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Biodivers Conserv (2011) 20:36273643 DOI 10.

1007/s10531-011-0154-5 ORIGINAL PAPER

Vanishing bird species in the Atlantic Forest: relative importance of landscape conguration, forest structure and species characteristics
Alexandre Uezu Jean Paul Metzger

Received: 4 August 2010 / Accepted: 3 September 2011 / Published online: 13 September 2011 Springer Science+Business Media B.V. 2011

Abstract Patch size, isolation, and vegetation structure are expected to strongly affect species persistence in fragmented landscapes, particularly for those with \30% of native habitat remaining. Those inuences should be modulated by species characteristics, resulting in complex relationships. In order to investigate how species, habitat structure and landscape factors are related and how they affected species persistence, we studied bird communities in a fragmented Atlantic Forest region. Patch size strongly affected species richness and population abundances. However, some functional groups were more affected than others, particularly endemic and understory insectivores, species that are near the limits of their geographical distribution, those using few forest types, and those with their center of abundance in high altitude tropical forests. The effect of vegetation structure was mainly at the species level, reecting specic responses to habitat quality. The importance of landscape variables varies according to the species group. For the most affected ones, which usually have low dispersal capacity, patch size and quality were the most relevant factors, whereas patch isolation was associated with the richness of groups with more generalist species. This pattern is due to the limited structural connectivity in the study region, composed of low matrix permeability (e.g. pastures and sugar cane), which isolate the most affected species, making them more dependent on local factors. In such a fragmented landscape, the largest patches should be prioritized for conservation purposes, as they aggregate the most vulnerable species and present the highest alpha diversity. Landscape management, as such, should also reconnect large fragments through corridors
Electronic supplementary material The online version of this article (doi:10.1007/s10531-011-0154-5) contains supplementary material, which is available to authorized users. A. Uezu (&) Institute for Ecological Research, Rod. D. Pedro I, km 47, Caixa Postal 47, IPE Paulista, SP, Brazil Nazare e-mail: aleuezu@ipe.org.br URL: www.ipe.org.br J. P. Metzger o Paulo, Rua do Mata o, Department of Ecology, Institute of Bioscience, University of Sa o Paulo, SP 05508-900, Brazil 321, travessa 14, Sa e-mail: jpm@ib.usp.br

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or matrix improvements, promoting better conditions for long-term persistence of the most affected species. Keywords Biodiversity Connectivity Conservation Fragmentation Landscape Ecology Species sensitivity

Introduction Habitat loss and fragmentation are the main drivers threatening biodiversity worldwide (Fahrig 2003; Fischer and Lindenmayer 2007). In landscapes with less than 30% of their natural vegetation cover, which is the regional condition of most ecosystems in the world (Myers et al. 2000; DeFries et al. 2004; Ribeiro et al. 2009), patch size, isolation and n 1994; vegetation structure particularly inuence the persistence of organisms (Andre geli et al. 2010). However, the Aleixo 1999; Metzger 1999; Fahrig 2002; Fahrig 2003; Vo relative effects of these factors, and their synergism (Laurance and Cochrane 2001), may comprise a huge variation depending on landscape conguration, composition, and species characteristics (Ewers and Didham 2006; Martensen et al. 2008; Prugh et al. 2008; Shanahan and Possingham 2009; Pardini et al. 2010). Therefore, the mechanisms that provoke species loss are far from being understood (Prugh et al. 2008), especially regarding the more complex systems like tropical forests, such as the Atlantic Forest, the fourth most threatened biodiversity hotspot in the world (Mittermeier et al. 1999; Myers et al. 2000; Metzger 2009). The Atlantic Forest has 201 endemic bird species (Parker et al. 1996) and because of the severe deforestation and fragmentation (about 1116% of the original forest remains, Ribeiro et al. 2009), 102 species are classied in some category of threat (Pacheco and Bauer 2000; IUCN 2007). It is thus urgent to understand how structural factors and bird traits interact to determine the fate of some species in the Atlantic Forest. Patch size may inuence species probability of extinction (Hanski and Gilpin 1997; Ferraz et al. 2007) once population size declines in smaller patches, and therefore increase their susceptibility to stochastic events (e.g. genetic and demographic). The negative effects of small patches may be related to different mechanisms, such as decrease in habitat heterogeneity (Tews et al. 2004), higher limitation of resources (Zanette et al. 2000), reduction in the survival probability of patchily distributed species (Goerck 1997), reduction of synergism in species interactions (Maldonado-Coelho and Marini 2003), smaller chances to receive migrants from other areas (MacArthur and Wilson 1967), decrease in reproductive and foraging success (Fahrig 2001), and an increase of edge effects (Banks-Leite et al. 2010). However, patches may be part of a set of remnants that compose the required amount of habitat for species persistence (Price et al. 1999; Awade and Metzger 2008; Martensen et al. 2008; Boscolo and Metzger 2009). In this instance, patch size might not be a good explanatory variable for species presence, independent of the landscape context (Uezu et al. 2005). The effect of patch isolation depends not only on the geographic distance among patches, but also on: the matrix type and composition (Antongiovanni and Metzger 2005; Bender and Fahrig 2005), the contrast between habitat patch and the adjacent matrix (Baum et al. 2004), and the capacity of species to cross habitat edges (Schtickzelle and Baguette 2003) and to move in the matrix (Uezu et al. 2008). All of which are inuenced lisle 2005). Isolation may also decrease the long-term by species behavior ecology (Be persistence of a metapopulation (Hanski and Gilpin 1997) by causing higher mortality

