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Sensitivity to fragmentation and spatial distribution of birds in forest fragments of northern paraná

Sensibilidade è fragmentação e distribuição espacial de aves em fragmentos florestais do norte do Paraná

Abstracts

In this study we investigated the relationship between the sensitivity to forest fragmentation of bird species and their habitat spatial distribution. We hypothesized that a homogenous spatial distribution is associated to habitat-generalist species, which would tend to be less sensitive to forest fragmentation; in contrast, a heterogeneous spatial distribution would drive to an increase of sensitivity to forest fragmentation. We concentrated on analyses of the suboscine birds, which are known to be closely associated to microhabitats. Field data was obtained in the Parque Estadual Mata dos Godoy (23°27′ S, 51°15′ W), southern Brazilian Atlantic forest. This reserve has high Biotic Integrity levels, with a relatively high number of recorded suboscines. Forty three species of suboscines were recorded, of which 21 species were considered to have high sensitivity and 22 to have low sensitivity to forest fragmentation. There was no association between levels of sensitivity to forest fragmentation and spatial distribution of suboscines. We only found significant correlation with the group of the subcanopy suboscines at the northern portion of Parque Estadual Mata dos Godoy. Therefore, we found a weak relationship between spatial distribution (habitat specialization) and sensitivity to forest fragmentation. The fact that habitat-specialist birds tend to live at the northern portion of Godoy State Park, which has the first type of terrain in a landscape to be converted into agriculture, indicate that that region has special importance for conservation.

microhabitat; habitat-specialization; suboscine birds


Neste estudo nós investigamos as relações entre sensibilidade è fragmentação florestal de aves e sua distribuição espacial no habitat. Nossa hipótese é que a distribuição espacial homogênea está associada a espécies habitat-generalistas, que tenderiam a ser menos sensíveis è fragmentação florestal, em contrapartida, uma distribuição espacial heterogênea seria resultado de uma maior sensibilidade è fragmentação florestal. As análises foram concentradas em aves suboscines por serem intimamente associada a microhabitats. Dados amostrais foram obtidos no Parque Estadual Mata dos Godoy (23°27′ S, 51°15′ W), sul da Mata Atlântica brasileira. Esta reserva apresenta alto ĺndice de Integridade Biótica, com um número relativamente elevado de aves suboscines. Quarenta e três espécies de aves suboscines foram registradas, sendo 21 espécies consideradas de alta sensibilidade e 22 de baixa sensibilidade è fragmentação florestal. Não houve associação entre os níveis de sensibilidade è fragmentação florestal e a distribuição espacial de aves suboscines. Só foi observada significância para as aves de sub-bosque da porção norte do Parque Estadual Mata dos Godoy. Portanto, encontramos uma fraca relação entre especialização de habitat e sensibilidade è fragmentação florestal. O fato destas aves habitat-especialistas tenderem a viver na porção norte do Parque Estadual Mata dos Godoy, que é o primeiro tipo de terreno a ser convertido para a agricultura em uma paisagem, indicam que essa região tem uma importância especial para a conservação.

aves suboscines; habitat-especialistas; microhabitat


Introduction

Forest fragmentation has been considered a major force in decreasing local biodiversity (e.g. Gardner et al. 2009GARDNER, T.A., BARLOW, J., CHAZDON, R.L., EWERS, R.M., HARVEY, C.A., PERES, C.A. & SODHI, N.S. 2009. Prospects for tropical forest biodiversity in a human-modified world. Ecol. Lett. 12(6):561-582. 10.1111/j.1461-0248.2009.01294.x.
https://doi.org/10.1111/j.1461-0248.2009...
, Laurance 2010LAURANCE, W.F. 2010. Understanding habitat fragmentation in the real world. In The Theory of Island Biogeography Revisited. (Losos, J.B. & Ricklefs, R.E. eds). Princeton University Press, New Jersey.). However, fragmentation does not act homogeneously on different species. In birds, several features have been identified as closely related to species that are more sensitive, such as population size, reproductive performance, annual survival, trophic position, rarity, and biogeographic position (e.g. Henle et al. 2004HENLE, K., DAVIES, K.F., KLEYER, M., MARGULES, C. & SETTELE, J. 2004. Predictors of species sensitivity to fragmentation. Bio. Divers. Conserv. 13:207-251. 10.1023/B:BIOC.0000004319.91643.9e.
https://doi.org/10.1023/B:BIOC.000000431...
, Anjos 2006ANJOS, L. 2006. Bird species sensitivity in a fragmented landscape of the Atlantic Forest Southern Brazil. Biotropica 32(2):229-234. 10.1111/j.1744-7429.2006.00122.x.
https://doi.org/10.1111/j.1744-7429.2006...
, Devictor et al. 2010DEVICTOR, V., CLAVEL, J., JULLIARD, R., LAVERGNE, S., MOUILLOT, D., THUILLER, W., VENAIL, P., VILLEGER, S. & MOUQUET, N. 2010. Defining and measuring ecological specialization. J. Appl. Ecol. 47(1):15-25. 10.1111/j.1365-2664.2009.01744.x.
https://doi.org/10.1111/j.1365-2664.2009...
). Another feature pointed out by Henle et al. (2004)HENLE, K., DAVIES, K.F., KLEYER, M., MARGULES, C. & SETTELE, J. 2004. Predictors of species sensitivity to fragmentation. Bio. Divers. Conserv. 13:207-251. 10.1023/B:BIOC.0000004319.91643.9e.
https://doi.org/10.1023/B:BIOC.000000431...
associating sensitivity of bird species to forest fragmentation is habitat specialization. Species that are more habitat-specialists tend to be locally extinct where forests are fragmented (Ribon et al. 2003RIBON, R., SIMON, J.E. & MATTOS, G.T. 2003. Bird extinctions in Atlantic forest fragments of Viçosa region, southeastern Brazil. Conserv. Biol. 17(6):1827-1839. 10.1111/j.1523-1739.2003.00377.x.
https://doi.org/10.1111/j.1523-1739.2003...
, Henle et al. 2004HENLE, K., DAVIES, K.F., KLEYER, M., MARGULES, C. & SETTELE, J. 2004. Predictors of species sensitivity to fragmentation. Bio. Divers. Conserv. 13:207-251. 10.1023/B:BIOC.0000004319.91643.9e.
https://doi.org/10.1023/B:BIOC.000000431...
).

