Landscape Ecol (2009) 24:907918 DOI 10.

1007/s10980-009-9370-8

RESEARCH ARTICLE

Is bird incidence in Atlantic forest fragments inuenced by landscape patterns at multiple scales?
Danilo Boscolo Jean P. Metzger

Received: 6 June 2008 / Accepted: 2 June 2009 / Published online: 14 June 2009 Springer Science+Business Media B.V. 2009

Abstract The degree to which habitat fragmentation affects bird incidence is species specic and may depend on varying spatial scales. Selecting the correct scale of measurement is essential to appropriately assess the effects of habitat fragmentation on bird occurrence. Our objective was to determine which spatial scale of landscape measurement best describes the incidence of three bird species (Pyriglena leucoptera, Xiphorhynchus fuscus and Chiroxiphia caudata) in the fragmented Brazilian Atlantic forest and test if multi-scalar models perform better than single-scalar ones. Bird incidence was assessed in 80 forest fragments. The surrounding landscape structure was described with four indices measured at four spatial scales (400-, 600-, 800- and 1,000-m buffers around the sample points). The explanatory power of each scale in predicting bird incidence was assessed using logistic regression, bootstrapped with 1,000 repetitions. The best results varied between species (1,000m radius for P. leucoptera; 800-m for X. fuscus and 600-m for C. caudata), probably due to their distinct feeding habits and foraging strategies. Multi-scale models always resulted in better predictions than single-scale models, suggesting that different aspects of the landscape structure are related to different

ecological processes inuencing bird incidence. In particular, our results suggest that local extinction and (re)colonisation processes might simultaneously act at different scales. Thus, single-scale models may not be good enough to properly describe complex pattern process relationships. Selecting variables at multiple ecologically relevant scales is a reasonable procedure to optimise the accuracy of species incidence models. Keywords Landscape structure Spatial scale Incidence Fragmentation AUC Atlantic plateau Pyriglena leucoptera Xiphorhynchus fuscus Chiroxiphia caudata o Paulo Brazil Sa

Introduction Birds living in fragmented habitats are frequently subject to higher extinction risks than those in continuous environments (Wiens 1995; Stratford and Stouffer 1999; Brooker and Brooker 2001). This occurs because fragmentation usually leads to reduced habitat availability and may inuence the dispersal ability and spatial distribution of various bird species (Clergeau and Burel 1997; Metzger 1998; Mazerolle and Villard 1999; Bakker et al. 2002). Some authors suggest that in landscapes with a very low proportion of suitable habitat (less than 30%

D. Boscolo (&) J. P. Metzger Department of Ecology, Institute of Bioscience, o Paulo (USP), Rua do Mata o, trav. 14, no University of Sa 321, Cid. Universitaria, Sao Paulo 05508-900, Brazil e-mail: danilo.boscolo@gmail.com

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908

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of habitat cover), bird species survival may depend mainly on the size and isolation of the remaining n 1994; Metzger and De camps 1997). patches (Andre Thus, reduced habitat cover, patch size and connectivity have been argued to have negative effects on lu et al. 2002; Castropical forest birds (Sekerciog telletta et al. 2005; Develey and Metzger 2006). The sensitivity to each of these factors may vary among species (Ferraz et al. 2007). Uezu et al. (2005) found that frugivorous birds in the fragmented Brazilian Atlantic forest were more affected by patch size than insectivorous species, which were more abundant in patches connected to other forests by corridors. Similarly, Martensen et al. (2008) found that Atlantic forest birds of different functional groups, such as terrestrial or understory insectivores, were differently affected by patch area and connectivity. These studies, however, did not take into account the spatial scale at which landscape parameters were measured. In fragmented habitats, the degree to which the landscape structure inuences the incidence of a species can depend on processes happening at varying spatial scales (Gutzwiller and Anderson 1987; Wiens 1989; Levin 1992; Lindenmayer 2000; Cushman and McGarigal 2004; Vergara and Armesto 2009), considering either the landscape extent (Fuhlendorf et al. 2002) or grain (Rahbek and Graves 2001; Meyer and Thuiller 2006). Bird occurrence and abundance may actually be related to the spatial range in which individuals can perceive or be affected by different aspects of the surrounding environment that happen at different scales, such as habitat heterogeneity and isolation (van Rensburg et al. 2002; Ewers and Didham 2006). Lawler and Edwards (2002) suggest that selecting the right scale to assess the effects of landscape structure on bird incidence is essential for deriving useful predictive habitat models. Some authors even indicate that using multi-scalar approaches to produce these models for different species (mammals and birds) can yield better models than single-scalar approaches (Jaquet 1996; Lindenmayer 2000; Graf et al. 2005). Considering each factor at its most appropriate scale may help to better describe the species relationship to the surrounding environment. However, studies of model ecological systems comparing the effects of using single and multi-scalar approaches are rare, even though some authors have

