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    Effects of structural and functional connectivity and patch size onthe abundance of seven Atlantic Forest bird species

    Alexandre Uezu a , Jean Paul Metzger a, *, Jacques M.E. Vielliard b

    a Departamento de Ecologia, Instituto de Biocie ncias, Universidade de Sao Paulo, Rua do Matao, 321, travessa 14, 05508-900, Sa o Paulo, SP, Brazil b Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, C.P. 6109, 13084-971, Campinas, SP, Brazil

    Received 10 July 2004


    We studied the importance of fragment size and structural and functional connectivity on the occurrence and abundance of sevenAtlantic Forest bird species in 13 patches (13275 ha) and three sites within a continuous forest (10,000 ha). We sampled birds withpoint counts and evaluated structural connectivity considering the presence of corridors and the degree of isolation. We denedfunctional connectivity by analyzing species movements using playbacks in forest corridors between fragments and in the surround-ing matrix. Species differed in their responses to fragmentation. For the frugivorous species, Trogon surrucura , Carpornis cucullatusand Triclaria malachitacea , patch size was the main factor determining abundance. Two understory insectivorous species, Basile-uterus leucoblepharus and Pyriglena leucoptera , were more affected by the degree of patch connectivity, the former by the presenceof corridors and the latter by the distance between patches. The capacity of P. leucoptera to use corridors and open areas (i.e. func-tional connectivity) shaped its abundance pattern. Fragmentation had no effect on the abundance of Chiroxiphia caudata and had apositive effect on Batara cinerea . This study emphasizes the importance of considering species perceptions of landscape, especiallyfunctional connectivity, in understanding the effects of habitat fragmentation.

    2005 Elsevier Ltd. All rights reserved.

    Keywords: Habitat fragmentation; Birds; Corridors; Patch size; Functional connectivity

    1. Introduction

    Connectivity and patch size are important parametersfor the persistence of species in fragmented landscapes(Karr, 1982; Blake and Karr, 1987; Bierregaard andStouffer, 1997; Stratford and Stouffer, 1999; Crooks

    et al., 2000 ). While connectivity is associated with migra-tion rates, and thus with the (re)colonization probabilityand the rescue effect, patch size is mainly related to theprobability of local extinction ( Levins, 1970; Hanski andGilpin, 1997 ).

    Connectivity can be dened as the capacity of thelandscape to facilitate biological uxes ( Taylor et al.,1993; Tischendorf and Fahrig, 2000 ). In structuralterms, it can be evaluated by measuring landscape pat-terns, such as density and complexity of corridors ( Beierand Noss, 1998 ), distance between patches, and inter-

    habitat matrix permeability ( Metzger and De camps,1997; Gascon et al., 1999; Antongiovanni and Metzger,2005 ). Functional connectivity is more complex. It de-pends not only on the landscape pattern, but also onthe interactions between this pattern and the biologicalcharacteristics of the target species, such as their abilityto move in areas of non-habitat ( Greenberg, 1989; Siev-ing et al., 1996 ). For example, understory insectivorousbirds, which are able to use more intensively deforestedcountryside, are less affected by fragmentation and have

    0006-3207/$ - see front matter 2005 Elsevier Ltd. All rights reserved.doi:10.1016/j.biocon.2005.01.001

    * Corresponding author. Tel.: +55 11 30917564; fax: +55 1138134151.

    E-mail addresses: [email protected] (A. Uezu), jpm@ib.usp.br (J.P.Metzger), [email protected] (J.M.E. Vielliard).


    Biological Conservation 123 (2005) 507519


    mailto:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]
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    lower extinction risk ( Sekercioglu et al., 2002 ). Interestin how species use different landscape elements to dis-perse is increasing ( Tischendorf and Fahrig, 2000; Gra-ham, 2001; Belisle and Desrochers, 2002; Adriaensenet al., 2003 ) as it is linked with the probability of an indi-vidual nding patches of habitat that are spread across

    the landscape and, therefore, is related with speciescapacity to persist in such environments.In the present study, we evaluated the abundance of

    seven Atlantic rainforest bird species in relation to patchsize and connectivity, considering not only structuralcharacteristics of the landscape but also movementbehavior of species.