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when individuals try to cross the matrix (Fahrig 2001), altering colonization-extinction dynamics. In addition to area and isolation, variations in vegetation structure may also inuence habitat availability for the species (Aleixo 1999; Marsden et al. 2001; Pardini et al. 2005; Shanahan and Possingham 2009). These variations may be natural, but can also be caused by human activities, particularly timber extraction, livestock grazing, and res. The altered areas may be avoided by some species, decreasing the effective size of forest remnants for these taxa (Moilanen and Hanski 1998). These structural factors inuence the community richness and diversity; however, to understand the mechanisms that cause the vanishing of some species and benet others, it is also necessary to consider species characteristics. Several studies have found that species extinction that follows habitat modication does not occur in a random trend, but depends on particular ecological traits (Newmark 1991; Castelletta et al. 2000; Ribon et al. 2003; Henle et al. 2004; Shanahan and Possingham 2009). A higher susceptibility may be modulated by intrinsic species features, and/or by particular regional context of environmental conditions. Species characteristics such as large body size, low exibility to use different types of forest, low relative abundance and type of resource exploitation (e.g., understory insectivores and large terrestrial birds), are usually associated with a higher vulnerability to human modication of natural habitats (Willis 1979; Goerck 1997; Renjifo 1999; Ribon et al. 2003; Henle et al. 2004). Additionally, variation in geographical location may also inuence how species respond to such changes. Particularly, species that are near the limits of their geographical distribution (Christiansen and Pitter 1997), and those that are outside their optimal altitudinal range (Kattan et al. 1994) and have a restricted geographical distribution, as the endemic species (Ribon et al. 2003), should be more sensitive. Therefore, the classication of species in functional groups can help to associate species features with their sensitivity to habitat fragmentation and thus can be useful to dene landscape management that benets the most vulnerable groups. Aiming to understand the processes that provoke species decline in the Atlantic Forest, we tested: 1. which bird traits (based on functional groups criteria) are more related to higher sensitivity; 2. how bird community, functional groups and species are affected by forest loss and fragmentation; and, 3. which structural factors (patch size, isolation or vegetation structure) are the most important explanatory variables, and for which bird groups.

Methods Study region The studied sites are in a region known as Pontal do Paranapanema (522929W and 22249S; Fig. 1). It is characterized by open hills, with gentle slopes (less than 15%; Ross and Moroz 1997). Oxisols are the predominant soil type (Oliveira et al. 1999). The vegetation is Tropical Semi-Deciduous Forest (Oliveira-Filho and Fontes 2000), one of the most threatened types inside the Atlantic Forest domain (Ribeiro et al. 2009). This forest is characterized by two distinct seasons: tropical, with rainy summers and high temperatures (reaching 40 C), followed by dry weather; and subtropical, without a dry season, but with physiological drought caused by the cold winters. The mean annual precipitation is about 1,500 mm.

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o Paulo. The large-scale map Fig. 1 The study region location in southeastern Brazil in the State of Sa illustrates in detail the Pontal do Paranapanema landscape and the locations of the sample units: control areas (C), large patches (L), medium patches (M) and small patches (S)

Deforestation in the Pontal do Paranapanema region began in the 1950s, mainly for forestry and pasture creation (Ferrari-Leite 1998). An important feature of the region is the presence of a continuous forest, the Morro do Diabo State Park, which is the largest remnant of Tropical Semi-Deciduous Forest in the state (*36,000 ha), being the best representation of the original form of this physiognomy. Adjacent to the park are forest patches ranging from 2 to 2,000 ha, mostly lying within private properties. The remaining forest now occupies about 13.1% of the region, including the state park, and only 4.4%