nez et al. 2003; Wu stressed the need for them (Mart 2007; Renfrew and Ribic 2008). According to Li and Wu (2007), the effects of spatial patterns on ecological processes can be misleading because choosing the wrong scale of measurement can hide important aspects of landscape structure and composition that modify the observed system at coarser or more rened levels. This issue should be taken into account when habitat models relating bird incidence to landscape structure data are constructed (Thompson and McGarigal 2002; Graf et al. 2005). In such cases, the selection of the correct spatial scale to measure landscape structure and the choice between a single or multi-scalar approach are essential decisions when assessing how habitat fragmentation can affect the incidence and persistence of different bird species. Our objectives in this study were: (1) to determine which spatial scale of measurement best describes the incidence patterns of three small passerine bird species found in the fragmented Atlantic forest in southeastern Brazil and (2) to compare the performance of single and multi-scalar approaches in predicting bird occurrence. Due to severe deforestation, the Brazilian Atlantic forest is currently composed of extremely small and isolated remnants (Ribeiro et al. 2009), and the processes affecting species survival in such an environment are expected to be caused mainly by changes in landscape structure (Goodwin and Fahrig 2002). Within the last few years, some studies have tried to relate understory bird distribution patterns to the structure of fragmented Atlantic forest landscapes (Uezu et al. 2005; Develey and Metzger 2006), but they did not account for the effects of inappropriate scale choice on the accuracy of their results. To properly understand processes effects on forest birds persistence and incidence in the Atlantic forest, we need to assess the accuracy and explanatory power of landscape structure measurements at varying scales.

Methods Study sites For this study we selected 80 Atlantic forest o Paulo fragments in the southwest portion of Sa state, on the Atlantic Plateau of Sao Paulo, Brazil

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(Boscolo 2007). The relief is largely characterised by convex hills with a low density of deep valleys (Ross and Moroz 1997). The climate is predominantly temperate, warm and rainy. The original forest cover in the region was classied as dense montane ombrophylous forests (Oliveira-Filho and Fontes 2000), but the use of natural wooded areas for agricultural elds, logging and charcoal production has severely fragmented it. In the present day, most of the natural vegetation fragments found on the Atlantic Plateau are of second-growth forests of varying ages and sizes. These forests are composed of about 220 tree species, most of them from the Fabaceae, Myrtaceae and Rubiacea families. Despite their richness, these secondary forests differ significantly in species composition from more mature forests found in an adjacent forest reserve (Bernacci et al. 2006; Durigan et al. 2008). We chose fragments embedded in a wide range of forest cover (570% within an 800-m buffer) and connectivity conditions (proximity index ranges from 1.5 to 250.0 with an 800-m search radius; McGarigal and Marks 1995). The minimum distance from a focal fragment to the nearest forest was 20 m and the maximum 260 m. Fragment size ranged from 1.2 to 274.3 ha, with a mean area of 34.3 ha. To reduce variation related to matrix composition and habitat quality, we intentionally selected only second-growth fragments with similar internal forest structures that were surrounded mainly by non-forested eld matrices (Boscolo 2007). Selected species We selected for the present study three passerine bird species that are strictly associated with forest and are unable to survive in non-forested environments. All species are nonmigratory year-round residents, exhibit strong territorial behaviour and are known to respond to playback stimuli (Stotz et al. 1996). Playback methods to determine their presence/ absence pattern have been studied and are consolidated, making their survey more precise and efcient (Boscolo et al. 2006). Because of their different home-range sizes and abilities to move through the non-forested matrix, they are expected to perceive and react to the structure of the surrounding landscape with distinct sensitivities and at different scales nior et al. 2001). In (Sick 1997; Goerck 1999; Melo-Ju

