Diversity and Distribution of Lizards in Fragmented Atlantic Forest Landscape in Southeastern Brazil Author(s): Mauricio Almeida-Gomes and Carlos Frederico Duarte Rocha Source: Journal of Herpetology, 48(3):423-429. 2014. Published By: The Society for the Study of Amphibians and Reptiles DOI: http://dx.doi.org/10.1670/12-187 URL: http://www.bioone.org/doi/full/10.1670/12-187
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Journal of Herpetology, Vol. 48, No. 3, 423–429, 2014 Copyright 2014 Society for the Study of Amphibians and Reptiles
Diversity and Distribution of Lizards in Fragmented Atlantic Forest Landscape in Southeastern Brazil MAURICIO ALMEIDA-GOMES1,2,3 1
AND
CARLOS FREDERICO DUARTE ROCHA4
´ Programa de Pos-Gradua ca ¸ ˜ o em Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro. Avenida Carlos Chagas Filho 373, Cidade Universita´ria, 21941-902, Rio de Janeiro, Rio de Janeiro, Brazil 2 Departamento de Ecologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil 4 Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Rua Sa˜o Francisco Xavier, 524, CEP 20550-900, Rio de Janeiro, Rio de Janeiro, Brazil
ABSTRACT.—In this study, we evaluated how different lizard species were distributed in a fragmented Atlantic Forest landscape and the influence of landscape metrics on lizard species richness in sampled fragments. We sampled (between July 2007 and March 2010) three ´ continuous forest sites of the Reserva Ecologica de Guapiacu ¸ (REGUA), 12 forest fragments of different sizes and five pasture matrix areas. We recorded 8 lizard species, the most abundant being Ecpleopus gaudichaudii and Enyalius brasiliensis. Species richness in the continuous forest sites (N = 4) was lower than in the set of fragments (N = 8); fragments harbored both typical forest species and more generalist species. The forest areas differed in the composition of lizard species, with continuous forest sites having a composition similar to each other and to larger fragments, whereas the smaller fragments differed from the larger fragments but showed similarity to each other. These data indicated that fragment size (area) can be an important factor for the maintenance of lizard species diversity in fragmented Atlantic Forest landscapes. RESUMO.—Neste estudo avaliamos como as diferentes espe´cies de lagartos estavam distribuı´das em uma paisagem fragmentada de Mata ˆ ˆ Atlantica e a influencia das me´tricas da paisagem sobre a riqueza de espe´cies de lagartos nos fragmentos amostrados. Amostramos (entre julho ˆ localidades de floresta contı´nua da Reserva Ecologica ´ de 2007 e marco ¸ de 2010) tres de Guapiacu ¸ (REGUA), 12 fragmentos florestais de diferentes tamanhos e cinco a´reas de matriz de pasto. No total, registramos 8 espe´cies de lagartos e as mais abundantes foram Ecpleopus gaudichaudii e Enyalius brasiliensis. A riqueza de espe´cies encontrada nos sı´tios de floresta continua (N = 4) foi menor do que a encontrada no conjunto de fragmentos (N = 8), o que pode ser explicado pelo conjunto de fragmentos abrigarem tanto espe´cies tı´picas de ha´bitats florestais quanto espe´cies mais generalistas. As a´reas de floresta diferiram em relaca ¸ ˜ o a` composica ¸ ˜ o de espe´cies, com os sı´tios de floresta contı´nua tendo uma composica ¸ ˜o similar entre si e com os maiores fragmentos, enquanto que os menores fragmentos mostraram maior similaridade entre si. Esses dados indicam que o tamanho do fragmento (a´rea) pode ser um importante fator para a manutenca ¸ ˜ o da diversidade de espe´cies de lagartos em paisagens ˆ fragmentadas de Mata Atlantica.