    The Brazilian Atlantic rainforest has one of the high-est levels of biodiversity and rates of endemism in theworld, and is among the world s top ve threatened hot-spots ( Myers et al., 2000; Mittermeier et al., 1999 ). De-spite strict environmental legislation, today less than 8%of the forest remains and deforestation persists ( Dean,1996; Fundacao SOS Mata Atla ntica/INPE, 2002 ).

    Due to habitat loss and the consequent fragmentation,populations are becoming isolated in small forestpatches and many species, especially endemics ( Ribonet al., 2003 ), are locally disappearing. For example, theAtlantic Forest has 188 endemic bird species ( Pachecoand Bauer, 2000 ) and among them 102 are considered

    threatened ( Pacheco and Bauer, 2000 ; IUCN, 2003 ).There is a growing literature concerning the effects of deforestation and fragmentation on bird communities inthis biome ( Willis, 1979; Aleixo and Vielliard, 1995;Christiensen and Pitter, 1997; Anjos and Bocon, 1999;Brooks et al., 1999a; Maldonado-Coelho and Marini,2000; Ribon et al., 2003 ), but few authors have consid-ered aspects of connectivity. Since the response to frag-mentation depends on the interaction between spatialcharacteristics of the landscape and the species behavior(Tischendorf and Fahrig, 2000 ), we analyzed connectiv-ity in structural and functional terms. Structurally, weconsidered the presence or absence of connections (cor-ridors) between small and larger patches in the land-

    Fig. 1. Location of the study region in Sao Paulo State, Brazil. The more detai led map shows the continuous forest (Morro Grande Reserve) and theadjacent fragmented landscape, with the 16 study sites (patch codes and spatial characteristics in Table 1 ).

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    scape as well as the distance between patches. In func-tional terms, we measured the species capacity to usecorridors and to cross open areas of the matrix. We con-sidered only strict forest species because, by denition,they are more sensitive to forest fragmentation. Anunderstanding of the mechanisms that maintain these

    species in fragmented landscapes will likely have appli-cations to other less demanding species ( Lambeck,1997; Simberloff, 1998 ).

    2. Methods

    2.1. Study region

    The study region is situated in the Plateau of Ibiu na,a Pre-Cambrian formation situated 40 km from the cityof Sao Paulo (23 35 0S23 50 0S; 46 45 0W47 15 0W; Fig.1). The elevation ranges from 870 to 1030 m, and thetopography is dominated by small round hills ( Poncanoet al., 1981 ). The weather is warm and humid, with meanmonthly temperature varying between 11 and 27 C.The annual precipitation is about 13001400 mm withseasonal variation, April to August being cooler and

    drier. The vegetation is classied as Lower MontaneRainforest ( Oliveira-Filho and Fontes, 2000 ). Floristicsurveys in the region showed a high tree richness (362species in the region with diameter at breast height>5 cm), with a dominance of Myrtaceae (79 species),Lauraceae (38) and Fabaceae (31) ( Bernacci et al.,

    2004 ).The region has well-preserved forest within the Mor-ro Grande Reserve ( 10,000 ha), with an adjacent rurallandscape where the forest occurs in patches and corri-dors ( Fig. 1 ). Both the Morro Grande Forest Reserveand the rural landscape have similar geologic, geomor-phologic, climatic and vegetational conditions, whichmake them suitable for comparison. In the fragmentedarea, the matrix is composed mainly of open areas (suchas horticultural crops, fallow elds, pastures and pioneervegetation; 60% of the matrix), rural installations andhouses (17%) and Eucalyptus and Pinus plantations(11%). Widespread deforestation began in the 19th cen-tury, and was particularly intense during World War II(Seabra, 1971 ). The entire study area, including theMorro Grande Reserve, is composed of intermediateto old second-growth forest reestablished after loggingand burning that occurred 5080 years ago ( Seabra,

    Fig. 2. Location of playback points used to test the functional connectivity of small fragments (Ibiu na Plateau, Southeastern Brazil). Points werechosen in corridors linking small connected patches (c) to large patches (L) to test the use of those corridors. Points were also placed around smallisolated patches (i) to test possible functional connection with adjacent large patches. Light gray corresponds to young secondary forests (56 mcanopy height) and dark gray to late and intermediate secondary forests (1520 m canopy height). Dashed lines represent the most likely routes forbird movement between small isolated and large patches.