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without considering the park. The matrix is composed mainly of pasture (60.0%) and agriculture (20.0%; Fig. 1). Study sites Survey efforts were focused in 28 sample units: 21 forest patches and seven areas inside the continuous forest control (The Morro do Diabo State Park, Fig. 1). To ensure a large range of patch size, to represent the entire set of patches that are relevant for bird conservation in the region, we selected seven large patches (4001,500 ha), seven medium (100200 ha) and seven small ones (3080 ha). Surveyed patches are spread across the region, distant from each other (on average about 23.5 km, edge-to-edge), and in general ([90% of the times), more than 5,000 km from any other studied patch (Fig. 1). Patches are separated from each other mostly by a matrix of pasture and sugar cane. Small settlements also occur in low density. Data collection We conducted a bird survey using the point count methodology (Blondel et al. 1970). The counts were recorded over 10 min at each point and repeated eight times during the breeding season, between August and February, from 2003 until 2005, including two visits in 2003 and three visits in 20042005. Sampling began at approximately sunrise (*6:00 h) and lasted about 3 h. Sampling points were arranged in a rectangular 3 9 2 format, 200 m apart. The survey was undertaken by only one observer (the rst author), avoiding bias provoked by different bird identication capacity. Whenever there was any doubt about bird song, it was recorded for later identication. Based on this survey, we calculated for each species, in each sample unit, the point abundance index (PAI), where the numbers of visual or audio contacts with individuals of one species are divided by the number of sampled points. To avoid sampling bias in each visit the rst sample point was randomly selected and a sequential survey was undertaken in the other points. To test which species features are associated with the susceptibility to habitat loss and fragmentation, we classied birds into functional groups considering the following seven criteria. (1) Proximity to the edge of geographical distribution, which was dened by using maps of species distribution (Ridgely et al. 2005), measuring the distance (d) between a central point in the study region and the nearest limit of a species distribution. We established two categories: near the edge of distribution (d \ 200 km), and far from the edge (d [ 200 km). (2) Degree of endemism: endemic and non-endemic to the Atlantic Forest (Parker et al. 1996). (3) Center of abundance: lower altitudes (\500 m) and higher altitudes ([500 m; adapted from Parker et al. 1996). (4) Flexibility in the use of different forest types: 12 types; 36 types (Parker et al. 1996). (5) Relative abundance: low (uncommon, patchily distributed and rare species), medium (fairly common species) and high (common species). This classication is based on qualitative evaluations of eld ornithologists (Parker et al. 1996). (6) Guilds: carnivores, large canopy frugivores and omnivorous, large canopy insectivores, edge insectivores, understory insectivores, canopy insectivores, edge frugivores and omnivores, understory omnivores, and large ground insectivores and frugivores (Willis 1979; Parker et al. 1996; Reinert et al. 1996). (7) Abundance in the control sites: high and low. We divided species according to their mean abundance index (PAI) in the seven sites within the State Park using the median abundance among all species surveyed as a criterion for segregation.

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The vegetation structural data were collected along the three tracks where birds were sampled and in 13 5 9 5 m parcels, distributed regularly at each 10 m along the tracks, summing to 39 parcels in each sample unit. Inside each parcel, we estimated the thicket and herbaceous strata cover (0100%) and used the average of all parcels as a parameter for the patch. Along the tracks we counted the number of observed emergent trees ([15 m high). We used three parameters with relatively low correlation (R \ 0.45) to characterize vegetation structure: number of emergent trees, density of thicket and density of herbaceous strata. More degraded vegetation should present lower number of emergent trees and higher densities of thicket and vegetation in herbaceous strata (Ditt 2002). Consequently, the considered parameters must represent different degrees of habitat quality for bird species. We obtained the land cover map used to calculate the landscape metrics from a supervised classication of a Landsat-5 image from 2003, taken in the middle of the study period. For the landscape metrics, we only considered two categories of classication: forest and non-forest (overall accuracy [ 85%). Subsequently, we calculated landscape indexes that represent patch size and degree of isolation (Appendix 1). We selected two indexes that have low correlation (R = 0.02): logarithm of the area (AREA) and the logarithm of proximity (PROX). The latter consists of the sum of all patch areas (areainformed isolation metric), inside a ray of 2 km (which must be enough to isolate many of the forest species) from the edge of the studied patch, divided by the squared distance, edge-to-edge, between these patches (Elkie et al. 1999). This index is robust, representing fairly well the rates of immigrants that a patch can receive from other patches (Bender et al. 2003). Using a GPS we obtained the coordinates of the central points where bird surveys were conducted (minimal precision of 15 m). From these data, we calculated a matrix of distance among all points to evaluate the independence of bird data. Data analysis Initially, we veried the spatial dependency of bird community using Mantels test, correlating community similarity (based on Sorensen similarity index) and the matrix of distances among sample units. We then tested the effect of patch size and habitat fragmentation on population abundance, comparing with ANOVA the PAIs index of each species that occurred in at least 10 fragments, among the four treatments: control areas, large patches, medium patches and small patches. When the sampled data did not t the parametric test assumptions, we used KruskalWallis (Zar 1996). For signi s test (parametric) or cant results (P \ 0.05) we conducted a posteriori Scheffe Dunns test (non-parametric) to verify between which categories the differences were related to. Based on the previous analyses, birds were classied in three responsive groups according to their sensitivity to habitat loss and fragmentation: 1. affected, species that occur only in the control areas or in large patches (presence in fragments above 400 ha), or those that the abundance was positively correlated with patch size; 2. not affected, species evenly distributed among patches, regardless of patch sizes; and 3. beneted, species that the abundance was negatively correlated with patch size, or that only occur in smaller patches (presence in fragments below 400 ha). To verify which characteristics of functional groups are associated with sensitivity to patch size and fragmentation we used the v2 statistic, considering observed and expected (no difference) of species proportion in the three types of response groups (affected, not