Variations in vegetation features, such as vertical and horizontal segregation associated with variations in floristic composition, increase diversity of microhabitats, which in turn drives to a mosaic of resources for the species, even in a continuous forest (Karr 1990KARR,JR. 1990. Interactions between forest birds and their habitats: A comparative synthesis. In Biogeography and ecology of forest bird communities. ( Keast, A. ed). SPB Academic Publishing. Ann Arbor.). This structural complexity entails, for example, greater diversity of foraging substrates, as occurs in certain groups of birds, like the Furnariidae and Tyrannidae families (e.g. Remsen 2003REMSEN, JR.J.V. 2003. Family Furnariidae (Ovenbirds). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions, Barcelona, v.8, p. 162-357., Fitzpatrick et al. 2004FITZPATRICK, J., BATES, J., BOSTWICK, K., CABALLERO, I., CLOCK, B., FARNSWORTH, A., HOSNER, P., JOSEPH, L., LANGHAM, G., LEBBIN, D., MOBLEY, J., ROBBINS, M., SCHOLES, E., TELLO, J., WALTHER, B. & ZIMMER, K. 2004. Family Tyrannidae (Tyrant-flycatchers). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Cotingas to pipits and wagtails. Lynx Edicions, Barcelona, v.9, p. 170-463.). Thus, a species could be found in certain habitats within a forest whilst being rare, or even absent, in others. Fragmentation can negatively affect the availability of those habitats for most specialized species, decreasing the chances of their survival in forest fragments (Uezu & Metzger 2011UEZU, A. & METZGER, J.P. 2011. Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers. Conserv. 20:3627-3643. 10.1007/s10531-011-0154-5.
https://doi.org/10.1007/s10531-011-0154-...
). Therefore, habitat-specialist species may have their survival compromised due to the loss or alteration of vegetation heterogeneity (Cerqueira et al. 2003CERQUEIRA, R., BRANT, A., NASCIMENTO, M.T. & PARDINI, R. 2003. Fragmentação: alguns conceitos. In Fragmentação de ecossistemas: causas efeitos sobre a biodiversidade e recomendações de políticas públicas (Rambalsi, D.M. & Oliveira, D.A.S. eds). MMA/SBF, Brasília.). However, the chances to persist in forest fragments should be higher in habitat-generalists.

In this study we evaluated the type of spatial distribution of forest suboscine birds in a reserve of southern Brazil, the Parque Estadual Mata dos Godoy (PEMG). The principal microhabitat features of some suboscine species in PEMG have already been described (Poletto et al. 2004POLETTO, F., ANJOS, L., LOPES, E.V., VOLPATO, G.H., SERAFINI, P.P. & FAVARO, F.L. 2004. Caracterização do microhabitat e vulnerabilidade de cinco espécies de arapaçus (Aves: Dendrocolaptidae) em um fragmento florestal do norte do estado do Paraná, sul do Brasil. Ararajuba. 12(2):89-96., Lopes et al. 2006LOPES, E.V., VOLPATO, G.H., MENDONÇA, L.B., FÁVARO, F.L. & ANJOS, L. 2006. Abundância, microhabitat e repartição ecológica de papa-formigas (Passeriformes, Thamnophilidae) na bacia hidrográfica do rio Tibagi, Paraná, Brasil. Rev. Bras. Zool. 23(2):395-403. 10.1590/S0101-81752006000200013.
https://doi.org/10.1590/S0101-8175200600...
, Volpato et al. 2006VOLPATO, G.H., ANJOS, L., POLETTO, F., SERAFINI, P.P., LOPES, E.V. & FÁVARO, F.L. 2006. Terrestrial passerines in an Atlantic Forest remnant of Southern Brazil. Braz. J. Biol. 66(2A):473-478. 10.1590/S1519-69842006000300013.
https://doi.org/10.1590/S1519-6984200600...
). Here we associated a homogeneous spatial distribution to habitat-generalist species, meaning that they could survive in larger spectrum of biotic and abiotic conditions within the forest. By contrast, species with heterogeneous spatial distribution were considered habitat-specialist, which indicates that they could not support a larger spectrum of environmental variations. We hypothesized that habitat-generalist suboscines are less sensitive to forest fragmentation than the habitat-specialists. The study was carried out in northern Paraná, where the sensitivity of species to forest fragmentation has been previously determined for several species (Anjos 2006ANJOS, L. 2006. Bird species sensitivity in a fragmented landscape of the Atlantic Forest Southern Brazil. Biotropica 32(2):229-234. 10.1111/j.1744-7429.2006.00122.x.
https://doi.org/10.1111/j.1744-7429.2006...
). We considered firstly all species of suboscines together and secondly according their general feeding habits (canopy, subcanopy or climber). Additionally, we evaluated variations in the composition of the bird assemblies in the PEMG.