addition, all three species are typical of three different widespread families of the Atlantic forest with very distinct biological traits and can be used to evaluate the effect of landscape scale on species with different ecological proles. Chiroxiphia caudata (Pipridae) is a small omnivorous bird that lives in groups with a strong hierarchical structure (Foster 1981; Sick 1997), a common characteristic of its family. It is able to cross up to 130 m of open matrix (Uezu et al. 2005) and has an average home-range size of 8 ha (Hansbauer et al. 2008). Xiphorhynchus fuscus (Dendrocolaptidae) is commonly seen in mixed bird ocks and, like most of the species in its family, can only land on upright logs (Brooke 1983; Soares and dos Anjos 1999). Individuals crossing an open matrix between forest patches must, therefore, do it in a single ight, which might limit the birds dispersal ability. The species expected habitat gap crossing ability is 150 m, and its home range is around 6 ha (Develey 1997; Boscolo et al. 2008). Pyriglena leucoptera (Thamnophilidae) is an ant-following bird that inhabits the understory of dense forests. Having a home-range size of about 15 ha (Hansbauer et al. 2008) and a gap crossing ability of only 60 m (Uezu et al. 2005), it is the most sensitive of the three species to habitat loss and fragmentation (dos Anjos and Boc on 1999). Bird surveys We collected bird species presence/absence data with the use of playback census techniques at one point per fragment located inside the forest and near the centre of each fragment. All surveys were done by the same person (DB) to avoid observer bias. The employed survey method was adapted from Boscolo et al. (2006) and consisted of broadcasting the songs of male birds to actively stimulate them and increase detection rates by making quiet individuals noticeable. Surveys occurred at the times of the day with the highest bird detection rates when using playbacks (Boscolo et al. 2006), namely sunrise and in the 2 h around noon. Boscolo et al. (2006) also attest that with the use of playback stimuli, the detectability of these birds does not vary throughout the year. For all species, each playback session lasted 5 min, followed by ve more minutes of silent observation, which was enough to account for late

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910 Fig. 1 Example of round landscape maps subset from the original classied images. a Part of the original map with concentric circles (grey lines) around a sampling point; b subset of round landscapes of varying radii, with bird sampling point in the centre. Black polygon: sampled forest fragment; Light grey polygons: other forests; White cross sampling point location

Landscape Ecol (2009) 24:907918

responsive birds. We noted a species as present at a given point if at least one individual was heard or seen within the surveyed fragment during or after the playback. We repeated the surveys in all fragments for 3 days in different weeks within 2 months of the rst survey of each sample point. If after this time no bird was detected at a certain point, we assumed the species to be absent at this location. According to Boscolo et al. (2006), three 10-min surveys on nonconsecutive days at a given location can assure for these species a probability greater than 95% of correct absence detection. In this manner, it was possible to assess bird occurrence with a reduced risk of false absence records (Thompson 2002), resulting in very precise presence/absence data. We conducted the bird surveys within the dry seasons from April 2004 to November 2005. Due to noise interference with bird detection, we did not execute playback sessions during rainy days or days with winds stronger than three in the Beaufort scale. Landscape structure We generated maps of forest cover for the studied region using ground-truth eld observations conducted together with the selection of study sites and

subsequent supervised classication of Landsat TM5 satellite images (bands 3, 4 and 5) from 2001. Because all fragments in the studied region consisted of similar second-growth forests and the landscape matrix mainly of open eld habitats, we classied land cover into only two classes, forest and nonforest. The nal maps consisted of raster les with 30-m pixel sizes for all landscapes. Based on groundtruthing, all maps accuracies were [90%. We plotted all bird sampling points on the digital maps and used them as central references to dene concentric circular buffers of varying radii representing distinct spatial extents or scales (Wu 2007). We used these buffers to subset the original classied images, generating round landscape maps of varying sizes (Fig. 1). We analysed the forest spatial structure inside each round landscape based on four landscape indices (Table 1) using FRAGSTATSTM (McGarigal and Marks 1995). All of these indices described either the connectivity or amount of available habitat in the landscape, factors we expected to directly affect bird occurrence patterns (Taylor et al. 1993; Wiens 1995; Fahrig 2003; Develey and Metzger 2006). We selected four spatial scales to be compared: 400-, 600-, 800- and 1,000-m radius. The total