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    1971 ). At present, approximately 31% of the fragmentedlandscape is composed of intermediate/old secondgrowth forest and 6% of young secondary forest (ca.10 years-old forest, 56 m high) ( Fig. 2 ). Most patchesare relatively small (212 ha) because of the small aver-age lot size (

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    patches with four points, a period that would corre-spond to a fth point was randomly chosen. During thistime we did not make any observations.

    The survey included 546 point counts considered asindependent samples: 28 for the two smallest patchesand 35 for each of the other fourteen sites. The sampling

    period began a few minutes before dawn and endedapproximately 4 h later. Observations were undertakenfor 20 min at each point. During each visit, the sequenceof the survey was randomly chosen to avoid non-inde-pendence of time and sampling points. For each species,a punctual abundance index (PAI) was calculated foreach site where the number of contacts, visual and/orauditory, was divided by the number of sampled pointcounts.

    2.4.2. Playback techniqueWe surveyed the areas surrounding the small patches

    to test the effectiveness of corridors and degree of patchisolation on each species studied ( Fig. 2 ). Playback tech-nique was used to increase individual detection by repro-ducing the pre-recorded species-specic vocalizations toinduce a response ( Vielliard, 1989; Parker, 1991 ). Allspecies studied here are territorial, so they typically re-spond very well to playback. The effectiveness of theplayback technique has previously been veried for thespecies considered here ( Boscolo, 2002 ). This techniqueefficiently detected the presence of a species when itsabundance was not too low (PAI > 0.05), and after threevisits we have a condence of 95% to conrm speciespresence.

    We played the bird songs in pre-determined points inthe corridors that links the small connected patches tothe larger forests and around the small isolated frag-ments as well ( Fig. 2 ). For the latter, we assumed themost likely routes used by birds to reach nearby largepatches to be the shortest distance through open areas(see routes in Fig. 2 ) and placed the playback pointsalong these lines. The number of points depended onthe length of the corridor and on the context (varietyof routes) where isolated fragments were situated. Thetest was done during October 2002, from 6:00 to 8:00and from 11:00 to 13:00. This was considered as the bestperiod of the year and time of day to detect the selectedspecies using this method ( Boscolo, 2002 ). To reach 95%condence in our results, each point was surveyed atleast three times when the species were not detected. If all species were detected in a point before three visits,then the survey was stopped. At each point, the vocali-zation of each species was played continuously for oneminute and followed by a 30-s listening interval. Thisprocedure was repeated three times for each species.The sequence of species at each point was determinedrandomly.

    We considered the presence of a species in a corridorto indicate that such a connection facilitates dispersal T

    a b l e 2

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    and thus gene ow. This assumption can be partlywrong if the territory of an individual in the corridorcan obstruct the movement of conspecics ( Soule andGilpin, 1991 ). However, even if there is no gene owat a specic time, we assume that the existence of a con-nection between territories should facilitate, through

    successive generations, gene ow between patches, andfor this reason the patches should be considered func-tionally connected.

    Similarly, we considered that the lack of response(after three playback sessions) at a chosen point on theline between an isolated and a large patch indicates thatthis particular species does not use this route to movebetween those patches. Playback stimulation aroundisolated patches was mainly focused in open matrix,which represents most of the landscape around studypatches. We did not control for the differences betweenopen matrix types (e.g. agricultural or pasture areas),because we assumed that they have the same effect onbird movement, since they are predominantly composedof herbaceous species. Except for urban areas, the openmatrix should be the most signicant impediment to for-est bird movement. Movement through urban areas wasnot considered because those areas represent less than7% of the matrix and rarely occur surrounding studypatches. However, we considered bird movementthrough young secondary forests because these canpotentially connect isolated patches due to a higher for-est structural similarity with intermediate/late secondaryforests. Although the non-detection of a species in thematrix does not mean that it does not move through

    it, this information gives a rough idea of the matrix per-meability for these species. When an individual was ob-served to cross open areas from a structurally isolatedpatch to a large patch, the former was considered func-tionally connected for this species.