Habitat loss and fragmentation are the main causes of declines and extinctions of species and contribute significantly to the reduction of diversity in different types of environments (Driscoll, 2004; Fischer and Lindenmayer, 2007; Pardini et al., 2009). Habitat loss and fragmentation transform the landscape into a complex mosaic, with fragments of different sizes and degrees of isolation immersed in a heterogeneous matrix (Umetsu et al., 2008; Ribeiro et al., 2009; Vieira et al., 2009). Parameters such as the size of remaining forest patches and landscape connectivity can significantly affect the persistence of animal populations in fragmented areas (Gascon et al., 1999; Ricketts, 2001; Dixo and Metzger, 2009). However, assessments of the possible impacts of these parameters on the local biota are still needed, especially in areas rich in biological diversity such as tropical rain forests (Turner et al., 1996; Laurance, 1999; Todd and Andrews, 2007). Among terrestrial vertebrates, reptiles represent the least studied group with respect to the assessment of potential negative effects of habitat loss and fragmentation on populations and species, despite evidence suggesting that these animals can be adversely affected by such processes (Dı´az et al., 2000; Gibbons et al., 2000; Lehtinen et al., 2003; Gardner et al., 2007). Some studies found a positive species-area relationship for reptiles (Smith et al., 1996; Alcala et al., 2004; Driscoll, 2004; Bell and Donnelly, 2006). However, in studies where only lizards were considered, the size of forest remnants generally did not affect the species richness, which was more affected by structure and quality of the habitat (Jellinek et al., 2004; Santos et al., 2008; Dixo and Metzger, 2009; Pardini et al., 2009). 3
Corresponding Author. E-mail:
[email protected]
DOI: 10.1670/12-187
Furthermore, for lizards there are some expected speciesspecific responses to edges, with some forest species being negatively affected, whereas more generalist species benefit (Schlaepfer and Gavin, 2001; Lehtinen et al., 2003; Gardner et al., 2007). The Atlantic Forest is one of the most threatened, and also fragmented, of the world’s biodiversity ‘‘hotspots.’’ There is little information about the potential effects of forest fragmentation on reptiles, and most of the available information refers only to leaf-litter lizards (Faria et al., 2007; Dixo and Martins, 2008; Dixo and Metzger, 2009; Pardini et al., 2009). The results of these studies show the importance of preserving large areas of forest and of increasing the connectivity among forest remnants. Our purpose in this study was to assess how lizard species are distributed in a fragmented landscape of the Atlantic Forest. The specific goals were to assess which species occur in an area of continuous forest, in the associated forest fragments, and in the surrounding matrix and to investigate whether there are relationships between species richness and landscape metrics. MATERIALS
AND
METHODS
Study Site.—We conducted the study between July 2007 and March 2010 in a fragmented landscape in the municipality of Cachoeiras de Macacu, State of Rio de Janeiro, Brazil. The ´ Reserva Ecologica de Guapiacu ¸ (hereafter REGUA) (22824 0 S, 0 42844 W) is a private reserve comprising about 7,200 ha of Atlantic Forest, most of which is continuous with the large ´ ˜ os mountain range (150,000 forest patch of the Serra dos Orga ha; Rocha et al., 2003). In continuous forest of REGUA, habitats range from secondary forests in the early stages of succession to
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FIG. 1. Map of study area, indicating continuous forest sites (CF1–CF3), sampled fragments (numbers 1–12), and sampled matrix areas (M1–M5), municipality of Cachoeiras de Macacu, state of Rio de Janeiro, Brazil.
areas of relatively undisturbed forest in the higher and more inaccessible portions of the reserve (Rocha et al., 2007). The area surrounding REGUA includes fragments of different sizes, degrees of regeneration and isolation, and different kinds of matrix (mainly pastures) (Almeida-Gomes and Rocha, 2014). In these fragments, there is a predominance of secondary forests in early stages of succession. The drier and colder part of the year in this region is between April and September, and the wetter and warmer period is between November and March (Bernardo et al., 2011). We sampled three continuous forest sites in REGUA (CF1–CF3, ranging from 100–186 ha and from 50–300 m), 12
forest fragments (F1–F12, ranging from 4.1–262.4 ha) and five pasture areas (matrix, M1–M5) (Fig. 1). We chose fragments with different sizes and degrees of isolation, to include the variation in these habitats. Collecting Methods and Analysis.—We used two different methods for lizard sampling: pitfall systems with drift fences (Corn, 1994) and visual encounter surveys (VES; Crump and Scott, 1994). We installed 15 pitfall/drift-fence systems, three at different sites within the continuous forest (ranging from 100– 200 m of altitude and at least 1 km from each other) and 12 sites in forest fragments (one system per fragment). The pitfall
LIZARD DIVERSITY IN A FRAGMENTED LANDSCAPE
425
´ TABLE 1. Lizard species abundances recorded during Visual Encounter Surveys in three continuous forest sites (CF1–CF3) of Reserva Ecologica de Guapiacu ¸ (REGUA), 12 forest fragments (F1–F12), and matrix areas (M), municipality of Cachoeiras de Macacu, state of Rio de Janeiro.