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Landscape Ecol (2009) 24:907918 Table 1 Indices used to describe the landscape structure around each sample point at three different spatial scales Variable code PFOREST PD Variable name Proportion of forest Patch density Description

911

Proportion of the landscape covered by forest Number of fragments in the round landscapes divided by total landscape area Mean area of all forest patches in the landscape Mean Euclidian distance to the nearest neighbour patch averaged for all patches in the landscape

AREAMN ENNMN

Mean patch area Mean Euclidean nearestneighbour distance

landscape areas of each scale were correspondingly: 50.26, 113.10, 201.06 and 314.16 ha. These extents were chosen as tentative scales and are considered reasonable for most understory birds with homerange sizes up to 15 ha (Develey and Metzger 2006). We did not use smaller scales because they were too restrictive, and not all indices could be correctly measured. We also set an upper scale limit of 1,000 meters to avoid the problem of strong spatial autocorrelation of the round local landscapes. Scale comparison To evaluate the spatial scales at which the landscape structure best explained the birds occurrence patterns, we modelled their incidence using logistic regression with landscape indices as explanatory variables. We built single and multi-scale models, both including two landscape indices, using binomial (logit link) generalised linear models (GLM). Singlescale models were those in which both explanatory variables belonged to the same spatial scale, while multi-scale refers to the models containing independent variables of distinct scales in its structure. We assessed each models explained variance using its adjusted R2 value and estimated its signicance through log-likelihood (v2) tests. To avoid including two signicant highly correlated variables in the same model, we pairwise selected variables using the Spearman correlation rank rs (Green 1979; Fielding and Haworth 1995). For each species, all models had the same set of two independent variables regardless of scale. Even though ecological requirements of a

species can be described by a different set of factors, this was done to standardise the models structure in order to maintain comparability among scales. For all analyses, we set alpha at 0.05. To avoid strong spatial autocorrelation among variables, no model included the same index more than once, even at different scales. We assessed the accuracy of all models using the Receiver Operating Characteristic curve (ROC, Deleo 1993). From this analysis, it was possible to calculate the area under the ROC function curve (AUC). The AUC is a widely used thresholdindependent measure of overall model accuracy and can be used to compare model strength (Brotons et al. 2004; Graf et al. 2005). For instance, an AUC value of 0.8 indicates that 80% of the time, a random data point with observed bird presence will have an occurrence probability higher than a random point in which birds were absent. With the aim of determining for each species which of the models among all single and multi-scale models could on average perform best, we used the bootstrap procedure (Efron 1979) to calculate the mean model accuracy, explained variance and log-likelihood for all possible scale combinations among the two variables included. The bootstrap procedure consisted of randomly selecting for the models only 60 of the 80 existing data points, repeating this selection 1,000 times with repositions. We were thus able to generate large distributions of AUC, R2 and log-likelihood values for each scale combination. We selected which variable combination would be analysed for each species based on the highest mean R2 values derived from the bootstrap procedure. The resulting AUC, R2 and log-likelihood distributions of the selected singlescale and the best explanatory multi-scale models were compared using single-factor analyses of variance (ANOVA). Between-groups effects were assessed a posteriori through the Tukey post hoc test. All statistical analyses were conducted with the R statistical package (R Development Core Team 2005) using the Hmisc (version 3.0-1) and Design (version 2.0-9) libraries (Harrell 2001).

Results All variables were positively correlated with each other, except for the mean euclidian distance to the

123

912
ENNMN(1,000)

Landscape Ecol (2009) 24:907918

Table 2 Spearman r correlation index and P values between all variables at the four spatial scales (N = 80 for each variable and scale)

The numbers in parentheses indicate the scale (radius, in meters) of each variable. See Table 1 for variable names and codes

* P \ 0.05; ** P \ 0.01; *** P \ 0.001

-.1923ns

ns

.0619ns

-.0549

PD(400)