    We thus used playback technique data to reclassifythe small patches. If no birds were observed using a cor-ridor that connects a small patch to a large one, the for-mer was considered functionally isolated for therespective species. Conversely, if individuals of a specieswere conrmed to leave a structurally isolated forest andreach a large one, the patch was considered functionallyconnected for this species.

    2.5. Quantitative analysis of landscape

    We selected two independent measures for the quan-titative landscape analysis: patch size (AREA), exclud-ing areas with less than 100 m in length (corridors);and the mean nearest neighbor (MNN). The latter indexis the mean distance of patches to their respective near-est neighbor. We considered all patches totally or par-tially inside a radius of 1 km from the center of thestudied patch. MNN was measured based on the short-est Euclidean edge-to-edge distance between fragments.

    Using a 1 km radius that includes the areas that arelikely to strongly inuence the presence of the study spe-cies, since most have territories of about 510 ha ( Deve-ley, 1997 ) and low dispersal capacity (Results). Largerradii would lead to a large overlap (>50%) among theradii of different patches. The metrics were calculated

    in ArcView 3.2 using the Patch Analyst 2.0 exten-sion ( Elkie et al., 1999 ).

    2.6. Data analysis

    Categorical (size class and connectivity) and continu-ous data (landscape indices) were used to relate birdabundance and landscape parameters. We used analysisof variance (ANOVA) and the t test (Zar, 1996 ) to testfor differences between abundances considering patchsize classes and the presence of structural or functionalconnections. We undertook four tests for each species:Morro Grande (forest landscape, n = 3) vs. patches(fragmented landscape, n = 13); large patches ( n = 5)vs. small patches ( n = 8); structurally connected patches(n = 4) vs. structurally isolated patches ( n = 4); function-ally connected patches vs. functionally isolated patches.In instances where species abundance did not satisfyANOVA or t test assumptions, we used the respectiveequivalents non-parametric analyses, KruskalWallisand MannWhitney. For signicant results (i.e. p < 0.05), we applied an a posteriori test to identifywhich variables accounted for signicant differences.We applied the Scheffe s test for parametric analysesand the Dunn s test ( Zar, 1996 ) for non-parametric tests.

    For the continuous data, we used regressions with birdabundances and landscape indices. The AREA indexwas log (base 10) transformed to present normal distri-bution characteristics. We used Statistica 5.01 for allanalyses.

    3. Results

    3.1. Landscape structure

    Mean nearest neighbor (MNN) values ranged from30 to 90 m, with an average of 54 m ( Table 1 ). Fragmentsize (log transformed) and isolation were uncorrelated(Pearson, r = 0.027, p = 0.930), which allowed theevaluation of the effect of these indices with bird abun-dances independently.

    3.2. Sensitivity to landscape structure

    The species showed varying patterns of abundance,indicating different degrees of sensitivity to fragmenta-tion ( Table 3 ). The comparison between forest andfragmented landscapes revealed that T. malachitaceaand C. cucullatus were the most sensitive to alterations

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    in forest cover, since they were present only in the for-est landscape ( Table 3 ). Even inside the Reserve, theywere restricted to a limited number of sites. Trogonsurrucura occurred in both landscapes, but was moreabundant in the Reserve than in the forest patches(Table 4 ). Conversely, B. cinerea was more abundant

    in the fragmented landscape than in the Reserve(Table 4 ).Within forest patches, T. surrucura was particularly

    sensitive to habitat loss ( Table 4 ). It showed a positiveand signicant correlation to patch size ( Table 5 ).Basileuterus leucoblepharus and P. leucoptera were bothsensitive to structural parameters of landscape connec-tivity. However, the former was signicantly more abun-dant in small connected patches than in small isolatedforests ( Table 4 ), while P. leucoptera was less abundantas the mean distance between patches increased ( Table5). Chiroxiphia caudata seems to be unaffected by anyof the landscape parameters considered in this study(Table 4 ).