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affected and beneted). For the guilds, we conducted this test only for groups that had a minimal sample size to assure the assumption of the test (Zar 1996). In order to identify the most important predictor variables to explain the species responses to habitat fragmentation, we conducted model selection, proposing simple (one variable) and multiple (combining two by two the co-variables) regressions using generalized linear model (nominal logistic regression, Dobson and Barnett 2008). We used as a response variable the species response to habitat fragmentation and loss (affected, not affected and beneted). For model selection, we used Akaikes Information Criterion adjusted for small samples (AICc), (Burnham and Anderson 1998), and calculated: AICc estimation of the relative distance between a candidate model and the real model; Di AIC relative difference of AICc value of every model in relation to the smallest value of AICc among all models; w AICc chance for the model to be selected, which varies from 0 to 1; evidence ratio relative fraction of the value of w AICc of every model with the higher value of w AICc among all models. We calculated bird species richness and Shannon diversity (H) for the bird community in each sampled area. We also calculated richness for the species functional groups. We did not include in the analysis species that are not forest-dependent according to the literature (Parker et al. 1996) and eld observations, with occasional occurrences in the sampled areas. Nor did we include species that did not t properly with the sampling methodology, such as some nocturnal species and those that vocalize inconspicuously. To verify how community, functional groups and bird species respond to forest fragmentation and which factors are the most important to determine their responses, we proposed eight linear models composed of all possible combination of the three explanatory variables (patch size, isolation and vegetation structure), plus a null model. To represent vegetation structure we used the rst factor of a PCA, done using the three vegetation variables collected in the eld (Appendix 1). We used model selection to rank the most likely models, given the collected data (see description above). We also calculated the relative importance of the variable, summing the chances of model selection (w AICc) of each model where a variable was included (Burnham and Anderson 1998) and the pseudo R2 pseudo coefcients of determination (Dobson and Barnett 2008). All analyses were conducted in R version 2.9.1. (R Development Core Team 2009). All models which presented values of Di AIC below two were considered, similarly, the most likely to be selected (Burnham and Anderson 1998).

Results We registered 13,677 contacts with birds, which represent 159 species, distributed in 40 families (Appendix 2). From those, 27 species are not forest-dependent, and 13 are nocturnal species or vocalize inconspicuously, and were thus not considered in the analyses. Among the surveyed forest birds, 52 were classied as affected by habitat loss and fragmentation, 44 were not affected, and 23 beneted in smaller patches (Appendix 2). We observed 15 species exclusively in control areas and 24 present in control or in large patches. Conversely, ve species were only detected in small or medium patches. The Mantels test revealed no spatial dependence among bird composition in the studied patches (r = 0.06; t = 1.15; P = 0.25) nor among the control areas (r = 0.01; t = 0.12; P = 0.91).