.1413ns

nearest patch (ENNMN), which was negatively correlated with every other variable regardless of the scale considered (Table 2). Most of the variables were signicantly correlated. Only the correlations of the mean patch area (AREAMN) with ENNMN and of the proportion of forest (PFOREST) and patch density (PD) were in general small (Table 2). Consequently, the models simultaneously contained either AREAMN and ENNMN or PFOREST and PD. According to the results of the bootstrap procedure, the variable combinations with the highest R2 for P. leucoptera and X. fuscus were PFOREST and PD. For C. caudata, the selected models included AREAMN and ENNMN. Among all four indices, the birds incidence patterns were negatively related only to ENNMN. Almost all models were on average signicant (Table 3). In the case of the single-scale models, mean AUC increased with local landscape size for P. leucoptera and X. fuscus, reaching its highest values for local landscapes dened with 1,000- and 800-m radii around the sample points, respectively (Fig. 2). The best single-scale model to predict the incidence of C. caudata was at the 600-m scale (Fig. 2). It is interesting to notice that all mean AUC, R2 and loglikelihood values had consistently low standard deviations (Table 3), indicating low variation and good reliability of models generated from randomly selected data points. The analysis of variance indicated that both AUC and R2 values presented signicant differences between scales within each species. According to the Tukey test, the accuracy (AUC) of all scales was signicantly different for both P. leucoptera and C. caudata. Nevertheless, the 600- and 1,000-m scales of X. fuscus had equal accuracies (Fig. 2) and explained variances (R2). The multi-scalar approach always resulted in signicantly higher model accuracy and explanatory power for all species (P \ 0.01), even when the differences were apparently small. This indicates better general performance of such models compared to the single-scalar models.

-.2993***

-.4199***

-.4981***

-.3361***

-.5041***

-.5516***

-.5319***

-.6242***

-.0219ns

-.0561ns
ns

-.0133ns
ns

ENNMN(800)

-.4532***

-.5473***

-.5806***

-.4457***

-.5243***

-.5909***

-.4544***

-.3400**

-.1406ns

-.1695
ns

-.1190
ns

ENNMN(600)

-.4081***

-.4514***

-.4595***

-.4622***

-.4064***

-.4117***

-.3019**

-.3709**

-.0674ns

-.0428
ns

-.1477
ns

ENNMN(400)

-.3858***

-.3211**

-.2732**

-.3305***

-.3456**

-.3271**

-.2942**

.0136ns

-.2564*

-.0213

-.0561

AREAMN(1,000)

.5244***

.5252***

.4974***

-.1702ns

-.2657*

-.2242*

AREAMN(800)

.6196***

.6063***

.5364***

.4506***

-.4188***

-.4497***

AREAMN(600)

-.4125****

.5708***

.6119***

.5247***

.4632***

AREAMN(400)

.6855***

.5929***

.4766***

.3831***

-.5654***

-.4350***

.0116ns

.1543ns

PD(1,000)

-.122ns

-.1268ns

ns

.1231ns

-.0124

PD(600)

.2113ns

.3498**

.0222ns

PD(800)

ns

.2439*

.1319

.2773*

-.3964***

-.2697*

-.3062**

-.2037ns

-.3160*

-.4267***

-.3579**

-.2426*

.4420

-.1256

ns

-.1675

ns

-.1907

ns

-.0570ns

ns Non signicant

PFOREST(1,000)

AREAMN(400)

PFOREST(400)

(600)

PFOREST(800)

AREAMN

AREAMN

AREAMN

PFOREST

(1,000)

Discussion Our results show that variations of the scale at which the landscape structure of fragmented Atlantic forest is measured seem to be a key factor for the power of

(600)

PD(400)

PD(800)

PD

123

PD

(1,000)

(600)

(800)