    3.3. Structural vs. functional connectivity

    Using the playback protocol we observed 157 indi-viduals. Of these, 95 were using corridors (44 B. leu-coblepharus , 22 C. caudata , 15 B. cinerea , 14 P.leucoptera ). We also noted 24 individuals crossing

    open areas (eight P. leucoptera , six C. caudata , fourB. leucoblepharus , four B. cinerea and one T. surru-cura ). These open areas varied from a small road(10 m length) to gaps of up to 130 m. We veried thatindividuals crossed through open areas towards otherforest patches. If we played recorded songs in a direc-tion where there was no forest, the individual couldeventually travel some meters from the forest, butthen went back to its original place.

    Observations in corridors and around small isolatedpatches yielded qualitative data about the use of theselandscape elements, providing indicators of functionalconnectivity foreach species ( Table 6 ). With theexceptionof T. surrucura , all species observed in the fragmented

    Table 4Signicance values for analyses of variance when comparing the abundance obtained with point counts of ve species considering habitat loss andfragmentation (patches vs. reserve), fragment size (large vs. small), and structural and functional connectivity (isolated vs. connected) treatments(Ibiuna Plateau, Southeastern Brazil)

    Patches vs. reserve Large vs. small Connected vs. isolated structural Connected vs. isolated functional

    n 16 13 8 8df 1, 14 1, 11 1, 6 1, 6Trogon surrucura a 0.041 ( )

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    area appear to use corridors as habitat( Table 6 ). This wasparticularly apparent in circumstances where the corridorwas characterized by intermediate or old successionalvegetation. These species were also able to use young sec-ondary forest and cross open areas varying from 60 to130 m ( Table 6 ). Batara cinerea was normally associatedwithintermediate/oldforestareasandwas found in youngsecondary forest only when crossing from one patch toanother as a result of the playback stimulation. In only

    one occasion was a T. surrucura individual observed tocross an open area, a small road approximately 10 mlength. Omitting T. surrucura , the average maximum dis-tance that individuals of all species traveled in open areasis greater than the mean distance between patches (54 m,Table 1 ). This suggests that most patches are effectivelyconnected for these species.

    The surveys around isolated patches and in corridorssuggest that structural connection is not always indica-tive of functional connectivity for some species ( Table7). Thus, although forests S1, S2, S3 and S4 are structur-ally isolated ( Table 7 ), S2 (14.1 ha) is not functionallyisolated for B. leucoblepharus , B. cinerea and C. caudatasince we observed individuals of those species movingbetween this patch and other forest areas that were mid-way to patch L1 (52.1 ha; Fig. 2 ). We did not observethese species crossing from the other isolated patches(S1, S3 and S4) to large forest areas. Similarly, we didnot observe P. leucoptera in the corridor between S8and L3 ( Table 7 ), although it was seen in corridors be-tween other structurally connected areas ( Table 7 ).

    The redenition of patch category concerning func-tional connectivity was especially important for P. leu-coptera . The new t test, considering the S8 patch asisolated, resulted in a signicant difference ( t = 3.33;

    p = 0.016; Table 4 ). Species abundance was higher inthe connected patches, although this difference was notdetected when using the structural denition for connec-tivity ( Table 4 ).

    4. Discussion

    4.1. Importance of area

    The species in this study showed different degrees of sensitivity to habitat area and connectivity, supportingprevious ndings with birds and other taxonomicgroups ( Willis, 1979; Laurance, 1991; Newmark, 1991;Pearson, 1993; Andre n, 1994; Stouffer and Bierregaard,1995; Jokimaki and Huhta, 1996 ). Patch size was partic-ularly important to large canopy frugivorous species.This is not surprising as they probably have a large arearequirement due to high energetic demand and to thespatial and temporal variation of their food resources(Goerck, 1997 ). Although it is not a consensus amongauthors that higher body size increases vulnerability(Gaston and Blackburn, 1996; Henle et al., 2004 ), itseems that such a correlation does exist for frugivorousbirds ( Willis, 1979; Kattan, 1994; Christiensen and Pit-ter, 1997; Renjinfo, 1999; Castelletta et al., 2000 ). Thusthe three most sensitive species in this study, T. malachit-acea , C. cucullatus and T. surrucura , belong to this guild.Although we found no data in the literature concerninghabitat requirements, these species may need large terri-tories to secure sufficient food during the entire year.For example, a study of other Trogon species in theAmazon Rainforest suggests they need territories, onaverage, of 8.5 ha ( Terborgh et al., 1990 ).