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Functional groups of sensitive species The number of species presented a high variation among the different functional groups (Appendix 3) and some of them were proportionally more negatively affected by habitat loss and fragmentation (Fig. 2). This was the case for 84% of the endemic species in the Atlantic Forest (X2 = 15.61; df = 2; P \ 0.01; Fig. 2a), 66% of the species located near the edge of distribution (\200 km; X2 = 12.67, df = 2, P \ 0.01; Fig. 2b), 76% of species which have their center of abundance in high elevation areas ([500 m; X2 = 13.42, df = 2, P \ 0.01; Fig. 2c), 66% of species with lower capacity of using different types of forest (12 types; X2 = 15.31, df = 2, P \ 0.01; Fig. 2d), 70% of the guild of understory insectivores (X2 = 11.25, df = 2, P \ 0.01; Fig. 2e), and 54% of the more abundant species in the control sites (X2 = 5.71, df = 2, P = 0.06; Fig. 2e). We could not perform statistical tests for groups with low abundance, guilds of understory omnivores and large terrestrial birds, because of the small number of sampled species. Nevertheless, we conclude that they comprise affected groups. Eight out of 12 species, which present low relative abundance, were veried to be affected by habitat loss and fragmentation, all understory omnivores were affected, and ve out of six large terrestrial were classied as affected (Appendix 2).

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Fig. 2 Percentage of species classied as affected, non-affected and beneted by habitat reduction and fragmentation, concerning different functional groups categorized by: a proximity to the edge of distribution; b degree of endemism in the Atlantic Forest; c center of abundance; d number of forest types they are able to use; and e understory insectivores. Pontal do Paranapanema, southeastern Brazil

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On the contrary, the guilds of carnivores, large canopy frugivores and omnivores, large canopy insectivores, edge insectivores, canopy insectivores and edge frugivores and omnivores, were not related to a higher sensitivity to habitat loss and fragmentation. The model composed of exibility in the use of different forest types and center of abundance is the most likely to explain the response of species to habitat fragmentation (AICc = 231.7, DAICc = 0, wAIC = 0.47). For all the others models DAICc presented higher than 2.0 (Appendix 4).

Patch size, isolation and vegetation structure Patch size, isolation and vegetation structure inuenced bird community, functional groups and species in different ways. For both community parameters, richness and diversity, the patch size (AREA) presented the highest relative importance in model selection (Table 1), although models which include patch isolation (PROX) and vegetation structure (VEG) were also ranked among the best models (Table 2).

Table 1 Relative importance of a variable (RwAICc) for bird community and functional groups parameters, considering the three covariates: patch size AREA; patch isolation PROX and vegetation structure VEG Functional groups Community Affected groups Richness Diversity Endemic 1-2 Types of forest Low Abundance High lands Edge of distribution (\200 km) Understory insectivores Understory omnivores Large ground insectivores and frugivores Non-affected groups Non-endemic [2 Types of forest dium abundance Me High abundance Low lands Center of distribution ([ 200 km) Carnivorous Large canopy frugivores and omnivores Large understory insectivores Edge insectivores Small canopy insetivores Edge omnivores and frugivores AREA 0.85 0.84 1.00 0.98 0.91 1.00 0.98 1.00 0.24 0.99 0.33 0.28 0.32 0.57 0.22 0.30 0.30 0.37 0.21 0.45 0.24 0.20 PROX 0.68 0.41 0.22 0.43 0.32 0.18 0.41 0.30 0.66 0.34 0.60 0.42 0.43 0.33 0.69 0.45 0.20 0.24 0.29 0.19 0.66 0.20 VEG 0.32 0.45 0.25 0.21 0.20 0.19 0.25 0.17 0.32 0.57 0.31 0.32 0.29 0.29 0.32 0.29 0.20 0.28 0.33 0.33 0.32 0.20

Higher values indicate the most important variables to explain bird richness and diversity. In bold are values higher than 0.50. Pontal do Paranapanema region, southeastern Brazil

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Table 2 The best models (DAICc \ 2) of richness and diversity variation of bird community and affected functional groups in the fragmented landscape of Pontal do Paranapanema region, southeastern Brazil Models Variables PseuR2 AICc DAICc wAIC Evidence ratio 1.00 2.22 1.00 1.31 1.39 2.27 1.00 1.00 1.26 1.00 2.19 1.00 1.00 1.39 1.00 2.28 1.00 2.15 2.31 1.00 2.02 2.12

Richness Diversity

md2 md5 md5 md2 md3 md1

AREA ? PROX AREA AREA AREA ? PROX AREA ? VEG AREA ? PROX ? VEG AREA AREA AREA ? PROX AREA AREA ? PROX AREA AREA AREA ? PROX AREA AREA ? PROX PROX PROX ? VEG 1 AREA ? VEG AREA ? PROX AREA