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Table 3 Results of the bootstrap procedure with 1,000 replications for each species multiple logistic regressions at all four scales and best explanatory multi-scale model (used scale in parentheses) Species P. leucoptera Scale 400 600 800 1,000 Multi-scale X. fuscus 400 600 800 1,000 Multi-scale C. caudata 400 600 800 1,000 Multi-scale Multivariate models PFOREST PD PFOREST PD PFOREST PD PFOREST PD PFOREST (600) PD (1,000) PFOREST PD PFOREST PD PFOREST PD PFOREST PD PFOREST (400) PD (800) AREAMN ENNMN AREAMN ENNMN AREAMN ENNMN AREAMN ENNMN AREAMN (400) ENNMN (600) b 0.0491 0.008 0.0700 0.031 0.0767 0.012 0.4131 0.250 0.0867 0.016 0.1206 0.051 0.0944 0.018 0.6854 0.410 0.0776 0.012 1.8464 0.449 0.0414 0.013 0.1023 0.030 0.0513 0.017 0.2046 0.051 0.0591 0.02 0.3617 0.080 0.0886 0.029 0.9652 0.582 0.0369 0.012 0.4710 0.082 0.0875 0.117 -0.0123 0.006 0.1030 0.152 -0.0295 0.007 0.1695 0.129 -0.0120 0.004 0.2425 0.142 -0.0104 0.005 0.1621 0.107 -0.0322 0.008 0.854 0.05 0.469 0.09 19.51 4.5*** 0.784 0.04 0.186 0.09 7.26 3.7* 0.758 0.05 0.185 0.08 7.20 3.5* 0.818 0.04 0.418 0.10 17.06 4.7*** 0.675 0.06 0.136 0.08 4.44 2.60 0.841 0.03 0.402 0.06 19.02 3.8*** 0.836 0.03 0.800 0.03 0.383 0.06 0.314 0.06 18.00 3.6*** 14.36 3.5*** 0.800 0.03 0.307 0.06 13.99 3.3*** 0.747 0.04 0.215 0.07 9.45 3.3** 0.831 0.03 0.432 0.06 23.52 4.1*** 0.825 0.03 0.384 0.06 20.47 4.3*** 0.821 0.03 0.388 0.07 20.73 4.3*** 0.815 0.03 0.373 0.06 19.73 3.9*** AUC 0.782 0.03 R2 0.296 0.06 v2 15.10 3.5***

N = 60 for each variable pair and repetition. b mean regression coefcient; AUC, mean model accuracy; R2, mean model variance explained; v2, mean log likelihood test (df = 2 for all regressions). All mean values are presented with standard deviations. See Table 1 for variable names and codes * P \ 0.05; ** P \ 0.01; *** P \ 0.001

incidence models to predict the presence/absence of bird species. The low R2 values (\0.5) presented by the models indicate that other factors not measured here that also inuence bird occurrence might exist. This study, however, did not intend to evaluate the effects of the whole set of environmental aspects that may affect bird incidence, but only of those related to landscape structure at varying scales. The way landscape structure variables measured at different

spatial scales inuenced the model results was unique for each species. This specicity is directly related to the extent to which each of them perceives its environment and arises from its biological characteristics (Levin 1992; Meyer and Thuiller 2006). Furthermore, for all species, multi-scale models performed better than the single-scale ones. Considering only the single-scale models, the best spatial scale to predict the incidence of P. leucoptera

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Fig. 2 Mean model accuracy (AUC) of the single-scale and best multi-scale models, with standard error bars, for each of the species. The dashed lines indicate the highest mean accuracy among each species models. The spatial scale is represented as the radius from the sample points used to dene each round local landscape. N = 1,000 for each scale and species. For each species, different letters above mean plots indicate signicant differences as veried by the Tukey post hoc test

was 1,000 m, for X. fuscus 800 m and for C. caudata one scale lower (600 m). These inter-specic variations may be primarily linked to the range of activity of each species. It is expected that the occurrence patterns of birds that have larger territories should be affected by larger spatial scales than those of birds with smaller area needs (Wiens 1989; Lawler and

Edwards 2002; Thompson and McGarigal 2002; Graf et al. 2005). In fact, other studies within the same region have shown that the mean home-range size of P. leucoptera in fragmented landscapes is approximately 15 ha, about double the size observed for C. caudata (8 ha; Hansbauer et al. 2008). However, the home-range of X. fuscus (for which the better scale was larger than for C. caudata) is approximately 6 ha (Develey 1997), suggesting that factors other than habitat requirements may be inuencing the birds sensitivity to landscape structure at different scales. Functionally, the differences in the best scale may be also related to the birds feeding characteristics. The best scales for both insectivorous species were larger than for C. caudata, which is omnivorous, (Sick 1997; del Hoyo et al. 2003a, b). According to some studies in tropical forests (Davis 1945; Roberts et al. 2000; Develey and Peres 2000), the availability of arthropod resources in the forest may vary considerably in time and space, reducing the feeding resources available to strictly insectivorous birds depending on the season and landscape structure. This would force them to periodically increase their range of activity in search of available food. On the other hand, C. caudata may be less sensitive to landscape structure variations at large scales because it can probably avoid local resource scarcity by shifting between insects and fruits (Snow 1976), reducing the need to wander far in search of resources. However, the effects of landscape structure variation for insectivorous versus omnivorous tropical birds have yet to be tested. Another hypothesis to explain the better performance of larger scales for the two insectivorous birds relates to their foraging strategies. Pyriglena leucoptera is constantly found following ant swarms to feed on eeing small animals (Willis and Oniki 1978; Sick 1997; Gomes et al. 2001; del Hoyo et al. 2003a). Because these are moving resources dispersing over large areas and different habitat types (Roberts et al. 2000), P. leucoptera is probably compelled to follow them, becoming subject to resource availability at larger scales compared to the other species. On the other hand, X. fuscus is common in mixed bird ocks (Goerck 1999; Maldonado-Coelho and Marini 2000; Develey and Peres 2000). Because these bird groups may occupy areas much larger than the mean homerange of X. fuscus, the inuence of landscape structure on its incidence would take place at bigger