    Table 6Capacity to use corridors and young secondary forests, and to cross open areas of the ve species observed in the fragmented landscape (Ibiu naPlateau, Southeastern Brazil)

    Use of corridors Use of young secondary forests Capacity to cross open areas with playback stimulation (m)

    Trogon surrucura No No 10Basileuterus leucoblepharus Yes Spontaneous 100Pyriglena leucoptera Yes Spontaneous 60Chiroxiphia caudata Yes Spontaneous 130

    Batara cinerea Yes With stimulation 60

    Table 5Simple linear regression ( n = 13, df = 1, 11) of species abundance with patch size (AREA) and with isolation (MNN), considering only data from thefragmented landscape (Ibiuna Plateau, Southeastern Brazil)

    Log (AREA) MNN

    R2 p R2 p

    Trogon surrucura 0.817

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    Rarity (low abundance within a habitat) also has astrong relationship with extinction susceptibility ( Leck,1979; Diamond et al., 1987; Laurance, 1990; Newmark,1991; Goerck, 1997; Manne and Pimm, 2001 ). Triclariamalachitacea is naturally rare ( Stotz et al., 1996 ) and isconsidered sensitive to even small habitat alterations(Magalhaes, 1999 ). We found this species in only twoareas inside the forest reserve, possibly due to the heter-ogeneity of forest structure. The degree of endemism,naturally low abundance and high sensitivity to habitatreduction are probably responsible for the status of thisspecies as globally threatened ( IUCN, 2003 ). The speciesmay also suffer from pet trade traffic (as do other Psit-tacidae), particularly in the fragmented region wheretheir habitat substantially interfaces with human activi-ties. However, we do not have any evidence of this activ-

    ity in the region. Alternatively, the low abundance of C.cucullatus might be related to the low forest quality inthe region, which was substantially altered during thepast 50 years. The species is common in other localitieswhere habitat is well preserved ( Ho ing and Lencioni,1992 ).

    Trogon surrucura is also highly sensitive to habitatloss, although it is not as vulnerable as the previoustwo species. It was more often observed in largerpatches, conrming results from previous studies ( Willis,1979; Christiensen and Pitter, 1997; Anjos and Bocon,1999; Marini, 2001 ). Although, there is no consensusabout the minimum patch size needed by the species,we obtained a similar result (12 ha) to that found by An- jos and Bocon (1999, 19.6 ha) . Note however that someauthors have found T. surrucura only in patches largerthan 63 ha ( Willis, 1979; Christiensen and Pitter, 1997;Marini, 2001 ). This may be due to differing conditionsin the spatial structure of the landscapes. Thus the spe-cies may be able to survive in smaller fragments if theyare part of a well-connected landscape. Our data alsoconrm previous observations that this species activelyrisks crossing open areas ( Magalhaes, 1999 ). For in-stance, we observed T. surrucura crossing open areasto feed in isolated fruit trees. Thus, although there is evi-

    dence that large patches are essential for the mainte-nance of this species, our results suggest that smallerpatches may also maintain this species. It seems to useseveral patches to nd resources, but visits largerpatches more frequently, possibly because of the greaterquantity of resources. Price et al. (1999) found a similarpattern for frugivorous birds in the tropical forests of Australia.

    Batara cinerea seems to benet from fragmentation atour study site since it was more abundant in patchesthan in the Reserve. These results run opposite to otherobservations that classify this species as sensitive to hab-itat alteration ( Stotz et al., 1996; Aleixo and Vielliard,1995; Anjos and Bocon, 1999 ). Although it is a relativelylarge and territorial species, qualities that theoreticallyshould make it more demanding in habitat selection

    (Terborgh, 1974; Leck, 1979 ), fragmentation did not ap-pear to negatively affect B. cinerea . Its capacity to crossopen areas ( Willis, 1979 ) may minimize the impact of forest reduction, allowing it to use resources from othernearby areas ( Rolstad, 1991 ). Batara cinerea was ob-served crossing open areas of up to 60 m. This may al-low individuals to explore many patches in alandscape such as Caucaia, where the mean distance be-tween patches is small (54 m). Moreover, the speciesdoes not seem to be restricted by vegetation quality asit was frequently seen at forest edges. Perhaps the spe-cies suffers negative effects from fragmentation in caseswhere the mean distance between patches is substan-tially larger than the one in Caucaia, as it was seen byother researchers ( Aleixo and Vielliard, 1995; Anjosand Bocon, 1999 ).