Gekkonidae Hemidactylus mabouia Gymnophtalmidae Ecpleopus gaudichaudii Leiosauridae Enyalius brasiliensis Phyllodactylidae Gymnodactylus darwinii Polichrotidae Anolis fuscoauratus Anolis punctatus Overall abundance
CF1
CF2
CF3
F1
F2
F3
F4
F5
F6
F7
F8
F9
F10
F11
F12
M
0
0
0
1
0
0
0
0
0
4
0
0
0
0
0
9
0
3
0
0
0
0
0
0
0
3
0
0
0
0
6
0
6
2
0
0
1
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
2
0
0
0
0
0
0
0 0 6
0 2 7
0 0 0
0 0 1
0 0 1
1 0 3
0 0 0
0 0 0
0 0 1
0 1 10
0 0 0
0 0 0
0 0 0
0 0 0
0 0 6
0 0 9
systems were placed at least 100 m from the forest edge of continuous forest and in the larger fragments and as far from the forest edge as possible within in smaller fragments. Each system had 11 60-liter buckets (approximately 60 cm of height) arranged 10 m apart in a line, connected by a drift fence (100 m total length for each system). All systems were sampled five times for six days (July–September 2007, January 2008, July 2008, January 2009, and August 2009), with a sampling effort of 4,950 trap days. Only during the first sampling period were the systems not opened simultaneously on consecutive days, because the systems were installed at different times. Sampling in the matrix was restricted to VES, because the risk of traps being trampled by cattle was high. Sampling by VES involved systematically inspecting different habitat types such as tree trunks, branches, and forest floor leaf-litter. We conducted VES at night (1900–0000 h) using headlamps in continuous forest sites, in the fragments, and in five pasture matrix areas (M1– M5). We performed VES during six periods (July to September 2007, December 2007 to March 2008, July to September 2008, January to March 2009, July to September 2009, and January to March 2010). Overall VES sampling effort totaled 960 h, ranged among sites from 9 (M2) to 114 h (F7). Visual encounter surveys were performed in different portions of the sampled areas (continuous forest sites, fragments, and matrix) to cover the largest possible area and the greatest variety of habitat types. We visited each continuous forest site and fragment at least six times and each matrix area at least four times. Landscape metrics used to understand the structuring of anuran communities in sampled fragments were area (ha) and proximity index = PROX: PROX=
n X aijs s=1
h2ijs
where aijs = area of the patch within the specified search radius of patch ij and hijs = the distance from patch ij to the neighboring patch of the same type, based upon edge-to-edge distance (Leita˜o et al., 2006). We used three buffer measures (500, 1,000, 2,000 m) for PROX calculation for each fragment (hereafter PROX 500, PROX 1000, and PROX 2000). This index tends to be higher when the focal patch is surrounded by larger or closer patches and, therefore, integrates information on the size and distance of like patches from a specified ‘‘focal patch’’ within a defined search radius (Leita˜o et al., 2006). For extraction of landscape metrics, we used the software ARCGIS 10.1.
Because of the relatively low richness and abundance of lizards found in our samples, the data obtained with VES and with pitfall systems were grouped and analyzed together. To evaluate the similarity in species composition and abundance among forest areas (continuous forest sites and fragments), we performed nonmetric Multidimensional Scaling (NMDS) using Bray-Curtis distance (Legendre and Legendre, 1998). This analysis was made using the software Systat 11. We used individual-based rarefaction (Gotelli and Colwell, 2001), which provides a richness estimation that is comparable among sampling areas with different sampling efforts, to evaluate whether there were differences in species richness for pooled data of continuous forest and fragments. We also used individual-based rarefaction, which provides data of abundance by lizard species, to compare observed richness in our study with those available studies in Atlantic Forest areas (e.g., Dixo and Verdade, 2006; Almeida-Gomes et al., 2008; Cicchi et al., 2009; Condez et al., 2009). For both analyses, we used EcoSim 7.71 (Gotelli and Entsminger, 2004) with 1,000 iterations. To understand the effect of landscape metrics on lizard species richness, we used model selection (Burnham and Anderson, 2002), which identifies the best approximating model, given the data and set of candidate models. To obtain AICc-values (Akaike’s Information Criterion corrected for small sample sizes), we assessed generalized linear models (GLMs) with Poisson distribution (Zuur et al., 2009) using R (vers. 2.13.0, R Development Core Team, 2011). We choose the best model(s) based on the weight of evidence (wi); the null model had only the intercept and error as parameters. RESULTS We recorded 98 individuals of 8 lizard species (Tables 1, 2). The most abundant species were Ecpleopus gaudichaudii Dume´ril and Bibron 1839 (29.6%) and Enyalius brasiliensis (Lesson 1830) (28.6%) (Tables 1, 2). In the continuous forest sites, we recorded 32 individuals belonging to four species, with the most abundant species being E. brasiliensis (68.7%) and E. gaudichaudii (21.8%). In the forest fragments, we recorded 57 individuals belonging to 8 species, and the most abundant species were E. gaudichaudii (38.6%) and Gymnodactylus darwini (Gray 1845) (30%). In the matrix, we recorded only nine individuals of the ` 1818). exotic species Hemidactylus mabouia (Moreau de Jonnes By VES, and considering all sampled areas, we found 6 lizard species (N = 44 individuals). We recorded Anolis punctatus Daudin 1802 and Anolis fuscoauratus D’Orbigny in Dume´ril and Bibron (1873) only by VES (Table 1), and the most abundant
426
M. ALMEIDA-GOMES AND C. F. D. ROCHA
´ TABLE 2. Lizard species abundances recorded by pitfall systems in three continuous forest sites (CF1–CF3) of Reserva Ecologica de Guapiacu ¸ (REGUA) and 12 forest fragments (F1–F12), municipality of Cachoeiras de Macacu, state of Rio de Janeiro.