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scales. This process may also explain why the incidence of X. fuscus was better predicted by a larger scale compared to C. caudata, even though this last species presents larger home-ranges. In addition to these characteristics, because the forest spatial structure was measured using areas considerably larger than the mean home ranges of the birds, the occurrence patterns found in the present study may also be related to the birds aptitude at moving among habitat remnants and maintaining viable populations in fragmented landscapes. At this level, the persistence of a species depends on local extinction rates and patch accessibility (Hanski 1994; Lindenmayer et al. 1999; Brooker and Brooker 2001; lu et al. 2002). While Bakker et al. 2002; Sekerciog these two factors directly inuence birds incidence patterns, they also arise from distinct ecological processes that might simultaneously happen at different spatial scales. Local extinctions may be inuenced by resource availability, which depends on foraging strategies and small scale internal habitat characteristics (Major et al. 1999; Stratford and Stouffer 1999; Beier et al. 2002). At the same time, patch accessibility is altered by forest connectivity and depends on the species moving abilities and the spatial arrangement of several habitat patches in a larger landscape scale (Taylor et al. 1993; Wiens 1995; Brooker and Brooker 2001; Heinz et al. 2005). The inuence on species survival of several ecological processes happening at different scales is probably the reason why the multi-scale models were more accurate and presented higher explained variance than the best single-scale ones. In the case of the species we studied, variables that are strongly related to the amount of surrounding available habitat, namely PFOREST and AREAMN (Neel et al. 2004), may directly inuence birds chances of nding good feeding and breeding sites at the scale of individual territories. At the same time, isolation (ENNMN) and fragmentation (PD) measures may be more related to general landscape restrictions of bird movements between patches at a larger scale, probably inuencing individual dispersal and patch recolonisation. Evidence of multi-scalar responses to landscape structure has also been found for other tropical species, such as Australian parrots (Manning et al. 2006) and opossums (Lindenmayer 2000). Equally, Thompson and McGarigal (2002) found that the American eagle (Haliaeetus leucocephalus)

chooses its habitat depending on resource selection or environmental disturbance at multiple scales. In the present study, the considerably better performance of the multi-scalar models indicates that single-scale models may not be good enough to properly describe the complex interactions between species ecology and landscape patterns. Because the relationships between bird ecology, population processes and landscape structure might function in a multi-scalar way (Wu 2007), the use of different variables in multiple ecologically relevant scales is a reasonable procedure to optimise the accuracy and explanatory power of bird incidence models. Studies that aim to assess the multiple effects of landscape structure on small tropical passerine birds found in fragmented forests should carefully consider each spatial scale of each variable as potentially relevant and test the use of more than a single scale whenever possible.
Acknowledgments We would like to thank the Helmholtz r UmweltforschungUFZ for institutional support, Institut fu guez, Milton Cezar Ribeiro, Paulo Roland Graf, Carlos Rodr nior and the staff from LEPaC for their assistance de Marco Ju in the data analysis and comments on previous versions of this manuscript, and Milton Cezar Ribeiro for aiding us with the image classications, GIS and Bootstrap procedures. This research was supported by CNPq Conselho Nacional de co e Tecnolo gico, an institution of Desenvolvimento Cient the Brazilian government dedicated to the development of science.

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