    Thus T. surrucura and B. cinerea respond differentlyto fragmentation, besides their large body size and thushigh energy demand. While T. surrucura is concentratedmainly in large patches, B. cinerea had a reasonablyeven distribution among all patches. This difference sug-gests that the dispersal capacity of T. surrucura is prob-ably attenuated through non-forest areas. Therefore, itmay be more dependent on local resources and more re-stricted to patches where it already occurs in comparison

    Table 7Classication of small patches according to structural and functional connectivity for the four species observed in these patches (Ibiu na Plateau,Southeastern Brazil)

    Study patches Structural connectivity Functional connectivity

    Basileuterus leucoblepharus Pyriglena leucoptera Chiroxiphia caudata Batara cinerea

    S1 I I I I I

    S2 I C I C CS3 I I I I IS4 I I I I IS5 C I C C CS6 C C C C CS7 C C C C CS8 C C I C C

    C, connected to a large patch (>50 ha); I, isolated from large patches.

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    to B. cinerea , which could search for resources in morethan one fragment.

    4.2. Structural and functional connectivity

    The species studied show distinct responses to

    structural connectivity. The distance between patchesis an important parameter accounting for the varia-tion in P. leucoptera abundance. However, sincepatches were relatively close to each other, the 60 mdispersion capacity demonstrated by this species is suf-cient to the species to effectively disperse betweenmost patches. From the perspective of P. leucoptera ,most patches are probably linked. However, the re-sults also suggest that this parameter varies amongthe habitat patches surrounding each studied area ina 1 km radius, and that such a factor is related withP. leucoptera abundance. Thus, besides the capacityof the species to cross open areas, this movementmay be less frequent as the distance between patch in-creases. Similar results were observed with a toucanspecies ( Ramphastos sulfuratus ) in Southern Mexico,where individual movement between habitat patcheswas positively correlated with distance between them(Graham, 2001 ). Although for P. leucoptera functionalconnectivity is better dened when we consider itscapacity to cross open areas, corridors may play amore important role for connecting local populationsas the distances between patches increase.

    Structural connections seems to be relevant only forB. leucoblepharus , an understory insectivorous species

    that forages near the ground, prefers humid areas andavoids open areas ( Silva, 1991 ). These peculiaritiesshould make it more averse to cross open areas. Thus,we expected it to use corridors more frequently thanthe other species to move from one patch to another.However, the use of corridors seems not to be relatedto a low capacity to cross open areas or to use youngsecondary forests, since B. leucoblepharus showed simi-lar characteristics as P. leucoptera and C. caudata .Moreover, the use of corridors is neither related to thecapacity to use forest edge habitats (which characterizethe corridors) since most of the contact with the speciesin point counts occurred in patch cores (i.e. >50 m fromthe forest edges).

    The option to cross longer distance using corridors orundertake shorter movements through the matrix is atleast partly related to the energetic cost of moving andthe risk of predation/mortality ( Tischendorf and Fahrig,2000 ). Studies have demonstrated that some bird speciesopt for the longer route (i.e. going around the forest)and only when the ratio between the distance throughthe forest and through the open area is high, they preferthe shorter option ( Belisle and Desrochers, 2002 ). Thecapacity to cross non-habitat areas is also intrinsicallyrelated to species characteristics such as: body size lar-

    ger species tend to have a lower predation risk ( Belisleand Desrochers, 2002 ); degrees of demand for specichabitats generalists are less averse to open areas(Greenberg, 1989 ); and behavior - some species movefaster through areas of non-habitat and thus reduce pre-dation risk ( Sieving et al., 1996 ). Nonetheless, our re-