Material and methods

1. Study area

The study was conducted in Parque Estadual Mata dos Godoy (PEMG) (23°27′ S, 51°15′ W, 656 ha) located 15 km south of Londrina, Paraná, in southern Brazil. It is characterized as an important conservation area of northern Paraná. According to Anjos et al. (2009)ANJOS, L., BOCHIO, G.M., CAMPOS, J.V., MCCRATE, G.B. & PALOMINO, F. 2009. Sobre o uso de níveis de sensibilidade de aves è fragmentação florestal na avaliação da Integridade Biótica: um estudo de caso no norte do Estado do Paraná, sul do Brasil. Rev. Bras. Ornitol. 17(1):28-36., it has a high value of Biotic Integrity (0,85), with a high bird species richness (114 species) compared to other southern Brazil fragments, especially in light of the vegetation heterogeneity resulting from topographical variation between the north and south of the park (the top of the slope to the valley bottom, see Santana & Anjos 2010SANTANA, C.R. & ANJOS, L. 2010. Associação de aves a agrupamentos de bambu na porção sul da Mata Atlântica, Londrina, Estado do Paraná, Brasil. Biota. Neotrop. 10(2): http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn00510022010ISSN 1676-0603 (last access on 21/05/2013).
http://www.biotaneotropica.org.br/v10n2/...
). In this study,Anjos et al. (2009)ANJOS, L., BOCHIO, G.M., CAMPOS, J.V., MCCRATE, G.B. & PALOMINO, F. 2009. Sobre o uso de níveis de sensibilidade de aves è fragmentação florestal na avaliação da Integridade Biótica: um estudo de caso no norte do Estado do Paraná, sul do Brasil. Rev. Bras. Ornitol. 17(1):28-36. determined an Index of Biotic Integrity (IBI) in 39 forest fragments in the north of Paraná State, southern Brazil, based on presence and absence of 30 selected bird species of different sensitivity levels to forest fragmentation.

The northern region of the PEMG, a plateau at about 600 m altitude, has a dense, closed canopy between 12 m to 20 m where the most abundant tree species areCabraela canjerana (Meliaceae), Euterpes edulis (Arecaceae), Ocotea indecora (Lauraceae) and Nectandra megapotamica (Lauraceae) (Torezan & Silveira 2002TOREZAN, J.M.D. & SILVEIRA, M. 2002. Fatores ambientais, diversidade e similaridade em florestas da bacia do rio Tibagi. In A bacia do rio Tibagi. (Medri, M.E., Bianchini, E., Shibata, O.A. & Pimenta, J.A. eds). Edição dos Autores, Londrina., Anjos et al. 2007ANJOS, L., VOLPATO, G.H., LOPES, E.V., SERAFINI, P.P., POLETTO, F. & ALEIXO, A. 2007. The importance of riparian forest for the maintenance of bird species richness in an Atlantic Forest remnant, southern Brazil. Rev. Bras. Zool. 24(4):1078-1086. 10.1590/S0101-81752007000400027.
https://doi.org/10.1590/S0101-8175200700...
). Because of the dense canopy, the midstory and understory receives little light, and the understory is relatively open, with short trees and bushes such as Eugenia verrucosa(Myrtaceae), Sorocea bonplandii (Moraceae),Miconiatritis (Melastomataceae), Marantasp. (Marantaceae) and Piper sp. (Piperaceae) (Torezan & Silveira 2002TOREZAN, J.M.D. & SILVEIRA, M. 2002. Fatores ambientais, diversidade e similaridade em florestas da bacia do rio Tibagi. In A bacia do rio Tibagi. (Medri, M.E., Bianchini, E., Shibata, O.A. & Pimenta, J.A. eds). Edição dos Autores, Londrina., Anjos et al. 2007ANJOS, L., VOLPATO, G.H., LOPES, E.V., SERAFINI, P.P., POLETTO, F. & ALEIXO, A. 2007. The importance of riparian forest for the maintenance of bird species richness in an Atlantic Forest remnant, southern Brazil. Rev. Bras. Zool. 24(4):1078-1086. 10.1590/S0101-81752007000400027.
https://doi.org/10.1590/S0101-8175200700...
). The southern portion consists of a sloped area (600 - 470 m) ending in a floodplain of the Apertados river, the southern boundary of the Park. The canopy is less compact, with the largest trees sparsely distributed, including Chrysophyllum gonocarpum (Sapotaceae), Campomanesia xanthocarpa(Myrtaceae) and Parapiptadenia rigida (Fabaceae). The midstory, however, has a higher density of smaller tree species, such as Nectandra megapotamica (Lauraceae), Alseis floribunda(Rubiaceae), Matayba elaeagnoides (Sapindaceae),Lonchocarpus muehlbergianus (Fabaceae), Sebastiana commersoniana (Euphorbiaceae), Eugenia verrucosa(Myrtaceae) and Trichilia cassaretti (Meliaceae) (Anjos et al. 2007ANJOS, L., VOLPATO, G.H., LOPES, E.V., SERAFINI, P.P., POLETTO, F. & ALEIXO, A. 2007. The importance of riparian forest for the maintenance of bird species richness in an Atlantic Forest remnant, southern Brazil. Rev. Bras. Zool. 24(4):1078-1086. 10.1590/S0101-81752007000400027.
https://doi.org/10.1590/S0101-8175200700...
, Santana & Anjos 2010SANTANA, C.R. & ANJOS, L. 2010. Associação de aves a agrupamentos de bambu na porção sul da Mata Atlântica, Londrina, Estado do Paraná, Brasil. Biota. Neotrop. 10(2): http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn00510022010ISSN 1676-0603 (last access on 21/05/2013).
http://www.biotaneotropica.org.br/v10n2/...
). It is common the fall of the tallest trees in this region, resulting in clearings dominated by the herbaceousCeltis iguanaea (Ulmaceae) and bambooChusquea sp. (Poaceae) (Silveira 2006SILVEIRA, M. 2006. A vegetação do Parque Estadual Mata dos Godoy. In Ecologia do Parque Estadual Mata dos Godoy. (Torezan, J.M.D. Org). Itedes, Londrina, p. 19-27., Anjos et al. 2007ANJOS, L., VOLPATO, G.H., LOPES, E.V., SERAFINI, P.P., POLETTO, F. & ALEIXO, A. 2007. The importance of riparian forest for the maintenance of bird species richness in an Atlantic Forest remnant, southern Brazil. Rev. Bras. Zool. 24(4):1078-1086. 10.1590/S0101-81752007000400027.
https://doi.org/10.1590/S0101-8175200700...
, Santana & Anjos 2010SANTANA, C.R. & ANJOS, L. 2010. Associação de aves a agrupamentos de bambu na porção sul da Mata Atlântica, Londrina, Estado do Paraná, Brasil. Biota. Neotrop. 10(2): http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn00510022010ISSN 1676-0603 (last access on 21/05/2013).
http://www.biotaneotropica.org.br/v10n2/...
). The edge of the park is characterized by a riparian forest floodplain which has little representation of the coverage in the PEMG;Bastardiopsis densiflora (Malvaceae) and Ocotea puberula (Lauraceae) are examples of trees that make up the vegetation in this portion of the Park (Silveira 2006SILVEIRA, M. 2006. A vegetação do Parque Estadual Mata dos Godoy. In Ecologia do Parque Estadual Mata dos Godoy. (Torezan, J.M.D. Org). Itedes, Londrina, p. 19-27.).