Gekkonidae Hemidactylus mabouia Gymnophtalmidae Ecpleopus gaudichaudii Leiosauridae Enyalius brasiliensis Phyllodactylidae Gymnodactylus darwinii Scincidae Mabuya macrorhyncha Teiidae Tupinambis merianae Overall abundance
CF1
CF2
CF3
F1
F2
F3
F4
F5
F6
F7
F8
F9
F10
F11
F12
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
2
2
0
0
1
0
0
0
6
0
0
1
1
4
9
2
3
0
0
2
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
2
0
6
2
1
3
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0 9
1 5
0 5
0 0
0 0
0 3
0 0
0 2
0 1
0 13
1 3
0 1
0 5
1 2
0 5
species found by VES were H. mabouia (31.8%) and E. gaudichaudii (27.3%) (Table 1). Likewise, we recorded six lizard species (N = 54 individuals) by pitfall systems (considering all sampled forest areas). Mabuya macrorhyncha Hoge 1946 and Tupinambis merianae (Dume´ril and Bibron 1839) were recorded only by this methodology (Table 2). The most abundant species captured in pitfall traps were E. gaudichaudi (31.5%) and E. brasiliensis (31.5%) (Table 2). In terms of lizard species composition, the continuous forest sites were most similar to the three largest fragments (F3, F7, and F12) (Fig. 2). However, most small fragments (F5, F6, F8, F9, and F10) had lizard species composition more similar to each other and different from the largest fragments (Fig. 2). When we estimated species richness from the pooled data (using the abundance of 31 individuals recorded in continuous forest sites as the minimum abundance), we found a higher richness in the set of fragments (N = 6.7) when compared to the continuous
forest area (N = 4). Additionally, when we compared the estimated species richness from our study with estimates from other studies of Atlantic Forest areas, we found similar lizard species richness (Table 3). The model with fragment areas (wi = 0.670) was the best model in the model selection procedure (Table 4). DISCUSSION The species richness of lizards (8 species) found in our study was within the range of species richness (5 to 13 species) that has been found in other studied Atlantic Forest areas (Dixo and Verdade, 2006; Rocha and Van Sluys, 2006; Almeida-Gomes et al., 2008; Pardini et al., 2009). Although some of these studies have focused exclusively on leaf-litter lizards, the species of the genus Enyalius (which typically have more arboreal habits) were also included because they are frequently captured by pitfall systems (Dixo and Verdade, 2006; Faria et al., 2007; Dixo and Martins, 2008; Dixo and Metzger, 2009). Even after estimating richness by individual-based rarefaction, we also found similar species richness to other Atlantic Forest areas (Faria et al., 2007; Dixo and Martins, 2008; Cicchi et al., 2009; Dixo and Metzger, 2009), indicating that the lizard species richness found in our study is in accordance to that found in another Atlantic Forest areas. In general, studies show that the overall reptile abundance in Atlantic Forest areas is relatively low, particularly in southern Brazil (Dixo and Verdade, 2006; Almeida-Gomes et al., 2008; Cicchi et al., 2009; Dixo and Metzger, 2009). Although some of our data were collected at night by VES, which can underestimate some diurnal species, we believed that our use of two methods (VES and pitfall systems) reduces this possibility; diurnal species may be found resting on leaves or branches at night. We believe that the low overall lizard abundance TABLE 3. Lizard species abundances, richness and estimated richness from different available studies done in Atlantic Forest areas.
FIG. 2. Nonmetric Multidimensional Scaling (NMDS) in two axes showing similarity among three continuous forest sites (CF1–CF3) of ´ Reserva Ecologica de Guapiacu ¸ and 12 forest fragments (F1–F12) regarding the lizard species composition and abundance, municipality of Cachoeiras de Macacu, state of Rio de Janeiro, Brazil.