0.31 0.20 0.26 0.30 0.30 0.34 0.63 0.48 0.58 0.33 0.39 0.43 0.39 0.46 0.45 0.49 0.20 0.27 0.00 0.65 0.61 0.51

163.0 165.0 5.8 6.3 6.4 7.4 89.2 118.0 118.0 81.50 83.10 120.0 120.0 121.0 113.0 115.0 97.6 99.1 99.2 30.1 31.5 31.6

0.00 1.59 0.00 0.54 0.65 1.64 0.00 0.00 0.47 0.00 1.57 0.00 0.00 0.66 0.00 1.65 0.00 1.53 1.67 0.00 1.41 1.51

0.43 0.19 0.29 0.22 0.21 0.13 0.58 0.43 0.34 0.51 0.23 0.66 0.43 0.31 0.57 0.25 0.35 0.16 0.15 0.44 0.22 0.21

Endemic 12 types of forest Low abundance High altitudes Edge of distribution Understory insectivorous Understory omnivorous Large ground insectivores and frugivores

md5 md5 md2 md5 md2 md5 md5 md2 md5 md2 md6 md4 md0 md3 md2 md5

Pseudo R2 pseudo coefcients of determination, AICc the model distance to the real model, D AICc relative difference to the value of AICc of the best model, w AICc Akaikes weight, which is the chance for the model to be selected, Evidence ratio relative ratio regarding the weight (wAICc) of the best model

For the most affected functional groups, categorized based on the Chi-square statistics shown above, model selection presented similar patterns as the previous ones for community, however emphasizing a clear relative importance for patch size (Table 1). Generally the best model (for six functional groups out of eight affected ones) included only patch size (AREA) as covariate (wAIC C 0.43), although, models that include patch isolation (PROX) also ranked among the selected ones (wAIC [ 0.2 and evidence ration \2.3, Table 2). Analyzing functional groups separated imply in a higher certainty in model selection and a better t of the model to the observed data (see pseudo coefcient of determination in Table 2). For non-affected and beneted functional groups, models that included patch isolation (PROX) as a covariate were generally ranked among the most likely to be selected. However model selection presented a higher uncertainty (generally with wAIC of best model below 0.40), the observed data tted poorly to the models (PseudoR2 \ 0.30), and the null model always ranked among the best ones (see Appendix 5). This indicates that the proposed explanatory variables have low inuence on the richness of these functional groups of birds.

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Table 3 Mean and standard deviation of relative importance of a variable (RwAICc) for bird species abundance with different responses to habitat loss and fragmentation (af affected, b beneted, and naf nonaffected), considering the three covariates: patch size AREA, patch isolation PROX and vegetation structure VEG Species sensitivity Affected Beneted Non-affected AREA 0.82 0.21 0.69 0.21 0.28 0.11 PROX 0.20 0.06 0.38 0.49 0.27 0.13 VEG 0.46 0.28 0.48 0.29 0.39 0.22

Higher values indicate the most important variables to explain the abundance of birds in Pontal do Paranapanema region, Southeastern Brazil

Regarding species level, model selection presented a large variation among the species. However, a pattern emerges when we evaluate the results considering the species responses to habitat loss and fragmentation (Table 3, Appendix 6 and 7). For the most affected species (af), patch size (AREA) was the most important covariate, although the vegetation structure (VEG) was also an important explanatory variable for many species. For species beneted by habitat alteration, AREA and VEG were also important, but with opposite directions when compared with affected groups (Table 3, Appendix 6). For non-affected birds, there were slight differences among the relative importance of covariates (Table 3) and a higher uncertainty in model selection. Besides, the null model was among the most likely one for these groups of birds (Appendix 6).

Discussion The distinct responses of species and functional groups Habitat loss and fragmentation affect bird species and groups in different ways. Although previous studies assemble species based largely on trophic guilds (Willis 1979; Kattan et al. 1994; S ekercioglu et al. 2002; Ribon et al. 2003; Renjifo 1999), we veried that many additional species features might be helpful to distinguish congruent species responses to landscape structure. Some functional groups have proved to be more vulnerable than others. The endemics in the Atlantic Forest and those near the limit of their distribution are very affected by fragmentation, and because the study region is in the extreme west of the Atlantic Forest domain, many species are coincident in these two groups. For instance, species like Basileuterus leucoblepharus, Chiroxiphia caudata and Automolus leucophtalmus are endemic to the Atlantic Forest and have their geographical distribution limit near the Pontal region (Appendix 1). They only occur in the control areas or in some large patches, in very low density, whereas in eastern regions they are present in high abundance even in small and degraded patches (Anjos and Boc on 1999; Uezu et al. 2005; Martensen et al. 2008). In another study, also on the border of the Atlantic Forest, it was registered the vanishing of six species and the decline of two others (Christiansen and Pitter 1997), among whom ve were also reported in the present study as affected by fragmentation (Chiroxiphia caudata, Hemitriccu sorbitatus, Chamaeza campanisoma, Pyriglena leucoptera, and Procnias nudicollis), and another one (Selenidera maculirostris) was observed only in the control areas, although not during the current survey, probably as a consequence of its low density. The high similarity in these results greatly supports the idea that these patterns are not