2. Field work

Point counts of limited distance were sampled (always by the same observer) along three trails. Each trail has 1300 m length. Two trails were in the upland forest (TA and TB) and the third on the sloped forest in the southern area (TC). On each trail, 14 points were established every 100 m and numbered in sequence (one to 14, Figure 1). Field sampling was obtained at each point and conducted from October to December 2011, beginning at sunrise. The radius of detection from each point was 50 m. On each day, the trails were walked twice in opposite directions. The point samplings in a day were considered as one sample. The starting point of each trail sample was alternated each day, offering the same odds of detection for all species. The sampling period at each point was 5 minutes, thus it lasted for about four hours. At each point, only the presence of the species was registered.

Figure 1
Location of sampling points in each of the three trails sampled in Parque Esta dual Mata dos Godoy, Londrina, Brazil. The dotted line indicates the division by altitude of the two types of forest in the Park.

3. Vegetation characterization

In order to evaluate whether the features of vegetation differ between the trails, general data on phyto-physiognomy were obtained at each point (36 points in total), by sampling at 25 m from each point along the trail and at 10 m from each side of the trail. Our sampled area for each point resulted in 1000 m2 (Figure 2). The vegetation variables that we collected were: number of large trees (height greater than 15 m), number of palmettos (only Euterpe edulisoccurs in PEMG, height greater than 4 m) and herbaceous, liana and bamboo densities. The densities were estimated according to the proportion of the sample area occupied using the following scale: absent (0); to 40% (1); between 40-60% (2); between 60-80% (3) and up to 100% (4). The sum of the percentages of herbaceous, liana and bamboo did not resulted in 100% because they were estimated independently. Our procedure was to estimate the area occupied for each of these three vegetation types.

Figure 2
Schematic diagram of the sampling points (P1 and P2) and the sampled area in which the vegetation was characterized.

4. Procedure for analysis

Levels of sensitivity to forest fragmentation of each bird species were based onAnjos (2006)ANJOS, L. 2006. Bird species sensitivity in a fragmented landscape of the Atlantic Forest Southern Brazil. Biotropica 32(2):229-234. 10.1111/j.1744-7429.2006.00122.x.
https://doi.org/10.1111/j.1744-7429.2006...
, which determined the sensitivity of bird species to fragmentation based on point counts conducted in 14 forest fragments of different sizes and degrees of isolation in northern Paraná. Species were considered highly sensitive if they occurred only in the controls and in large and not-isolated forest remnants; species with low sensitivity were those occurring in all categories of the forest remnants, including those smaller and more isolated (Anjos 2006ANJOS, L. 2006. Bird species sensitivity in a fragmented landscape of the Atlantic Forest Southern Brazil. Biotropica 32(2):229-234. 10.1111/j.1744-7429.2006.00122.x.
https://doi.org/10.1111/j.1744-7429.2006...
). We considered the bird list of species of Anjos et al. (1997)ANJOS, L., SCHUCHMANN, K.L., BERNDT, R. 1997. Avifaunal composition, species richness, and status in the Tibagi river basin, Paraná State, southern Brazil. Ornitol. Neotrop. 8(2): 145-173. to select the suboscines that occur in PEMG. We allocated each species to groups based on foraging habits, according to Remsen 2003, Marantz et al. 2003MARANTZ, C., ALEIXO, A., BEVIER, L. & PATTEN, M. 2003. Family Dendrocolaptidae (Woodcreepers). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions, Barcelona, v.8, p. 358-447., Zimmer & Isler 2003ZIMMER, M. & ISLER, M. 2003. Family Thamnophilidae (Typical Antbirds). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions, Barcelona, v.8, p. 448-681., Krabbe & Schulenberg 2003KRABBE, N. & SCHULENBERG, T. 2003. Family Formicariidae (Ground-antbirds). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions. Barcelona, v.8, p. 682-731., Whitney 2003WHITNEY, B. 2003. Family Conopophagidae (Gnateaters). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions. Barcelona, v.8, p. 732-745., Krabbe & Schulenberg 2003KRABBE, N. & SCHULENBERG, T. 2003. Family Formicariidae (Ground-antbirds). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Broadbills to tapaculos. Lynx Edicions. Barcelona, v.8, p. 682-731., Snow 2004SNOW, D. 2004. Family Pipridae (Manakins). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. ). Cotingas to pipits and wagtails. Lynx Edicions, Barcelona, v.9, p. 110-169., Fitzpatrick et al. 2004FITZPATRICK, J., BATES, J., BOSTWICK, K., CABALLERO, I., CLOCK, B., FARNSWORTH, A., HOSNER, P., JOSEPH, L., LANGHAM, G., LEBBIN, D., MOBLEY, J., ROBBINS, M., SCHOLES, E., TELLO, J., WALTHER, B. & ZIMMER, K. 2004. Family Tyrannidae (Tyrant-flycatchers). In Handbook of birds of the world (del Hoyo, J., Elliot, A. & Sargatal, J. eds). Cotingas to pipits and wagtails. Lynx Edicions, Barcelona, v.9, p. 170-463.. The groups were: (1) canopy species, (2) subcanopy species, including species that frequent the ground and (3) climber species. We considered these distinct groups of species because they seem to present different levels of sensitivity to forest fragmentation. Subcanopy species seem to be more sensitive than canopy ones, while climbers seem to have intermediate sensitivity levels (Aleixo & Vielliard 1995ALEIXO, A. & VIELLIARD, J.M.E.1995. Composição e dinâmica da comunidade de aves da Mata de Santa Genebra, Campinas, SP. Rev. Bras. Zool. 12(3):493-511., Anjos & Soares 1999ANJOS, L., SOARES, E.S. 1999. Efeito da fragmentacão florestal sobre aves escaladoras de tronco e galho na região de Londrina, norte do Estado do Paraná, Brasil. Ornitol. Neotrop. 10:61-68., Ribon et al. 2003RIBON, R., SIMON, J.E. & MATTOS, G.T. 2003. Bird extinctions in Atlantic forest fragments of Viçosa region, southeastern Brazil. Conserv. Biol. 17(6):1827-1839. 10.1111/j.1523-1739.2003.00377.x.
https://doi.org/10.1111/j.1523-1739.2003...
, Uezu & Metzger 2011UEZU, A. & METZGER, J.P. 2011. Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers. Conserv. 20:3627-3643. 10.1007/s10531-011-0154-5.
https://doi.org/10.1007/s10531-011-0154-...
).