Dixo and Verdade, 2006 Faria et al., 2007 Almeida-Gomes et al., 2008 Cicchi et al., 2009 Condez et al., 2009 Dixo and Metzger, 2009 Present study
Abundance
Richness
Estimated Richness
111 431 16 44 160 228 98
4 12 6 5 8 5 8
2.4 5.9 6.0 4.3 4.1 2.8 5.1
LIZARD DIVERSITY IN A FRAGMENTED LANDSCAPE TABLE 4. Models predicting relationships among lizard species richness and landscape metrics, in an Atlantic Forest fragmented landscape. K = number of parameters; LL = model log likelihood; AICc = Akaike’s Information Criterion corrected for small samples; wi = evidence weight. The best model and the null model are in bold and italic format, respectively. Response variable
Richness
Model
K
LL
AICc
DAICc
wi
Area PROX 1000 PROX 2000 PROX 500 Null
3 3 3 3 2
-16.570 -17.942 -18.979 -19.095 -19.180
33.140 35.884 41.959 38.190 38.360
0.000 2.744 4.819 5.050 5.220
0.670 0.169 0.060 0.053 0.049
recorded in our study reflects the actual low abundance of most species in Atlantic Forest areas. The most abundant species recorded were the leaf-litter dweller E. gaudichaudii and the semiarboreal E. brasiliensis. Similarly, in other areas of Atlantic Forest in southeastern Brazil, E. gaudichaudii and species of the genus Enyalius have also been described as the most abundant among the recorded lizard species (Dixo and Verdade, 2006; Condez et al., 2009; Dixo and Metzger, 2009). Thus, our data and those of other studies suggest that, in areas of Atlantic Forest in southeastern Brazil, E. gaudichaudii and species of the genus Enyalius are the dominant species of lizards in their local communities. The species richness recorded in the continuous forest was lower than the total number of species recorded in the entire set of 12 fragments surveyed, even after we performed the individual-based rarefaction. In areas affected by habitat loss and fragmentation, the lizard composition can change with the disappearance of sensitive species and the increase in abundance of more generalized species (Bell and Donnelly, 2006; Scott et al., 2006; Urbina-Cardona et al., 2006; Dixo and Metzger, 2009). In the continuous forest area, with the exception of T. merianae, only typical forest-dwelling species were recorded (e.g., E. brasiliensis). However, in the set of fragments, not only forest species were recorded but also habitat-generalist species such as the invasive exotic H. mabouia and the native G. darwinii (see Pellegrino et al., 2005; Anjos and Rocha, 2008). Thus, the greater pooled species richness observed in the set of fragments can result from the fragments being able to sustain species typical of forest together with those species more tolerant to disturbed habitats. The occurrence of the exotic species H. mabouia within a few fragments reinforces the idea that this species is an invasive in remnants of Atlantic Forest (Rocha et al., 2011). This species has already started to occupy other natural environments such as the Cerrado and coastal ‘‘restingas’’ (Ro¨dder et al., 2008; Rocha et al., 2011). Some ecological characteristics of this species that may be responsible for its success in the occupation of new environments include its generalized diet and habitat requirements (Anjos and Rocha, 2008). Hemidactylus mabouia did not occur in the continuous forest but occupied areas near the edges of the fragments and was the only species found in the matrix. Thus, it is possible that this species has benefited from the process of habitat loss and fragmentation that has occurred in the area. Our data showed that most small fragments tend to be similar to each other in species composition and abundance of lizards. Additionally, the greater similarity between the largest fragments and the continuous forest sites, and the results of the
427
model selection, suggest that fragment sizes might affect the structuring of lizard communities. In general, large fragments have greater availability and diversity of resources when compared to smaller fragments, which theoretically allows the occurrence of larger populations (Bell and Donnelly, 2006; Metzger et al., 2009; Vieira et al., 2009). Small fragments generally have smaller populations, which are more subject to stochastic events (Fischer and Lindenmayer, 2007; Metzger et al., 2009; Vieira et al., 2009). However, fragment size generally does not affect the species richness in studies where only lizards were considered, which show that lizards are more affected by habitat structure and quality (Jellinek et al., 2004; Santos et al., 2008; Dixo and Metzger, 2009; Pardini et al., 2009). The relationship between lizard species richness and fragment size that we report may be explained either by the effect of area per se (i.e., ‘‘target effect’’) (MacArthur and Wilson, 1967) or by the quality and structure of habitats, which may also be related to fragment size (Alcala et al., 2004; Jellinek et al., 2004; Gardner et al., 2007; Santos et al., 2008). The use of different microhabitats by each species may be responsible for different responses to habitat loss and fragmentation (Schlaepfer and Gavin, 2001; Lehtinen et al., 2003; Dixo and Metzger, 2009). Arboreal lizards use the vertical strata in the forest more frequently than the horizontal one, which makes them more sensitive to structural changes in the vegetation than other species (Dixo and Metzger, 2009). However, some species, such as E. gaudichaudii, tend to be dependent on the quality of the leaf litter (Dixo and Metzger, 2009). The maintenance of large and continuous forest areas and the increase of landscape connectivity among forest fragments can be the most important factors for the conservation of diversity of leaf-litter lizard species in Atlantic Forest fragmented landscapes (Dixo and Metzger, 2009). Besides, some forest species have limited dispersal abilities, which can prevent the recolonization of fragments where the species has become extinct (Dı´az et al., 2000). At REGUA and the surrounding area, improvement in landscape connectivity would allow the continuous forest to function as a potential source area of dispersers to the fragments, minimizing the risk of local extinction. We conclude that the richness and abundance of lizard species found in our study is consistent with that of other Atlantic Forest areas, especially in southeastern Brazil. The higher species richness found in the set of fragments compared with that found in the continuous forest area can be explained by the presence of both typical forest species and more generalist species. The size (area) of forest fragments seems to affect the lizard species richness and composition, but we cannot discard the influence of environmental factors, such as microhabitat quality and availability. Acknowledgments.—This study was supported by research grants from the Conselho Nacional de Desenvolvimento ´ Cientı´fico e Tecnologico (CNPq) (processes 304791/2010-5 and 470265/2010-8) and from Fundaca ¸ ˜ o de Amparo a` Pesquisa do Estado do Rio de Janeiro (FAPERJ) through ‘‘Cientistas do Nosso Estado’’ Program (Process 26.102.765/2012) to CFDR. This project also benefited from funding from the ‘‘Edital Espe´cies Ameacadas’’ ¸ of Fundaca ¸ ˜ o Biodiversitas/CEPAN and RAN/ICMBio (Project 0158A/012006). We thank N. J. Locke of ´ the Reserva Ecologica de Guapiacu ¸ (REGUA) for making many facilities available during our fieldwork in that area. MA-G received Ph.D. fellowships from Conservation InternationalBrasil and FAPERJ and currently receives a Post-Doctoral
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fellowship from PNPD-CAPES. We thank all colleagues who helped us with data collection and D. Vrcibradic and M. Van Sluys for kindly revising a draft version of the manuscript. We also thank two anonymous reviewers that helped us to improve our manuscript.