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particular to a specic region. Moreover, Ribon et al. (2003) also found that endemic species of Atlantic Forest were more prone to go locally extinct. Near the border of their distribution the species would nd their ecological limits and, therefore, would likely have a lower density and restricted habitat availability (Kattan et al. 1994). In the extremes of distribution, recolonization would also be unlikely, as the number of sources for these events to occur is smaller than in a central region of a birds distribution (Renjifo 1999). Similarly, species with a center of abundance in higher elevation regions ([500 m) are more affected by fragmentation probably because the local altitude varies around 350 m. Therefore, like those near the border of geographical distribution, they would be at their ecological and altitudinal limits. Kattan et al. (1994) also veried such an effect for Andean birds where they veried that birds most susceptible to go locally extinct were both above and below their characteristic altitudinal range. Remarkably, the Pontal region still has some Atlantic Forest endemic species, present at low density and that are affected by fragmentation all over their geographical distribution. For example, Hemitriccus orbitatus (Christiansen and Pitter 1997; Aleixo 1999; Martensen et al. 2008), which is classied as near-threatened (IUCN 2007). The combination of these factors make them, globally, more threatened and of more conservation concern. This study revealed that birds that are more abundant in the control sites tend to be more affected by fragmentation. This result might be due to two reasons. Birds that are common abundant in small and degraded forest may have low density in continuous forest because they are less adapted to this latter condition. On the contrary, birds that are better adapted to continuous forest may not t well to a fragmented condition and so decline in abundance or disappear in fragments. However, this pattern may be blurry (the result is not statistically signicant, P = 0.06) because of two groups of species: some generalists, that benet in both conditions, and a group composed of the most sensitive and rare species, which present low abundance in continuous forest and also decline in forest patches. Birds that are less able to use different types of forest (12 types) must be more vulnerable because of their lower exibility to adapt to different conditions (Aleixo 1999), especially concerning the degraded vegetation, which is very frequent in the region (Ditt 2002). For these species, the fragmentation process is expected to be more restrictive. As forest remnants are usually composed of a mosaic of vegetation that differs in successional stages and degrees of degradation, the low exibility in the use of these physiognomies may reduce their effective area of occurrence and increase the isolation. It was not a surprise that birds with natural low abundance and the guilds of understory insectivores and large terrestrials birds were found to be more affected by habitat loss and fragmentation, as this result is congruent with many other studies (Willis 1979; Kattan et al. 1994; Stratford and Stouffer 1999; Goerck 1997; Renjifo 1999; S ekercioglu et al. 2002; Ribon et al. 2003). However, the understory omnivores, generally, are not considered a susceptible group. Probably, its higher sensitivity in the region is related to a lower capacity to cross the landscape matrix (Uezu et al. 2008), which is very resistant, the same cause as observed for understory insectivores. As well, most of the species included in this group are at the limit of their distribution in Pontal (Appendix 2), showing an interaction of these two characteristics. For the guild of large canopy frugivores and omnivores, we also found contrasting results with previous studies, as this group did not present a higher proportion of affected birds than expected by chance (see Willis 1979; Kattan et al. 1994; Newmark 1991; Renjifo 1999 for different results). These divergences may be caused by differences in landscape conguration (see next section) and distinct species composition. The combination of predictive variables of the functional groups is also important to understand species sensitivity to habitat fragmentation, as revealed by the model that