5. Statistics and additional comments

Kruskal Wallis analysis of variance was used to compare the variation in the number of trees and palmettos between trails studied (TA, TB and TC). For the remaining vegetation variables (density of vines, bamboo and herbaceous) it was used a contingency table (p < 0.05) to test whether the proportion of variables is similar in the three trails. This analyze was made by comparing the number of sampled areas wherein each vegetation variable was estimated according to the occupancy scale, in other words the number of sampled areas in each percentage range for each trail.

To evaluate whether bird species are habitat-generalist or habitat-specialist in PEMG we calculated the percentage of points that were occupied. To do this, we associated a homogeneous spatial distribution to habitat-generalist species, which would tend to be less sensitive to forest fragmentation. In contrast, we associated a heterogeneous spatial distribution to habitat-specialist species, which would tend to be more sensitive to forest fragmentation. Therefore, if a species was recorded at 4 points out of a total of 32 points from the trails, it would give us a percentage of 13% of occupancy. If another species was recorded at 28 points it would result in a percentage of 88% of occupancy. This way, we determined that species with an occupancy percentage equal and below 30% were habitat-specialists and those above that value were habitat-generalist. In the first example the species would be habitat-specialist and in the second, habitat-generalist. The value of 30% was arbitrary selected. We know that detectability differs between the species, as has already been considered for some birds of the PEMG (Bochio et al. 2012BOCHIO, G.M., ANJOS, L. 2012. The Importance of Considering Bird Detectability for Assessing Biological Integrity. Nat. Conservação 10:72-76. 10.4322/natcon.2012.012.
https://doi.org/10.4322/natcon.2012.012...
). We countered this by sampling each point 12 times on 12 different days, making the possibility that a species was present but not recorded very low.

We evaluated the association between spatial distribution and the levels of sensitivity in the trails separately. As explained above, the distinction between homogenous and heterogeneous spatial distribution was based in the occupancy of the points; an occupancy equal and below 30% were of heterogeneous spatial distribution (habitat-specialists) and those above that value were of homogenous spatial distribution (habitat-generalist). Contingency table (p < 0.05) was used to verify whether the spatial distribution (homogeneous and heterogeneous) was associated with sensitivity levels of suboscine species (sensitive and non-sensitive) or with foraging habits groups. All analyses were carried out using the software R.

Nonmetric multidimensional scaling (NMDS) was also used to examine the distribution of bird assemblies in the PEMG. For data analysis, the data were standardized and square-root transformed to reduce the effect of the most strongly represented species. For this data analysis, the relative frequency of each species at each point was used. Therefore, if a species was recorded 3 times out of 12 times a point was sampled, it had a frequency of occurrence of 40%. This analysis was carried out using the software PRIMER 6.1.13 (Clarke & Gorley 2006CLARKE, K.R. & GORLEY, R.N. 2006. Primer v6: user manual/tutorial. PRIMER-E. Plymouth.).

The sequence of species follows the checklist of the American Ornithologists’ Union (2013)AMERICAN ORNITHOLOGISTS’ UNION. 2013. Check-list of South American Birds. [Cited 20 May 2013.] Available from URL: http://www.museum.lsu.edu/˜Remsen/SACCBaseline.html (last access on 20/05/2013).
http://www.museum.lsu.edu/˜Remsen/SACCBa...
.

Results

The number of large trees and palmettos and the densities of herbaceous plants were not significantly different among the studied trails (Tables 1, 2). However, higher density of bamboo was found on TC (G = 26.25, p = 0.001), while TA and TB had a higher density of vines (G = 16.28, p = 0.01).

Table 1
Mean (X) and standard deviation (S) of vegetation variables in each trail. P indicates the significance between the values of the variables between trails. (Kruskal Wallis).

Table 2
Total sampled areas wherein each vegetation variable was estimated according to the following occupancy scale: absent (0); to 40%; (1) between 40-60% (2); between 60-80% (3) and up to 100% (4).P value indicates the significance between trails. (G-test).

A total of 43 different suboscine birds were recorded; 36 species were seen in the northern and 40 in the southern portion of the PEMG. The numbers of species observed on each trail were: 34 species in TA, 32 species in TB and 40 in TC. For each trail there were (respectively on TA, TB and TC) 15, 13 and 13 species with a heterogeneous spatial distribution (habitat-specialists), and 19, 19 and 27 with a homogeneous spatial distribution (habitat-generalist). Overall, of the 43 species recorded in the present study, 21 were considered to have high sensitivity and 22 to have low sensitivity to forest fragmentation, following the literature cited above (see methods; Table 3). Among the high sensitivity species, 17, 16 and 19 species were found respectively on TA, TB and TC, whereas for species with low sensitivity, 18 were observed on TA, 16 on TB and 21 on TC.