    sults suggest that it is difficult to dene whichbiological characteristics predispose a species to use cor-ridors or to cross an open matrix. Thus, although B. leu-coblepharus and P. leucoptera have distinct responses tolandscape structure, they show many similar biologicalcharacteristics. Both are small understory insectivores,are able to cross open areas and can use young forests.We did not detect any characteristic that produced a dif-ferent perception of landscape elements for these twospecies. Such perception might reect ancestral differ-ences and/or may be due to some behavioral character-istics. For example, P. leucoptera developed aspecialization to forage following ants and thus abun-dance of this resource might reect in its capacity to sur-vive in habitat patches or to use corridors.

    For B. cinerea and C. caudata , neither parameter of structural connectivity seems to explain variation inabundance. The distance between patches is probablyinsufficient to impact abundance and does not corre-spond to a signicantly elevated cost of dispersion forthese species. In this situation, all patches are function-ally connected and species distribution and abundanceare probably more associated with local factors, suchas resource availability.

    4.3. Conservation implications

    Although fragmented landscapes support a propor-tion of bird community, local extinctions occur whenthere is intense fragmentation ( Ribon et al., 2003; Deve-ley and Metzger, 2005 ). Triclaria malachitacea and C.cucullatus illustrate the importance of continuous areas,such as the Morro Grande Reserve, for the maintenanceof a complete bird community. These two area demand-ing species might be considered umbrella-species poten-tially useful in dening appropriate Atlantic rainforestconservation areas for similarly sensitive birds.

    Although this biome has been substantially dimin-ished, the time lag between forest loss and extinction(Brooks and Balmford, 1996; Brooks et al., 1999b )and the distribution patterns of the remnant fragmentsmay explain the lack of signicant mass extinctions.The remaining forest areas tend to be comprised of largefragments (e.g. Morro Grande) surrounded by manysmaller patches. Species loss could have been substan-tially higher if the fragmentation had been morehomogeneous.

    The larger patches (>60 ha) were extremely impor-tant, guaranteeing the presence of demanding species,such as T. surrucura , in this fragmented landscape. Con-

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    sequently, their conservation should be a priority, par-ticularly since many other species have a similar pattern.This results is also important in the larger Atlantic Rain-forest context, because many remnants of this biome aresmaller than 30 ha.

    Our results suggest that the distance between patches

    is also an important consideration since shorter inter-patch distances facilitate biological uxes through thelandscape and thus promote species maintenance. Thus,small patches may act as stepping-stones for dispersionbetween larger patches. For this reason, landscape man-agement should also incorporate additional elementssuch as small patches, corridors and different types of matrices (e.g. young secondary forest).

    Our study suggests that the response to habitat alter-ation and fragmentation is species-specic. Some taxawere more affected by fragment size, while others byconnectivity. The limited dispersal capacity of under-story insectivorous birds, for example, may be a key fac-tor determining their sensitivity to fragmentation(Sekercioglu et al., 2002 ). With respect to connectivity,some species may be more sensitive to inter-patch dis-tance, whereas others are more sensitive to the presenceof corridors. These different perceptions are particularlyrelevant since they can elucidate which landscape com-ponents play major roles for each species. Functionalconnectivity is thus a key property to dene functionalspecies groups in the context of fragmentation, which al-low us to make generalizations about its effects. Conser-vation may be more effective if we consider theperception and demands of these different functional



    We thank Clinton Jenkins, Pedro Develey, AlexandreMartensen, and Pedro M. Pedro for revising a previousversion of the manuscript. We are also grateful to DenisSaunders, Cagan Sekercioglu, and an anonymous re-viewer for their detail analysis and efficiency throughoutthe review process. We appreciate the cooperation dur-ing all the steps of this study of members of the projectBiodiversity conservation in fragmented landscapes atthe Atlantic Plateau of S ao Paulo . We thank SABESP,which allowed us access to the Morro Grande Reserveand also all private owners of the properties containingpatches. Without their agreement this study could nothave been undertaken. Financial support was providedby FAPESP (99/05123-4; 00/01120-0).


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