LITERATURE CITED ALCALA, E. L., A. C. ALCALA, AND C. N. DOLINO. 2004. Amphibians and reptiles in tropical rainforest fragments on Negros Island, the Philippines. Environmental Conservation 31:254–261. ALMEIDA-GOMES, M., AND C. F. D. ROCHA. 2014. Landscape connectivity may explain anuran species distribution in an Atlantic Forest fragmented area. Landscape Ecology. In Press. ALMEIDA-GOMES, M., D. VRCIBRADIC, C. C. SIQUEIRA, M. C. KIEFER, T. KLAION, P. ALMEIDA-SANTOS, D. NASCIMENTO, C. V. ARIANI, V. N. T. BORGES JR., R. F. FREITAS-FILHO ET AL. 2008. Herpetofauna of an Atlantic Rainforest area (Morro Sa˜o Joa˜o) in Rio de Janeiro State, Brazil. Anais ˆ da Academia Brasileira de Ciencias 80:291–300. ANJOS, L. A., AND C. F. D. ROCHA. 2008. The Hemidactylus mabouia Moreau ` 1818 (Gekkonidae) lizard: an invasive alien species de Jonnes broadly distributed in Brazil. Natureza and Conservaca ¸ ˜ o 6:196–207. BELL, K. E., AND M. A. DONNELLY. 2006. Influence of forest fragmentation on community structure of frogs and lizards in northeastern Costa Rica. Conservation Biology 20:1750–1760. BERNARDO, C. S. S., H. LLOYD, N. BAYLY, AND M. GALETTI. 2011. Modelling post-release survival of reintroduced red-billed curassows Crax blumenbachii. Ibis 153:562–572. BURNHAM, K. P., AND D. R. ANDERSON. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, NY. CICCHI, P. J. P., H. SERAFIM, M. A. SENA, F. C. CENTENO, AND J. JIM. 2009. Herpetofauna em uma a´rea de Floresta Atlantica ˆ na Ilha Anchieta, municı´pio de Ubatuba, sudeste do Brasil. Biota Neotropica 9:201– 212. Available from: http://www.biotaneotropica.org.br/v9n2/pt/ fullpaper?bn01009022009+pt CONDEZ, T. H., R. J. SAWAYA, AND M. DIXO. 2009. Herpetofauna dos remanescentes de Mata Atlantica ˆ da regia˜o de Tapiraı´ e Piedade, SP, sudeste do Brasil. Biota Neotropica 9:157–185. Available from: http:// www.biotaneotropica.org.br/v9n1/pt/fullpaper?bn01809012009+pt CORN, P. S. 1994. Straight-line drift fences and pitfall traps. In W. R. Heyer, M. A. Donnely, W. M. Roy, and L. C. Hayek (eds.), Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians, pp. 109–117. Smithsonian Institution Press, Washington, DC. CRUMP, M. L., AND N. J. SCOTT JR. 1994. Visual encounter surveys. In W. R. Heyer, M. A. Donnelly, W. M. Roy, and L. C. Hayek (eds.), Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians, pp. 84–92. Smithsonian Institution Press, DC. DAUDIN, F. M. 1802. Histoire naturelle, generalle et particulieres des reptiles. Tome HI, Paris. ´ , T. SANTOS, AND J. L. TELLERI´A. 2000. DI´AZ, J. A., R. CARBONELL, E. VIRGOS Effects of forest fragmentation on the distribution of the lizard Psammodromus algirus. Animal Conservation 3:235–240. DIXO, M., AND M. MARTINS. 2008. Are leaf-litter frogs and lizards affected by edge effects due to forest fragmentation in Brazilian Atlantic Forest? Journal of Tropical Ecology 24:551–554. DIXO, M., AND J. P. METZGER. 2009. Are corridors, fragment size and forest structure important for the conservation of leaf-litter lizards in a fragmented landscape? Oryx 43:435–442. DIXO, M., AND V. K. VERDADE. 2006. Herpetofauna de serrapilheira da Reserva Florestal de Morro Grande, Cotia (SP). Biota Neotropica 6:1– 20. Available from: http://www.biotaneotropica.org.br/v6n2/pt/ fullpaper?bn00806022006+pt DRISCOLL, D. A. 2004. Extinction and outbreaks accompany fragmentation of a reptile community. Ecological Applications 14:220–240. ` des DUME´RIL, A. M. C., AND G. BIBRON. 1839. Histoire naturelle complete reptiles. Tome V, Paris. DUME´RIL, A. M. C., AND G. BIBRON. 1837. Erpe´tologie Ge´ne´rale ou Histoire Naturelle Complete des Reptiles. Vol. 4. Libr. Encyclope´dique Roret, Paris. FARIA, D., M. L. B. PACIENCIA, M. DIXO, R. R. LAPS, AND J. BAUMGARTEN. 2007. Ferns, frogs, lizards, birds and bats in forest fragments and