Table 3
Species sampled, divided according to levels of sensitivity to forest fragmentation in accordance with Anjos (2006)ANJOS, L. 2006. Bird species sensitivity in a fragmented landscape of the Atlantic Forest Southern Brazil. Biotropica 32(2):229-234. 10.1111/j.1744-7429.2006.00122.x.
https://doi.org/10.1111/j.1744-7429.2006...
, foraging habits (FH) and frequency of occurrence (FO) in trails (TA, TB and TC). The species frequency of occurrence with heterogeneous distribution is shown in bold. The foraging habits are: subcanopy (SC), climber (CL) and canopy (CP). Species are in systematic and phylogenetic position following nomenclature of the South American Classification Committee of the American Ornithologists' Union (2013).

There was no association between levels of sensitivity to forest fragmentation and spatial distribution of suboscine birds when the whole PEMG was considered (G = 0.02, p = 0.87). Significance was only found in the group of subcanopy suboscine birds when TA and TB were considered separately (G = 6.96, p = 0.008 and G = 4.41, p = 0.03 respectively; Table 4). Subcanopy suboscine birds showed a significant association between homogeneous spatial distribution (habitat-generalists) and low sensitivity to forest fragmentation. Canopy and climber suboscine birds did not exhibit significant association in any situation.

Table 4
The number of species according to sensitivity degree of forest fragmentation and spatial distribution category, homogeneous and heterogeneous, considering the foraging habits and the three sampled trails (TA, TB and TC) in Parque Estadual Mata do Godoy.

The nonmetric multidimensional scaling (NMDS) ordination revealed three distinct groups of bird species. One group is composed of species that preferentially occupy the northern portion, another of species that occupy the southern portion, while the third group consists of species that occupy the transition region between the northern and southern portions of the PEMG (Figure 3).

Figure 3
Nonmetric multidimensional scaling (NMDS) representing the profile similarity of sampling points according to the occupancy patterns of suboscine bird species sampled in Parque Estadual Mata dos Godoy.

Discussion

We found an unexpectedly high number of suboscine birds with homogenous spatial distribution, which would suggest the majority of them could be considered habitat-generalists. This could mean that the studied suboscine birds are not closely associated to microhabitats as previously thought. In addition, contrary to our expectations, spatial distribution was not associated with level of sensitivity to forest fragmentation when all species of suboscine birds were considered together. This association was only found for the subcanopy suboscine birds and even then, only in the northern portion of the PEMG. These results should be considered carefully however, since it is possible that the area of forest sampled may not have been large enough to properly detect variations in habitat occupancy.

Subcanopy suboscine birds, or understory birds in general, have been seen as one of the more vulnerable groups to forest fragmentation (Willis 1979WILLIS, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia 33:1-25., Kattan 1994KATTAN, G.H., ALVAREZ-L=PEZ, H. & GIRALDO, M. 1994. Forest fragmentation and Bird extinctions: San Antonio eighty years later. Conserv. Bio. l8(1):138-146. 10.1046/j.1523-1739.1994.08010138.x.
https://doi.org/10.1046/j.1523-1739.1994...
, Aleixo & Vielliard 1995ALEIXO, A. & VIELLIARD, J.M.E.1995. Composição e dinâmica da comunidade de aves da Mata de Santa Genebra, Campinas, SP. Rev. Bras. Zool. 12(3):493-511., Stouffer & Bierregaard 1995STOUFFER, P.C. & BIERREGAARD, R.O. 1995. Use of Amazonian forest fragments by understory insectivorous birds. Ecology 76(8):2429-2445., Bierregaard & Stouffer 1997BIERREGAARD, R.O. & STOUFFER, P C. 1997. Understory birds and dynamic habitat mosaics in Amazoniam rainforests. In Tropical forest remnants: ecology, management, and conservation of fragmented communities (Laurance,W.F. & Bierregaard, R.O. eds). The University of Chicago Press, Chicago., Goerck 1997GOERCK, J.M. 1997. Patterns of Rarity in the Birds of the Atlantic Forest of Brazil. Conserv. Biol. 11(1):112-118. 10.1046/j.1523-1739.1997.95314.x.
https://doi.org/10.1046/j.1523-1739.1997...
, Aleixo 1999ALEIXO, A. 1999. Effects of selective logging on a bird community in the Brazilian Atlantic forest. Condor 101:537-548., Stratford & Stouffer 1999BIERREGAARD, R.O. & STOUFFER, P C. 1997. Understory birds and dynamic habitat mosaics in Amazoniam rainforests. In Tropical forest remnants: ecology, management, and conservation of fragmented communities (Laurance,W.F. & Bierregaard, R.O. eds). The University of Chicago Press, Chicago., Ribon et al. 2003RIBON, R., SIMON, J.E. & MATTOS, G.T. 2003. Bird extinctions in Atlantic forest fragments of Viçosa region, southeastern Brazil. Conserv. Biol. 17(6):1827-1839. 10.1111/j.1523-1739.2003.00377.x.
https://doi.org/10.1111/j.1523-1739.2003...
, Henle et al. 2004HENLE, K., DAVIES, K.F., KLEYER, M., MARGULES, C. & SETTELE, J. 2004. Predictors of species sensitivity to fragmentation. Bio. Divers. Conserv. 13:207-251. 10.1023/B:BIOC.0000004319.91643.9e.
https://doi.org/10.1023/B:BIOC.000000431...
, Lees & Peres 2008LEES, A.C. & PERES, C.A. 2008. Avian life-history determinants of local extinction risk in a hyper-fragmented neotropical forest landscape. Anim. Conserv. 11(2):128-137. 10.1111/j.1469-1795.2008.00162.x.
https://doi.org/10.1111/j.1469-1795.2008...
, Uezu & Metzger, 2011UEZU, A. & METZGER, J.P. 2011. Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers. Conserv. 20:3627-3643. 10.1007/s10531-011-0154-5.
https://doi.org/10.1007/s10531-011-0154-...
). Their habitat specialization is thought to be the reason for such higher vulnerability (Stratford & Stouffer 1999STRATFORD, J.A. & STOUFFER, P.C. 1999. Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conserv. Biol. 13(6):1416-1423. 10.1046/j.1523-1739.1999.98494.x.
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, Hansbauer et al. 2008aHANSBAUER, M.M., STORCH, I., PIMENTEL, R.G. & METZGER, J.P. 2008a. Comparative range use by three Atlantic Forest understorey bird species in relation to forest fragmentation. J. Trop. Ecol. 24(3):291-299. 10.1017/S0266467408005002.
https://doi.org/10.1017/S026646740800500...
, 2010HANSBAUER, M.M., VEGVÁRI, Z., STORCH, I., BORNTRAEGER, R., HETTICH, U., PIMENTEL, R.G. & METZGER, J.P. 2010. Microhabitat Selection of three Forest Understory Birds in the Brazilian Atlantic Rainforest. Biotropica 42(3):355-362. 10.1111/j.1744-7429.2009.00593.x.
https://doi.org/10.1111/j.1744-7429.2009...
, Sodhi et al. 2011SODHI, N.S., SEKERCIOGLU, C.H., BARLOW, J. & ROBINSON, S.K. 2011. Conservation of Tropical Birds. Wiley-Blackwell, Oxford.), which seems to be corroborated by the data presented here.