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aggregated the variable exibility in the use of different forest types and center of abundance. This result indicates that there must be synergistic or additive effects of species traits on species responses (Ewers and Didham 2006). A search for an integral understanding of species responses to habitat alteration must consider this multiple dimension of species characteristic. The inuence of patch size, isolation and vegetation structure Patch size and vegetation structure are the most important parameters for the affected groups. The effect of patch size is stronger and emerges at species, functional group and community levels. The inuence of vegetation structure is secondary, becoming visible at the species level, affecting their abundance variation. This is an important result as it shows that if we only focus on responses of higher levels of organization (community or functional groups), as frequently found in many studies, we may not recognize the effects of this latter covariate. The degree of isolation (PROX), in opposition to patch size and vegetation structure, inuences more the distribution of the non affected groups. This can be explained by the fact that many of these species are generalists and present a higher dispersion capacity, even along such an adverse matrix, as, for example: Amazona aestiva, Columba picazuro, Pitangus sulphuratus and Colaptes melanochlorus (Uezu et al. 2008). To understand the inuence of patch size, isolation and vegetation structure on bird abundance and richness in the studied region, we must evaluate the landscape conguration and composition. The patches are embedded in a hostile and contrasting matrix, composed of pasture and sugar cane, which must be very resistant for the movement of most forest species (Antongiovanni and Metzger 2005). In such a condition, if species could overcome the matrix resistance, interpatch distance could be a good predictor of species parameters (Bender and Fahrig 2005). However, it seems that the effective distances among forest patches surpasses the scale of the organisms movement, particularly for the affected species, with lower capacity to cross open areas (Baum et al. 2004; Uezu et al. 2008). As a result, these groups become completely isolated, relying solely on the intrinsic characteristics of patches: size and quality (Willis 1979; Aleixo 1999). In contrast, the nonaffected species probably can overcome the geographical distances among patches and make isolation an important explanatory variable. This result also shows that relative causal effects of landscape parameters and vegetation structure on biodiversity depends on the scale of species perception of the landscape. Our ndings differ from other studies in more connected Atlantic Forest landscapes (Anjos and Boc on 1999; Uezu et al. 2005; Develey and Metzger 2005; Martensen et al. 2008). In landscapes with short inter-patch distance and/or that are better connected by a network of corridors, the degree of isolation is more relevant to dene species distribution and abundance in forest patches (Uezu et al. 2005; Martensen et al. 2008). Furthermore, in such instances the threshold of patch size to guarantee the presence of the more affected species seems to be lower (20-50 ha; Anjos and Boc on 1999; Uezu et al. 2005; Martensen et al. 2008) than observed in this study (400 ha). These results emphasize the relative importance of the landscape parameters. In poorly connected landscapes, the patch size and habitat quality are essential to explain the variation of species richness and composition, whereas in better connected landscapes these factors have a secondary role and the landscape conguration (essentially parameters related with the landscape connectivity) becomes more signicant. This is a similar conclusion to that by Martensen et al. (2008) for birds and Pardini et al. (2010) for small mammals (although see Bender et al. 1998 and

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geli et al. 2010 for contrasting results in a meta-analysis). Conservation management Vo should regard such differences in landscape conguration.

Conservation recommendations Several implications for conservation emerge from the present study. In landscapes where habitat remnants are very isolated from each other, patch size is the most important parameter in determining biodiversity. Several species were observed exclusively in the control sites, indicating the need to keep continuous forest in a landscape, particularly to maintain the most affected species (Uezu et al. 2005). Large patches also contribute to regional biodiversity, as many species appear to have a threshold patch size of 400 ha before they are present. These tracts of forest prevent the local extinction of many species, as has been reported in other Atlantic Forest regions (Christiansen and Pitter 1997; Ribon et al. 2003; Develey and Metzger 2005), and therefore should be prioritized. Habitat quality should also be a concern in these areas, as it may outline the effective size of forest patches and determine the presence of several affected species. Landscape connectivity should also be promoted, as most of the populations of affected species are isolated in the large forest remnants due to the long distances among them and the high resistance of the matrix. To increase the chances of long-term survival of these populations (Hanski and Gilpin 1997), it is imperative to reconnect forest remnants using continuous corridors and matrix management (Baum et al. 2004; Uezu et al. 2008). Although medium and small patches (\200 ha) do not hold a very high biodiversity, and are almost depleted of sensitive species, they must be regarded for this purpose of increasing connectivity (Urban and Keitt 2001). Finally, the similar responses of some functional groups can assist us to understand how and why species are affected by habitat modication. Those groups could be used as conservation surrogates indicating the integrity of an ecosystem, priority areas for conservation, and what type of management should be accomplished in different situations, optimizing conservation efforts.
. Marini, Paulo Ina cio Prado and Wesley Silva Acknowledgements We thank Pedro Develey, Miguel A for revising previous version of this manuscript. We are in debt with Clinton Jenkins, for valuable suggestions and for improving the English. We are also grateful for the cooperation of the staff of Institute for Ecological Research. Financial support was provided by FAPESP (The State of Sa o Paulo IPE Research Foundation, process no. 02/01746-1), Idea Wild and Association of Field Ornithologists.

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