shaded cacao plantations of two contrasting landscapes in the Atlantic Forest, Brazil. Biodiversity and Conservation 16:2335–2357. FISCHER, J., AND D. B. LINDENMAYER. 2007. Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography 16:265–280. GARDNER, T. A., J. BARLOW, AND C. A. PERES. 2007. Paradox, presumption and pitfalls in conservation biology: the importance of habitat change for amphibians and reptiles. Biological Conservation 138: 166–179. GASCON, C., T. E. LOVEJOY, R. O. BIERREGAARD, J. R. MALCOM, P. C. STOUFFER, H. VASCONCELOS, W. F. LAURANCE, B. ZIMMERMAN, M. TOCHER, AND S. BORGES. 1999. Matrix habitat and species persistence in tropical forest remnants. Biological Conservation 91:223–229. GIBBONS, J. W., D. E. SCOTT, T. J. RYAN, K. A. BUHLMANN, T. D. TUBERVILLE, B. S. METTS, J. L. GREENE, T. MILLS, Y. LEIDEN, S. POPPY ET AL. 2000. The global decline of reptiles, deja-vu amphibians. Bioscience 50:653–667. GOTELLI, N. J., AND R. K. COLWELL. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4:379–391. GOTELLI, N. J., AND G. L. ENTSMINGER. 2004. EcoSim: Null Models Software for Ecology. Vers. 7. Acquired Intelligence, Inc. and Kesey-Bear, Jericho, VT. Available from: http://garyentsminger.com/ecosim/ index.htm. GRAY, J. E. 1845. Catalogue of the Specimens of Lizards in the Collection of the British Museum. Trustees of die British Museum, London. HOGE, A. R. 1946. Um novo lagarto da Ilha da Queimada Grande. ´ Memorias do Instituto Butantan 19:241–248. JELLINEK, S., D. A. DRISCOLLL, AND J. B. KIRKPATRICK. 2004. Environmental and vegetation variables have a greater influence than habitat fragmentation in structuring lizard communities in remnant urban bushland. Austral Ecology 29:294–304. LAURANCE, W. F. 1999. Reflections on the tropical deforestation crisis. Biological Conservation 91:109–117. LEGENDRE P., AND L. LEGENDRE. 1998. Numerical Ecology. Elsevier, Amsterdam. LEHTINEN, R. M., J. B. RAMANAMANJATO, AND J. G. RAVELOARISON. 2003. Edge effects and extinction proneness in a herpetofauna from Madagascar. Biodiversity and Conservation 12:1357–1370. LEITA˜O, A. B., J. MILLER, J. AHERN, AND K. MCGARIGAL. 2006. Measuring Landscapes: A Planner’s Handbook. Island Press, Washington, DC. LESSON, R. P. 1830. Description de quelques reptiles nouveaux ou peu connus. Zoologie 2:1–65. MACARTHUR, R. H., AND E. O. WILSON. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ. METZGER, J. P., A. C. MARTENSEN, M. DIXO, L. C. BERNACCI, M. C. RIBEIRO, A. M. G. TEIXEIRA, AND R. PARDINI. 2009. Time-lag in biological responses to landscape changes in a highly dynamic Atlantic Forest region. Biological Conservation 142:1166–1177. ` , A. 1818. Monographie du mabouja des murailles, on MOREAU DE JONNES Gecko Mabouja des Antilles. Bulletin des Sciences, Socie´te´ Philomatique de Paris 3:138–139. PARDINI, R., D. FARIA, G. M. ACCACIO, R. R. LAPS, E. MARIANO, P. A. PACIENCIA, M. DIXO, AND J. BAUMGARTEN. 2009. The challenge of maintaining Atlantic Forest biodiversity: a multi-taxa conservation assessment of an agro-forestry mosaic in southern Bahia. Biological Conservation 142:1178–1190. PELLEGRINO, K. C. M., M. T. RODRIGUES, N. A. WAITE, M. MORANDO, Y. Y. YASSUDA, J. W. SITES JR. 2005. Phylogeography and species limits in the Gymnodactylus darwinii complex (Gekkonidae, Squamata): genetic structure coincides with river systems in the Brazilian Atlantic Forest. Biological Journal of the Linnean Society 85:13–26. R DEVELOPMENT CORE TEAM. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing [Internet]. Available from: http://www.R-project.org. RIBEIRO, M. C., J. P. METZGER, A. C. MARTENSEN, F. J. PONZONI, AND M. M. HIROTA. 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142:1144–1156. RICKETTS, T. H. 2001. The matrix matters: effective isolation in fragmented landscapes. American Naturalist 158:87–99. ROCHA, C. F. D., AND M. VAN SLUYS. 2006. New records of reptiles from Ilha Grande Island in Rio de Janeiro State, Brazil. Herpetological Review 37:112–114. ROCHA, C. F. D., H. G. BERGALLO, M. A. S. ALVES, AND M. VAN SLUYS. 2003. A Biodiversidade nos Grandes Remanescentes Florestais do Estado do Rio de Janeiro e nas Restingas da Mata Atlantica. ˆ Rima Editora, Brasil.