Some studies claim that species of suboscine birds found on trunks and twigs, which we referred to as climbers in the present study, can be considered sensitive to even slight changes in the structure of vegetation (Willis 1979WILLIS, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia 33:1-25., Aleixo & Vielliard 1995ALEIXO, A. & VIELLIARD, J.M.E.1995. Composição e dinâmica da comunidade de aves da Mata de Santa Genebra, Campinas, SP. Rev. Bras. Zool. 12(3):493-511., Christiansen & Pitter 1997CHRISTIANSEN, M.M. & PITTER, E. 1997. Species loss in a forest bird community near Lagoa Santa in Southeastern Brazil. Biol. Conserv 80(1):23-32. 10.1016/S0006-3207(96)00073-0.
https://doi.org/10.1016/S0006-3207(96)00...
, Anjos 1998ANJOS, L. 1998. Consequências biológicas da fragmentação no Norte do Paraná. Série. técnica. IPEF 12(32):87-94., Poletto et al. 2004POLETTO, F., ANJOS, L., LOPES, E.V., VOLPATO, G.H., SERAFINI, P.P. & FAVARO, F.L. 2004. Caracterização do microhabitat e vulnerabilidade de cinco espécies de arapaçus (Aves: Dendrocolaptidae) em um fragmento florestal do norte do estado do Paraná, sul do Brasil. Ararajuba. 12(2):89-96.). Authors tentatively described the microhabitat of those birds, especially species of Dendrocolaptidae (Cintra et al. 2006CINTRA, R., MARUOKA, A.E. & NAKA, L.N. 2006. Abundance of two Dendrocincla woodcreepers in relation to forest structure in Central Amazonia. Acta. Amazônica. 36(2):209-219. 10.1590/S0044-59672006000200011.
https://doi.org/10.1590/S0044-5967200600...
, Poletto et al. 2004POLETTO, F., ANJOS, L., LOPES, E.V., VOLPATO, G.H., SERAFINI, P.P. & FAVARO, F.L. 2004. Caracterização do microhabitat e vulnerabilidade de cinco espécies de arapaçus (Aves: Dendrocolaptidae) em um fragmento florestal do norte do estado do Paraná, sul do Brasil. Ararajuba. 12(2):89-96.). However, the results of this study suggest that the reason for climbers being sensitive to forest fragmentation is not closely associated with the microhabitat specialization. Possibly their sensitivity could be the result of variations in vegetation structure at broader scales. According to Poletto et al. (2004)POLETTO, F., ANJOS, L., LOPES, E.V., VOLPATO, G.H., SERAFINI, P.P. & FAVARO, F.L. 2004. Caracterização do microhabitat e vulnerabilidade de cinco espécies de arapaçus (Aves: Dendrocolaptidae) em um fragmento florestal do norte do estado do Paraná, sul do Brasil. Ararajuba. 12(2):89-96., Dendrocolaptidae with stricter ecological requirements may relate with other vegetation features, selecting fairly homogeneous sites at late successional stages, such as Dendrocincla turdina, or even areas with tangled vegetation and rough bark large trees as Xiphocolaptes albicollis.

Canopy suboscine birds, in turn, do not appear to be associated with microhabitats. The canopy birds are adapted to move long distances seeking resources distributed unevenly in the canopy (Karr & James 1975KARR, R. & JAMES, F.C. 1975. Eco-morphological configurations and convergent evolution in species and communities. In Ecology and Evolution of Communities. (Cody, M.L. & Diamond, J.M. eds). Harvard University Press. Cambridge., Winkler & Preleuthner 2001WINKLER, H. & PRELEUTHNER, M. 2001. Behaviour and ecology of birds in tropical rain forest canopies. Plant. Ecol. 153:193-202. 10.1023/A:1017595321548.
https://doi.org/10.1023/A:1017595321548...
). Probably the broad potential of habitat occupancy (homogeneous spatial distribution) contributed to their low sensitivity to forest fragmentation (e.g. Karr 1982KARR, JR. 1982. Avian Extinction on Barro Colorado Island, Panama: A Reassessment. Am. Nat. 119(2):220-239. 10.1086/283904.
https://doi.org/10.1086/283904...
, Ribon et al. 2003RIBON, R., SIMON, J.E. & MATTOS, G.T. 2003. Bird extinctions in Atlantic forest fragments of Viçosa region, southeastern Brazil. Conserv. Biol. 17(6):1827-1839. 10.1111/j.1523-1739.2003.00377.x.
https://doi.org/10.1111/j.1523-1739.2003...
, Uezu & Metzger 2011UEZU, A. & METZGER, J.P. 2011. Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers. Conserv. 20:3627-3643. 10.1007/s10531-011-0154-5.
https://doi.org/10.1007/s10531-011-0154-...
).

