanella N., Cechin S.Z. 2006. Taxocenose de serpentes no Planalto

Médio do Rio Grande do Sul, Brasil. Revista Brasileira de Zoologia 23:211–217. doi:10.1590/S0101-81752006000100013

Zar J.H. 1999. Biostatistical Analysis. Prentice Hall, New Jersey. Zug G.R., Vitt L.J., Caldwell J.P. 2001. Herpetology: An Introductory

Biology of Amphibians and Reptiles. Academic Press, San Diego.