LIZARD DIVERSITY IN A FRAGMENTED LANDSCAPE ROCHA, C. F. D., D. VRCIBRADIC, M. C. KIEFER, M. ALMEIDA-GOMES, V. N. T. BORGES-JUNIOR, P. C. F. CARNEIRO, R. V. MARRA, P. ALMEIDA-SANTOS, C. ´ ET AL. 2007. A survey of the leaf-litter C. SIQUEIRA, P. GOYANNES-ARAUJO ´ frog assembly from an Atlantic Forest area (Reserva Ecologica de Guapiacu) ¸ in Rio de Janeiro State, Brazil, with an estimate of frog densities. Tropical Zoology 20:99–108. ROCHA, C. F. D., L. A. ANJOS, AND H. G. BERGALLO. 2011. Conquering Brazil: the invasion by the exotic gekkonid lizard Hemidactylus mabouia (Squamata) in Brazilian natural environments. Zoologia 28: 747–754. RO¨DDER, D., M. SOLE´, AND W. BO¨HME. 2008. Predicting the potential distributions of two alien invasive house geckos (Gekkonidae: Hemidactylus frenatus, Hemidactylus mabouia) North-Western Journal of Zoology 4:236–246. SANTOS, T., J. A. DI´AZ, J. P. PE´REZ-TRIS, R. CARBONELL, AND J. L. TELLERI´A. 2008. Habitat quality predicts the distribution of a lizard in fragmented woodlands better than habitat fragmentation. Animal Conservation 11:46–56. SCHLAEPFER, M. A., AND T. A. GAVIN. 2001. Edge effects on lizards and frogs in tropical forest fragments. Conservation Biology 15:1079– 1090. SCOTT, D. M., D. BROWN, S. MAHOOD, B. DENTON, A. SILBURN, AND F. RAKOTONDRAPARANY. 2006. The impacts of forest clearance on lizard, small mammal and bird communities in the arid spiny forest, southern Madagascar. Biological Conservation 127:72–87. SMITH, G. T., G. W. ARNOLD, S. SARRET, M. ABENSPERG-TRAUN, AND D. E. STEVEN. 1996. The effect of habitat fragmentation and livestock grazing on animal communities in remnants of gimlet Eucalyptus
429
salubris woodland in the western Australian wheatbelt. II. Lizards. Journal of Applied Ecology 33:1302–1310. TODD, B. D., AND K. M. ANDREWS. 2007. Response of a reptile guild to forest harvesting. Conservation Biology 22:753–761. TURNER, I. M., K. S. Y. CHUA, B. C. SOONG, AND H. T. TAN. 1996. A century of plant species loss from an isolated fragment of lowland tropical rain forest. Conservation Biology 10:1129–1244. UMETSU, F., J. P. METZGER, AND R. PARDINI. 2008. Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic Forest small mammals. Ecography 31:359–370. URBINA-CARDONA, J. N., M. OLIVARES-PE´RES, AND V. H. REYNOSO. 2006. Herpetofauna diversity and microenvironment correlates across a pasture-edge-interior ecotone in tropical rainforest fragments in Los Tuxtlas Biosphere Reserve of Veracruz, Mexico. Biological Conservation 132:61–75. VIEIRA, M. V., N. OLIFIERS, A. C. DELCIELLOS, V. Z. ANTUNES, L. R. BERNARDO, C. E. V GRELLE, AND R. CERQUEIRA. 2009. Land use vs. fragment size and isolation as determinants of small mammal composition and richness in Atlantic Forest remnants. Biological Conservation 142: 1191–1200. ZUUR, A. F., E. N. IENO, N. J. WALKER, A. A. SAVELIEV, AND G. M. SMITH. 2009. Mixed effects models and extensions in ecology with R. Springer, New York. Accepted: 18 October 2013.