The results found in the analysis of structural variation of the vegetation showed that PEMG can be differentiated according to the structure of understory vegetation, with it being subdivided into areas occupied predominantly by bamboos or vines. Large densities of bamboos were found only in the southern portion of the park (Silveira 2006SILVEIRA, M. 2006. A vegetação do Parque Estadual Mata dos Godoy. In Ecologia do Parque Estadual Mata dos Godoy. (Torezan, J.M.D. Org). Itedes, Londrina, p. 19-27., Santana & Anjos 2010SANTANA, C.R. & ANJOS, L. 2010. Associação de aves a agrupamentos de bambu na porção sul da Mata Atlântica, Londrina, Estado do Paraná, Brasil. Biota. Neotrop. 10(2): http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn00510022010ISSN 1676-0603 (last access on 21/05/2013).
http://www.biotaneotropica.org.br/v10n2/...
). The bamboo clusters that make up the southern portion of the Atlantic Forest often occupy gaps and areas of secondary growth, especially in riparian forest or hills, where they have an aggregate distribution, forming a dense environment with a lower stratum of anatomically similar leaves (Kratter 1997KRATTER, A.W. 1997. Bamboo specialization by Amazonian birds. Biotropica 29(1):100-110., Santana & Anjos 2010SANTANA, C.R. & ANJOS, L. 2010. Associação de aves a agrupamentos de bambu na porção sul da Mata Atlântica, Londrina, Estado do Paraná, Brasil. Biota. Neotrop. 10(2): http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn00510022010ISSN 1676-0603 (last access on 21/05/2013).
http://www.biotaneotropica.org.br/v10n2/...
). Contrary to clusters of bamboo, vine tangles were found predominantly in the northern portion of the park. According to Kratter (1997)KRATTER, A.W. 1997. Bamboo specialization by Amazonian birds. Biotropica 29(1):100-110., vine tangles are probably the most physiognomic similar microhabitat to clusters of bamboo, providing habitat and food source for many organisms (Schnitzer & Bongers 2002SCHNITZER, S.A. & BONGERS, F. 2002. The ecology of lianas and their role in forests. Trends. Ecol. Evol. 17(1):223-230. 10.1016/S0169-5347(02)02491-6.
https://doi.org/10.1016/S0169-5347(02)02...
, Thomsen et al. 2010THOMSEN, M.S., WERNBERG, T., ALTIERI, A., TUYA, F., GULBRANSEN, D., MCGLATHERY, K.J., HOLMER, M. & SILLIMAN, B.R. 2010. Habitat Cascades: The Conceptual Context and Global Relevance of Facilitation Cascades via Habitat Formation and Modification. Integr. Compe. Biol. 50(2):158-175. 10.1093/icb/icq042.
https://doi.org/10.1093/icb/icq042...
). Data presented here (Table 3 and figure 3) revealed differences between the pattern of occupancy of the suboscine birds species between the areas occupied by bamboos and vines, which seems to disagree with the interpretations of Kratter (1997)KRATTER, A.W. 1997. Bamboo specialization by Amazonian birds. Biotropica 29(1):100-110..

In the present study we found a weak relationship between spatial distribution (habitat specialization) and sensitivity to forest fragmentation. But our data suggested that suboscine birds occupied differently the northern and the southern portions of PEMG. Indeed, higher species numbers that have been considered as habitat-specialists were more common in the bird assembly of the northern portion of PEMG. The northern portion of the PEMG is the first type of terrain in a landscape to be converted into agriculture and should be considered as the most vulnerable area of that reserve. Many studies have evaluated effects of forest fragmentation comparing fragments of different sizes and levels of connectivity (e.g. Uezu et al. 2005UEZU, A., METZGER, J.P. & VIELLIARD, J.M.E. 2005. Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol. Conserv. 123:507-519. 10.1016/j.biocon.2005.01.001.
https://doi.org/10.1016/j.biocon.2005.01...
, Hansbauer et al. 2008aHANSBAUER, M.M., STORCH, I., PIMENTEL, R.G. & METZGER, J.P. 2008a. Comparative range use by three Atlantic Forest understorey bird species in relation to forest fragmentation. J. Trop. Ecol. 24(3):291-299. 10.1017/S0266467408005002.
https://doi.org/10.1017/S026646740800500...
,2008bHANSBAUER, M.M., STORCH, I., LEU, S., NIETO-HOLGUIN, J.P., PIMENTEL, R.G., KNAUER, F. & METZGER, J.P. 2008b. Movements of neotropical understory passerines affected by anthropogenic forest edges in the Brazilian Atlantic rainforest. Biol. Conserv. 141:782-791. 10.1016/j.biocon.2008.01.002.
https://doi.org/10.1016/j.biocon.2008.01...
, Gillies & Clair 2010GILLIES, C.S. & ST CL.A.I.R., C.C. 2010. Functional responses in habitat selection by tropical birds moving through fragmented forest. J. App. Ecol. 47(1):182-190. 10.1111/j.1365-2664.2009.01756.x.
https://doi.org/10.1111/j.1365-2664.2009...
). But variations in the vegetation inside the forest fragment should be also considered in such studies (Hansbauer et al. 2010HANSBAUER, M.M., VEGVÁRI, Z., STORCH, I., BORNTRAEGER, R., HETTICH, U., PIMENTEL, R.G. & METZGER, J.P. 2010. Microhabitat Selection of three Forest Understory Birds in the Brazilian Atlantic Rainforest. Biotropica 42(3):355-362. 10.1111/j.1744-7429.2009.00593.x.
https://doi.org/10.1111/j.1744-7429.2009...
), as in the case of the PEMG.

We thank Erivelto Goulart, Mario Luís Orsi, and Sandra Maria Hartz for revising a previous version of the manuscript, the Universidade Estadual de Londrina for logistical support and the InstitutoAmbiental do Paraná (252/10) for permission to conduct research in the Godoy State Park.

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Publication Dates

  • Publication in this collection
    Sept 2014

History

  • Received
    05 Aug 2013
  • Reviewed
    03 Feb 2014
  • Accepted
    13 Aug 2014
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